Shark Populations in Marine Protected Areas in Raja Ampat

Running Head: SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT

DIVERSITY AND ABUNDANCE OF SHARKS IN NONO----TAKETAKE AND FISHED SITES IN THE MARINE PROTECTED AREA NETWORK OF RAJA AMPAT, WEST PAPUA, INDONESIA, USING BAITED REMOTE UNDERWATER VIDEO (BRUVs(BRUVs))))

ANGELA JUNE ELIZE BEER

B.Sc., Queen’s University, 2001 B.Ed., Lakehead University, 2003

A thesis submitted in partial fulfillment of the requirements for the degree of

MASTER OF SCIENCE in ENVIRONMENT AND MANAGEMENT

We accept this thesis as conforming to the required standard

...... Dr. Steven Lindfield, Thesis Supervisor University of Western Australia

...... Dr. Audrey Dallimore, Thesis Coordinator School of Environment and Sustainability

...... Dr. Chris Ling, Director School of Environment and Sustainability

ROYAL ROADS UNIVERSITY

February 2015

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 2

Abstract Sharks are essential elements for healthy marine ecosystems and require conservation. A new law has been passed for their protection in Raja Ampat, Indonesia, yet there is a lack of knowledge about their current status in the region. This research quantifies diversity and abundance of shark populations in two areas (Penemu and Dampier Straight) within Raja Ampat, and provides a comprehensive baseline for the areas to evaluate management strategies. Baited remote underwater video systems were used to survey shark populations in no-take and fished sites, across a 3 to 80 m depth gradient. Overall, nine species of sharks from five families were recorded; Carcharhinus melanopterus was the most abundant species. PERMANOVA analysis showed no statistical difference between areas nor zoning status; likely due to the relatively recent designation of the Marine Protected Areas (MPAs) and inconsistent management/enforcement. Greater shark abundance overall was recorded in Penemu than in

Dampier Strait, whereas Dampier exhibited greater diversity of species. Penemu also showed a greater difference in shark abundance between the fished and no-take zones, with more sharks in fishing-prohibited no-take zones. Over the depth gradient studied, there was an inverse trend for species richness and abundance, with the greatest shark abundance in shallow samples, whereas the greatest shark diversity was at depth. These results provide important knowledge on the distribution of these valuable, yet poorly understood, apex predators in Raja Ampat, West Papua.

Furthermore the findings and protocols developed in this study will benefit the management planning of the Raja Ampat MPA network .

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Table of Contents

Abstract ...... 2 Table of Contents ...... 3 List of Figures ...... 5 List of Tables ...... 5 Acknowledgements ...... 7 Introduction and Background...... 9 Sharks – Importance and Global Status ...... 9 Conservation in Raja Ampat ...... 10 MPAs and Shark Protection ...... 12 Raja Ampat Shark Sanctuary ...... 13 Studying Shark Populations – the use BRUVs ...... 14 Significance and Application of the Research ...... 15 Research Question and Objectives ...... 15 Research Questions ...... 15 Research Objectives ...... 15 Research Methodology ...... 16 Description of Study Areas ...... 16 Study Species ...... 19 Research Design and Sampling Strategy ...... 19 Sampling Technique and Equipment: Baited Remote Underwater Video (BRUVs) Systems21 BRUVs equipment setup and standardization...... 21 Data collection and standardization ...... 23 Data Analysis ...... 23 Video processing ...... 23 Statistical analysis ...... 24 Results ...... 26 Shark Diversity and Abundance ...... 26 Variation Between Area and Status ...... 27 Variation Between Depths ...... 30 Overall depth variation...... 30 Area-related depth variation...... 31 Status-related depth variation...... 32 Shark Population Assemblage Variation ...... 32 Species-related Variation in Depth ...... 36 Field Work Effort and Efficiency ...... 39 Discussion ...... 40 The Effectiveness of MPAs for Conservation of Shark Populations in Raja Ampat ...... 40 The Effect of Depth on Shark Abundance ...... 43 Shark Diversity Recorded in Raja Ampat ...... 45 Shark Assemblages in Raja Ampat ...... 49 Significance of the Research and Implication for Conservation Efforts ...... 51 Lessons and Recommendations for Studying Shark Populations in Raja Ampat ...... 52 Conclusions ...... 55

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References ...... 56 Appendix 1: Marine Protected Areas in Raja Ampat ...... 64 Appendix 2: List of Shark Species Recorded in Raja Ampat ...... 65 Appendix 3: Shark Monitoring Protocol for Raja Ampat MPA Network using baited remote underwater video stations (BRUVS) ...... 66 Appendix 4: Annotated Bibliography ...... 77 Appendix 5: Abbreviations ...... 78

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 5

List of Figures

Figure 1. Map of the Raja Ampat archipelago, West Papua, Indonesia showing the location of major islands and marine protected areas (MPAs and MCAs). Protected areas shown are: Ayau-Asia Islands*, Wayag-Sayang*, Raja Ampat National (previously West Waigeo), Penemu-Bamboo (Pam-Saukabu)**, Dampier Strait**, Mayalibit Bay, Kofiau and Boo Islands*, and Southeast Misool*. Those marked with a double asterix (**) were the focus in this study, while those marked with a single asterix (*) are currently being sampled using the protocol from this study...... 14 Figure 2. Map showing study area sample sites in no-take and fished zones within Penemu and Dampier Strait protected areas (P = Penemu; D = Dampier; NTZ = No Take Zone; UZ = Use Zone; sites are numbered 1-10 in each Area x Status)...... 15 Figure 3. BRUVs sampling design strategy for field work data collection, resulting in 360 total planned replicate BRUVs deployments...... 16 Figure 4. A Baited Remote Underwater Video System (BRUVs) setup resting on the sea floor. Top: As seen from water surface with buoy attached; Bottom: Resting on benthos. Images copyright Steven Lindfield...... 17 Figure 5. A frame grab taken during video analysis process using the EventMeasure software interface showing the field of view of a shallow BRUVs deployment with species Carcharhinus melanopterus MaxN =1...... 19 Figure 6. Overall mean relative abundance (MaxN per 60 minute deployment ±SE) in shark species diversity observed throughout the study. Note . Unidentified species are included as Carcharhinus sp...... 21 Figure 7. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait No-take Zones and Penemu MCA samples in study areas...... 22 Figure 8. Mean relative abundance (MaxN per 60 minute deployment ±SE) in no-take and fished samples in study areas...... 23 Figure 9. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait and Penemu Areas by status (No-take zones versus use zones)...... 23 Figure 10 . Mean relative abundance (MaxN ±SE) of sharks by depth factor (D = deep, M = mid-water, S = shallow)...... 23 Figure 11. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait and Penemu Areas by depth factor...... 24 Figure 12. Mean relative abundance (MaxN ±SE) of sharks by depth inside and outside no-take zones...... 24 Figure 13. Mean relative abundance (MaxN ±SE) of shark species in Dampier versus Penemu sampling areas. Note . Unidentified species are included as Carcharhinus sp...... 26 Figure 14. Mean relative abundance (MaxN ±SE) of shark species in no-take versus fished status areas in Penemu MCA area. Note . Unidentified species are included as Carcharhinus sp...... 27 Figure 15. Mean relative abundance (MaxN ±SE) of shark species in no-take versus fished status areas in Dampier Strait MPA area. Note . Unidentified species are included as Carcharhinus sp...... 27 Figure 16. Depth variation in relative abundance (sum MaxN) and shark species diversity (for deep (D), medium (M) and shallow (S) depths)...... 28 Figure 17. Mean relative abundance (MaxN ±SE) of shark species in shallow (S), medium (M) and deep (D) samples...... 29

List of Tables

Table 1 PERMANOVA table of results showing differences in relative abundance of all shark species for the Penemu and Dampier protected areas with respect to Area (AR), Status (ST), Depth (DE), Sites (SI) and their interactions...... 28 Table 2 Pairwise PERMANOVA table of results showing differences in shark assemblages for the Penemu (P) and Dampier (D) areas with respect to Status (NTZ or UZ) and the differences between Status within each Area ... 28 Table 3 Pairwise PERMANOVA table of results showing differences in relative abundance of all shark species for the Penemu and Dampier protected areas with respect to Depth (D = deep, M = mid-water, S = shallow...... 31

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Table 4 PERMANOVA table of results showing differences shark assemblage structures for the Penemu and Dampier protected areas with respect to Area (AR), Status (ST), Depth (DE) and their interactions...... 33 Table 5 Pairwise PERMANOVA table of results showing differences in shark assemblages for the Penemu (P) and Dampier (D) protected areas with respect to Area (AR) and with respect to Status (ST) from the ARxST interaction ...... 35 Table 6 SIMPER results showing differences in contributions of species with high influence on shark assemblages for the Penemu and Dampier areas with respect to Depth (DE)...... 37

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Acknowledgements I have sincere gratitude for many supporters throughout the development of this thesis.

First and foremost, I would like to sincerely thank my supervisor, Steven Lindfield, whose guidance was invaluable for the completion of this project. Steve’s vital support in experimental design and statistical analysis, writing and editing, as well as his fun, positive, and incredibly helpful presence in the field, made the last year and a half of BRUV shark research work not only possible, but enjoyable.

Mark Erdmann, who had the initial brainwave for this project, is a constant source of inspiration with his insights into the critical components, and practical application, of conservation through multi-disciplinary approaches to marine protected area development and management. It was also his, and Royal Roads’ Gwen Campden’s, support through the grant application process that made the NSERC-IPS grant a reality; the grant funded a substantial portion of the equipment used in this study and was subsequently donated to the local monitoring science team to continue this research.

This research was undertaken with the support of NSERC through the Industrial

Postgraduate Research Scholarship and Conservation International Indonesia. I am very grateful to CII for supporting this project by providing professional and technical advice, field equipment, as well as logistical and administrative support. Special thanks to Nur Ismu Hidayat, Ronal

Mambrasar, Asser Burdam, Manu Mofu, Daud, Abraham Sianipar, Hastuti Sabrang, Captain

Wempy and the crew of the Inbekwan MPA floating ranger station, all of whom became

BRUV’ers extraordinaire in the field, and ensured that operations were smooth, safe and fun while at sea in the remote archipelago. Also to Tuti who spent endless hours watching videotapes

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 8 to help with the data post-processing, and Ismu, the GIS guru, whose map expertise was invaluable.

I would also like to thank Sea Sanctuaries Trust for accommodating my use of the MV

Hang Tuah as a base from which to complete the second portion of field sampling in the Penemu archipelago during February 2014. Thanks to the Aquanauts for their assistance and ingenuity, especially Aquaman Mateus Baronio who helped coordinate and facilitate the Penemu portion of the sampling as well.

I would also like to thank Vanessa Jaiteh, whose insights into the practical use of BRUVs in the eastern-Indonesian context, and loan of her own BRUV systems for pilot trials in Raja

Ampat which was very helpful in the development of the project.

I also greatly appreciate the financial support I received during my studies, in addition to the NSERC research grant, particularly through the TD Environmental Sustainability Scholarship and Chawkers Foundation Award.

As always, my greatest thanks goes to my family for their never-ending support and patience, especially during the post-processing and writing phase of this undertaking. I also owe immense gratitude to Calvin Beale for his editing of drafts (!?!), but mostly for his knack at keeping my spirit in tact throughout writing process and providing a rejuvenating manta dive in the most challenging time.

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Introduction and Background Sharks – Importance and Global Status Sharks are the dominant apex predators in marine ecosystems; they are exceptionally vulnerable to overfishing and concerns have arisen about localized extinctions (Worm et al .,

2013; García, Lucifora & Myers, 2008). The intrinsic life histories and ecological sensitivity of most shark species (low-fecundity, slow, late-maturity), combined with exposure to fishing mortality, results in an elevated extinction risk in sharks (Dulvy et al., 2014; Worm et al ., 2013).

Sharks are ecologically important species that influence the health of fish populations and by extension, the state of regional fisheries (Friedlander & DeMartini, 2002). Management and conservation of shark populations, including deep-water, oceanic and continental shelf species, are therefore a high priority across the globe (Dulvy et al., 2014; García et al., 2008). Recent comprehensive analysis of global shark mortality indicates that approximately 100 million sharks are killed each year (Worm et al ., 2013; García et al., 2008). Yet for the sharks that remain, there is limited understanding about the natural population levels and community structure, which makes it difficult to assess the effects of management and conservation policies.

Drastic global declines in shark populations are likely to continue, as there is a serious lack in formal protection for these species (Lucifora, García & Worm, 2011; Robbins, Hisano,

Connolly & Choat, 2006; Worm et al ., 2013). Just over 140 species of shark are categorized as

“Threatened” 1 or “Near Threatened” 2 on the International Union for the Conservation of Nature

(IUCN)’s Red List (IUCN, 2012b). Yet only nine of these are listed in Appendix II of the

Convention on International Trade of Endangered Species (CITES) convention, which regulates

1 “facing high risk of extinction in the wild” (IUCN, 2012a). 2 “plants and animals that are either close to meeting the threatened thresholds or that would be threatened were it not for an ongoing taxon-specific conservation program” (IUCN, 2012a).

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 10 international trade of listed species (IUCN, 2013). The main driver for shark fishing is the trade for shark fins to international markets, particularly in Asia where a single shark fin can fetch prices as high as €1,000 (Oceana, 2010). As shark fins are such a valuable item, this drives large scale fishing practices that are often not managed or monitored. Indonesia supports the world’s largest shark fishery (Blaber et al., 2009), yet seriously lacks information on the numbers and species of sharks and rays caught. There are many communities in Indonesia whose economies are heavily reliant on shark fishing that are experiencing dwindling catches (V. Jaiteh, personal communication).

Conservation in Raja Ampat The Raja Ampat archipelago of West Papua has been scientifically classified as the epicenter of the worlds’ marine biodiversity (Allen & Erdmann, 2009, 2012; Veron et al ., 2009).

Located in the heart of the ‘Coral Triangle’, Raja Ampat is the crown jewel of the Bird’s Head

Seascape (BHS) of Eastern Indonesia, and has been identified as a global priority for marine conservation (Huffard, Erdmann & Gunawan, 2009). Low population density and rich natural resources, combined with recent attention to these riches and an influx of immigrants, have made the region highly threatened by pollution, destructive fishing practices that damage coral reefs, and overfishing of several target species including sharks. Raja Ampat is also being targeted for economic development in fisheries, marine tourism, mining and forestry. Larsen (as cited in

Mangubhai et al ., 2012) found that over 90% of the Raja Ampat population depends on the sea for their livelihoods, so even if fishers do not specifically target sharks, the ocean is an integral aspect of life for these coastal communities, and the loss of the regulatory influence of sharks in the marine ecosystem could be detrimental for local livelihoods.

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Like many parts of the world, sharks have faced a history of fishing pressure in Raja

Ampat. Harvesting of sharks in Raja Ampat, mostly for their valuable fins, has been practiced since the 1980s (Varkey, Ainsworth, Pitcher, Goram & Sumaila, 2010). Anecdotal evidence and personal observations from outside no-take zones indicate sharks have declined in recent years.

In addition, underwater visual census (UVC) of six marine protected areas (MPA) in Raja Ampat from 2010-2012 show very few sharks (Mangubhai et al ., 2012). Increasing tourism has begun to confer a small degree of protection on sharks in Raja Ampat in recent years: Locals realize the sharks’ tourism draw, and illegal fishers and government officials are under local and international pressure to comply with, and enforce laws respectively. There are signs of recovery of certain shark species in geographic pockets around Raja Ampat as observed with UVC

(Conservation International, unpublished data), which may be attributable to a combination of eco-tourism, education and awareness campaigns, local patrols and implementation of no-take zones.

A network of marine protected areas (MPAs) has been established in Raja Ampat in an attempt to ensure long-term food security and wellbeing for local traditional communities (Fig.

1). For the purposes of this paper, the term MPA will be used as defined by the World

Conservation Union: “Any area of intertidal or sub-tidal terrain, together with its overlying water and associated flora, fauna, historical and cultural features, which has been reserved by law or other effective means to protect part or all of the enclosed environment” (IUCN, 1988). The Raja

Ampat MPAs cover over 1,400,000 ha of marine and coastal ecosystems; they were designated by indigenous communities and are collaboratively-managed in a partnership between local communities and the Raja Ampat regency government, with additional support from International

Non-Governmental Organizations (NGOs) Conservation International (CI) and The Nature

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Conservancy (TNC) (Mangubhai et al ., 2012). This network has been augmented by several

Marine Concession Areas (MCAs) that are managed in partnership between communities and private enterprises (such as dive resorts). The individual areas and legal status of these protected areas can be seen in the table in Appendix 1. For the purpose of this study, ‘no-take zone’ is defined as a marine area that is effectively completely protected and where no extractive activities are allowed (this may be in an MPA or MCA). MPAs and MCAs are a major focus in conservation biology, marine ecology and fisheries management globally, as these areas can reduce the effects of fishing and aid the recovery of certain species if they are well respected and monitored (Green, White & Tanzer, 2012).

MPAs and Shark Protection Though MPAs have been implemented to successfully protect the benthos and less- mobile species in several areas, the effect of spatial closures on mobile pelagic species such as sharks is debated (Claudet et al., 2010; Kaplan, Chassot, Gruss & Fonteneau, 2010; Santana-

Garcon, Newman, Langlois & Harvey, 2014). Model-based evidence found that the size of the protected area must be larger than home range of the individuals of the species targeted (Grüss,

Kaplan & Hart, 2011), yet also that the quality of the protected area (i.e. if it includes spawning or nursery grounds) is important for protection of more mobile species (Apostolaki, Milner-

Gulland, McAllister, & Kirkwood, 2002). In a meta-analysis of European reserves, Claudet et al.

(2010) found that even mobile species benefit from designated protected areas.

MPAs provide protection and can positively affect shark populations, particularly for reef shark species, which exhibit high site-fidelity (Bond et al., 2012; Cappo, De’ath, Stowar,

Johansson & Doherty, 2009a; Goetze & Fullwood, 2013; Randall, 1977). MPAs have been shown to generate benefits for multiple shark species with different life history and ecological

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 13 characteristics (Knip, Heupel & Simpfendorfer, 2012). Although MPAs may buffer population loss, some evidence suggests that generalist MPAs, i.e. those that still allow some forms of fishing, are not enough, and complete ‘no-go’ zones, or diligently enforced ‘no-take’ zones, are required to provide adequate protection for sharks (Meekan, Cappo, Carleton & Marriott , 2006;

Robbins et al ., 2006). Robbins et al. (2006) recorded reductions between 80 to 97% in shark populations on restricted-fishing reefs versus no-entry reefs in the Great Barrier Reef (GBR) of

Australia, while Meekan et al. (2006) found sharks to be 2-4 times more abundant on un-fished reefs. More recently, a ten-year study on the Great Barrier Reef Marine Park of Australia showed significant increases in shark populations in non-fished sites over time (Espinoza, Cappo, Heupel,

Tobin & Simpfendorfer, 2014).

Raja Ampat Shark Sanctuary In addition to the protection afforded by MPAs and MCAs, and more specifically, no-take zones, the Raja Ampat Regency Government declared the entire archipelago a “Sanctuary for

Sharks and Rays” in September 2012, which is backed by regional-level law, PERDA 9/2012.

The law explicitly forbids the capture of any shark, ray, whale, dugong, sea turtle, or endemic species in Raja Ampat waters, conferring an additional level of protection for these species throughout the region. Although regarded as an encouraging stride, Mangubhai et al . (2012) also suggest that the absence of critical baseline information on shark stocks and poor enforcement of existing regulations will likely see stocks continue to decline in the BHS.

The recently imposed ‘shark sanctuary’ may provide positive benefits for the remaining shark populations in Raja Ampat, but in order to increase social acceptance and adherence, and promote the use of such large scale management to other areas in the world, the benefits need to be well documented though rigorous scientific surveys. This study focused on the former

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 14 knowledge gap by assessing the current status of Raja Ampat shark populations (diversity and abundance), providing imperative baseline data for the region.

Studying Shark Populations – the use of BRUVs This study used Baited Remote Underwater Video stations (BRUVs) to quantify reef shark diversity and abundance in Raja Ampat. BRUVs techniques are an effective means to non- destructively assess these population characteristics of sharks and other reef fish (Brooks,

Sloman, Sims & Danylchuket, 2011; Meekan & Cappo, 2004; Meekan et al ., 2006; Cappo et al,

2007), which means they are appropriate for use in sensitive habitats and protected areas. Depth has a considerable influence on shark assemblage structure: Meekan et al. (2006) observed a strong depth-effect in species richness with less than half the total shark species observed occurring in shallow BRUVs in Australian MPAs. This diver-less method allows for sampling beyond the no-decompression limits of diver-based surveys, and also increases the potential sampling replication and coverage by use of multiple BRUVs systems simultaneously (Cappo,

De’ath & Speare, 2004), An overall cost-benefit analysis by Langlois et al. (2010) showed that

BRUV stations are a more cost-effective means of monitoring than alternative methods.

Additionally, BRUVs provide a permanent tape record, which allows for independent verification of results, or possible re-analysis for alternative data for future studies (Cappo, Speare & De’ath,

2007). This method has proved useful for detecting MPA effects on shark populations in Fiji

(Goetze & Fullwood, 2013) and Australia’s Great Barrier Reef (Espinoza, Cappo, Heupel, Tobin

& Simpfendorfer, 2014).

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 15

Significance and Application of the Research The baseline data, protocols and local capacity developed during this research, provides a basis for continued monitoring and evaluation of Raja Ampat shark populations. This will increase understanding of how the management status of local marine areas influences the characteristics of shark populations and may contribute to recovery of these endangered apex predators. This knowledge will serve to inform management efforts, including development of zonation plans, and effectiveness of enforcement, education and outreach programs. This study will help managers adopt MPA management planning for changing marine and social conditions, providing protection for valuable shark populations, improving biodiversity protection, and by extension, fisheries security.

Research Question and Objectives Research Questions 1. Do shark populations differ between no-take zones and fished areas in Raja Ampat?

2. Do shark populations differ along gradients of depth?

3. Are BRUVs an appropriate methodology for monitoring shark populations in Raja

Ampat?

Research Objectives The objectives aligned with the purpose of the research and being answered by the above research questions, are as follows:

1. To provide a scientific characterization of the status of shark populations in Raja Ampat

(baseline data including diversity and abundance). Assessing how shark populations

change between no-take and fished areas will also serve as a baseline to monitor changes

over time and compare to alternative management strategies. Knowledge on the

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 16

distribution of shark populations will provide important information on what areas should

be prioritized for management or protocols to mitigate the effects of fishing on sharks in

Raja Ampat.

2. To develop optimal protocols and assess the practicality for the use of BRUVs in future

research and monitoring of shark populations and to develop the capacity of the local

scientific monitoring teams to conduct this research.

3. To document the effectiveness of the shark sanctuary and management zones with the

potential to influence adoption of similar strategies in other areas of Indonesia and the

world to reduce the widespread decline in shark populations.

4. To contribute to global knowledge in the field of shark ecology and conservation.

The focus of this research has been developed collaboratively with Conservation

International Indonesia (CII), an NGO that has worked extensively in Raja Ampat since 2001.

Results of the study are being shared with the protected areas management planning authorities, government partners and other stakeholders in the region.

Research Methodology This research uses non-destructive sampling techniques to quantify shark diversity and abundance in two areas with no-take and comparable fished sites in the Raja Ampat archipelago.

Description of Study Areas The Raja Ampat archipelago consists of a network of eight marine protected areas ( Figure

1). Two of Raja Ampat’s marine protected areas (MPAs) were sampled in this study: Dampier

Strait MPA and Penemu-Bamboo MCA (Figure 1). The Penemu-Bamboo MCA represents a total protected area of 69,828 ha and is comprised of two sub-MCA areas off the western end of the Dampier Strait: the Penemu MCA consists of a 5,610 ha area surrounding the Penemu and

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 17

Keruo Islands; while the Bamboo MCA is 64,218 ha surrounding the Bamboo islands even further to the west. These MCAs are exclusively no-take in nature. Due to weather and sea conditions, sampling was completed only in the Penemu MCA area. The Dampier strait MPA protects a total area of 336,200 ha stretching from the southern side of Waigeo and Gam islands across the Dampier Strait to include the island of Batanta, and has its southern border on the north side of Salawati Island. This area is sub-divided by a zonation plan that includes traditional use zones and no-take zones.

Within each protected area, ten sites were sampled as representative of the area, these sites were then related to an equal number of fished sites outside the MPA that were comparable in terms of village proximity, habitat, geographic, bathymetric, and oceanographic factors

(Figure 2).

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Figure 2. Map showing study area sample sites in no-take and fished zones within Penemu and Dampier Strait protected areas (P = Penemu; D = Dampier; NTZ = No Take Zone; UZ = Use Zone; sites are numbered 1-10 in each Area x Status).

Study Species Sharks (Subclass Elasmobranchs, of the Class Chondrichthyes ) were the target species for analysis in this study. Twenty-two shark species have been previously documented in Raja

Ampat (Appendix 2).

Research Design and Sampling Strategy Baited Remote Underwater Video stations (BRUVs) were used to quantify reef shark diversity and abundance in Raja Ampat. A four factor sampling design was used consisting of

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 20

Area (n=2, fixed); Status ( two levels: fixed, no-take or fished) ; Depth (three levels, fixed, shallow

(2-12 m), mid-water (15-30 m) and deep (50-85m); and Site (n=10, random, nested in Area x

Status x depth). At each site, three replicate BRUVs were deployed at least 500 m apart. This design resulted in 360 replicate deployments (or 180 replicates from each area; 180 replicates from each status; 120 replicates from each depth) (Figure 3). However due to a lack of reef habitat at some sites or some deployments failing (due to video recording errors, video bottom time being less than the standardized 60 minutes, BRUVs structure falling over or changing position during recording, or the BRUV field of view being obscured), only 328 replicates could be used. Prior to sampling, the level of replication (30 BRUVs per factor of interest) was decided from power analysis on shark abundance at another location (Mariana Islands) using G*POWER

3 software (Faul, Erdfelder, Lang & Buchner, 2007). Increasing the number of sites (rather than replicates) provided a more powerful test to detect differences between MPA status as determined using PERMANOVA software (Anderson, Gorley & Clarke, 2008); more sites allows for representative sampling of relatively large areas.

Figure 3. BRUVs sampling design strategy for field work data collection, resulting in 360 total planned replicate BRUVs deployments.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 21

Sampling Technique and Equipment: Baited Remote Underwater Video (BRUVs) Systems Baited remote underwater video techniques are an effective means to non-destructively assess the diversity and abundance of sharks and other reef fish (Brooks et al., 2011; Meekan &

Cappo, 2004; Meekan et al ., 2006; Cappo et al, 2007). This method was selected after undertaking a critical review of potential elasmobranch sampling techniques and critical analysis of appropriateness of application for the remote archipelago of Raja Ampat.

BRUVs equipment setup and standardization. Customized BRUVs were designed and built locally for this study based on the standard design, similar to those employed by Cappo et al. (2009b). Each BRUVs setup consists of a high definition video camera in underwater housing and depth gauge attached to a galvanized steel frame designed for placement on the seafloor with minimal damage to the reef. Cameras are oriented parallel to the sea floor, with the benthos visible, which allows a larger field of view including the general area of encounter for shark species (Mallet & Pelletier, 2014). Deployment of BRUVS is done by careful placement of the cameras on the substrate to ensure no damage is caused to the substrate (especially coral in reef areas), and to provide an unobstructed field of view. GoPro Hero3 cameras were used in this study as they provide a wide field of view in high- definition quality. Cameras recorded with 1920 x 1080 resolution on wide setting for 25 fps in

PAL format. Each BRUVs frame has an attachment of a plastic-coated metal bait-bag (250 x 350 mm) at the end of a 1.5m-long plastic pole, and is attached to a 7 mm floating rope and surface float ( Figure 4). Ropes were 1.5 times the max depth of the sampled sites, ensuring enough length for strong currents. Bait consisting of approximately 1kg of chopped and crushed fresh skipjack tuna (Katsuwonus pelamis ) was used to attract sharks to the viewing area of the cameras.

It was found that oily baits such as tuna consistently attracted greater numbers of predatory

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 22 species, such as sharks, thus provide better statistical power in detecting differences in populations than un-baited cameras (Harvey, Cappo, Butler, Hall & Kendrick, 2007).

Figure 4. A Baited Remote Underwater Video System (BRUVs) setup resting on the sea floor. Top: As seen from water surface with buoy attached; Bottom: Resting on benthos. Images copyright Steven Lindfield.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 23

Data collection and standardization BRUVs were deployed and left to film for 60 minutes, as this is the standard used in previous studies (Mallet & Pelletier, 2014). Replicate deployments were randomly stratified over the coral reef habitat along the exposed reef edge. Adjacent deployments were separated by 500 m to reduce the likelihood of sharks moving between replicates. Sampling was conducted from

January to February 2014 and took place during daylight hours between 07.00 and 16.00 hrs. For more in-depth detail about the sampling protocol and field work data collection process, please see Appendix 3: Shark Monitoring Protocol for Raja Ampat MPA Network using baited remote underwater video stations (BRUVS) , developed during this research project to serve as a guideline for continued use in the region.

Data Analysis Video processing Interrogation of video footage was conducted using a specialized software interface

(EventMeasure, www.seagis.com.au) to manage field data. The dynamics of appearance of shark species in the field of view was used to develop estimates of density and relative abundance

(Figure 5). Shark data was recorded for: (1) species identification (including JPG reference image), (2) maximum number of individuals of any given species seen together in the field of view (Max N), and (3) time of arrival of each species. Max N is used as a measure of relative abundance as it ensures no double-counts, and is generally acknowledged to provide a conservative estimate of abundance (Cappo et al., 2004; Willis, Millar & Babcock, 2000).

Visibility observed during the study was generally very good (approx. 20 m) and sharks were recorded to the limits of visibility. Additional data recorded during the video processing included shark behavior (passing, feeding/scavenging, chasing, etc.), stage (adult or juvenile), bottom-time

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 24 placement, benthic images for habitat classification, and other comments. Videotape analysis was standardized to 60 minutes from time of placement on the benthos and shark abundance presented as MaxN per hour. Video analysis was very time-consuming; using an increased playback rate of 4x, it still required almost 40 minutes to review each BRUV deployment video.

Figure 5. A frame grab taken during video analysis process using the EventMeasure software interface showing the field of view of a shallow BRUVs deployment with species Carcharhinus melanopterus MaxN =1.

Statistical analysis The shark population metrics, species richness and abundance were analyzed using univariate and multivariate statistical approaches. The sampling design for this study consisted of four factors as previously mentioned, but as the design was not completely balanced with n=3 due to some failed replicates from technical errors in the field, the MaxN data was averaged on the Site x Depth level, which also decreased the prevalence of zero values in the dataset. I tested the null hypotheses that there is no difference in population metrics between the factors of Area

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 25

(Dampier and Penemu), Status (no-take areas vs. fished areas) or Depth (deep vs. mid-water vs. shallow).

Spatial & depth comparisons of no-take and fished sites Univariate permutational analysis of variance (PERMANOVA; with 9999 permutations) using dissimilarity matrices constructed with Euclidean distance were used to test for differences in the relative abundance (MaxN) of all shark species combined using the PRIMER 6 with

PERMANOVA+ add-on statistical software package (Plymouth Routines in Multivariate

Ecological Research; Anderson et al., 2008; Clarke & Gorley, 2006). This was consistent with the analysis performed by Goetze and Fullwood (2013) for a similar study in Fiji’s marine reserves. Data transformation was deemed unnecessary for use with PERMANOVA, due to the low variance in counts (typically 0 or 1) and supported by a test of dispersion (PERMDISP), which is equivalent to Levene’s test of heterogeneity of variances (Anderson, 2006).

Species assemblage comparisons Multivariate permutational analysis of variance (PERMANOVA; with 9999 permutations) using dissimilarity matrices constructed with Bray-Curtis similarities on square- root transformed data were used to test for differences in the assemblages of shark species between areas (Dampier and Penemu), status (No-Take and Fished) and depth (shallow, medium and deep) using the PRIMER 6 with PERMANOVA+ add-on statistical software package

(Plymouth Routines in Multivariate Ecological Research; Anderson et al., 2008; Clarke &

Gorley, 2006). Again, the data was pooled to the level of site x depth by averaging replicates in order to standardize for the slight discrepancy in number of successful replicates due to technical errors in the field. SIMPER (similarity percentages) routine in PRIMER was used to determine

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 26 the species responsible for dissimilarity in the shark assemblage structures (Anderson et al.,

2008), using the Bray-Curtis dissimilarity matrix among samples.

Results Shark Diversity and Abundance Nine species of sharks (from five families) and 135 individuals were observed in this study. From the 328 BRUVs replicates used in this study, sharks were recorded on ~36% of the

BRUVs (118 replicates samples). Overall, the average relative abundance of sharks was a MaxN of 0.41 sharks/hour. The majority of observations were reef sharks from the Carcharhinid family

(Figure 6). The most abundant species recorded was Carcharhinus melanopterus (blacktip reef shark) with a total of 98 individuals recorded and highest MaxN recorded of 3 sharks in one video frame. This species comprised ~73% of sharks observed in the study and appeared in ~28% of replicates.

Other shark species observed in the study (and number of sightings) were: Triaenodon obesus (whitetip reef shark; 7), Nebrius ferrugineus (tawny nurse shark; 7), Carcharhinus amblyrhynchos (grey reef shark; 3), Sphyrna lewini (scalloped hammerhead; 3), Hemipristis elongata (snaggletooth shark; 1) , Chaenogaleus macrostoma (hooktooth shark; 1) , Carcharhinus limbatus (blacktip shark; 1), Eucrossorhinus daypogon (tasseled wobbegong; 1). There were also

13 individual sharks recorded on film that could not be identified with complete certainty due to lighting or visibility issues. Four species ( Hemipristis elongata, Chaenogaleus macrostoma,

Carcharhinus limbatus , and Eucrossorhinus daypogon ) were recorded in only a single replicate, all of which were single individuals.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 27

Figure 6. Overall mean relative abundance (MaxN per 60 minute deployment ±SE) in shark species diversity observed throughout the study. Note . Unidentified species are included as Carcharhinus sp.

Variation Between Area and Status There was no overall significant difference (p<0.05) in shark abundance between sampling areas (AR; Dampier and Penemu) or between no-take and fished sites, according to the four-factor PERMANOVA test (Table 1). There was a slightly higher relative abundance of sharks recorded within the Penemu Area (average MaxN of 0.48 ±0.05 (mean ± SE, n= 142)) than the Dampier Area (average MaxN of 0.36 ±0.04 (mean ± SE, n= 186)) (Figure 7). There was also slightly higher relative abundance of sharks recorded within NTZ’s, with an average

MaxN of 0.43 ±0.05 (mean ± SE, n= 161) compared to 0.39 ±0.05 (n=167) in fished zones

(Error! Reference source not found. ).

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There was however an interaction effect for Area x Status (p=0.049). Pairwise tests

(Table 2) showed that this was driven by more of sharks (p=0.031) within the Penemu MCA no- take area (average MaxN of 0.57 ±0.08 SE, n= 70) compared to the Dampier MPA no-take zones

(average MaxN of 0.33 ±0.06 SE, n= 91) while numbers of sharks in use-zones were similar between areas (p=0.657) (Figure 9). Although not quite significant at the P<0.05 level, the interaction effect for Status within Areas showed more sharks on average within the NTZ compared to fished sites at Penemu (p=0.07) whereas numbers were similar between zones at

Dampier (p=0.379) ( Figure 9).

Table 1

PERMANOVA table of results showing differences in relative abundance of all shark species for the Penemu and Dampier protected areas with respect to Area (AR), Status (ST), Depth (DE), Sites (SI) and their interactions.

Source df SS MS Pseudo-F P(perm) AR 1 0.298 0. 298 2.053 0.1542 ST 1 9.769 9.767 0.673 0.4184 DE 2 2.254 1.127 7.761 0.0008 ARxST 1 0.573 0.572 3.942 0.0491 ARxDE 2 2.391 1.197 8.233 0.922 STxDE 2 0.178 8.912 0.614 0.5494 ARxSTxDE 2 0.413 0.207 1.423 0.2494 SI(ARxSTxDE) 102 14.67 0.149 0.288 0.9178 Res 1 0.5 0.5 Total 114 19.064 Note . Significant results are presented in bold. Significance considered at the p<0.05 level.

Table 2 Pairwise PERMANOVA table of results showing differences in shark assemblages for the Penemu (P) and Dampier (D) areas with respect to Status (NTZ or UZ) and the differences between Status within each Area Groups t P(perm) Within NTZ D, P 2.1813 0.0309

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 29

Within UZ D, P 0.4395 0.6573 Within Dampier NTZ, UZ 0.89219 0.379 Within Penemu NTZ, UZ 1.8355 0.07 Note . Significant results are presented in bold. Significance considered at the p<0.05 level.

Figure 7. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait No-take Zones and Penemu MCA samples in study areas.

Figure 8. Mean relative abundance (MaxN per 60 minute deployment ±SE) in no-take and fished samples in study areas.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 30

Figure 9. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait and Penemu Areas by status (No-take zones versus use zones).

Variation Between Depths Overall depth variation. Depth is clearly an important factor influencing the abundance of sharks in the areas sampled (Table 1; p<0.001). The greatest relative shark abundance (average MaxN of 0.58 ±0.06

SE, n= 108) was recorded from the shallow depth group (2 m – 12 m) and decreased with depth to an average MaxN of 0.24 ± 0.05 SE (n= 88) at the deep depth group (50 m – 85 m) (Figure

10 ). Pairwise-tests ( Error! Reference source not found. ) show highly significant difference

(P<0.001) between shallow and deep depths, while other comparisons are close to the p<0.05 level.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 31

Figure 10 . Mean relative abundance (MaxN ±SE) of sharks by depth factor (D = deep, M = mid-water, S = shallow).

Table 3 Pairwise PERMANOVA table of results showing differences in relative abundance of all shark species for the Penemu and Dampier protected areas with respect to Depth (D = deep, M = mid- water, S = shallow. Groups t P(perm) D, M 1.9425 0.053 D, S 4.0813 0.001 M, S 1.9338 0.056 Note . Significant results are presented in bold. Significance considered at the p<0.05 level.

Area-related depth variation. Relative abundance of sharks in Dampier and Penemu areas at the three depth factors mirrored the overall trend and depth effect with increasing abundance from deep to shallow replicates ( Figure 11 ). This was supported by the non-significant interaction term Area x Depth was (p=0.922; Table 1).

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 32

Figure 11. Mean relative abundance (MaxN per 60 minute deployment ±SE) in Dampier Strait and Penemu Areas by depth factor.

Status-related depth variation. Although the interaction term status x depth was not significant (p=0.55; Table 1), Figure

12 shows that there was a trend for greater shark abundance within protected zones compared to fished zones in the medium and deep depth groups but not at the shallow depth.

Figure 12. Mean relative abundance (MaxN ±SE) of sharks by depth inside and outside no-take zones.

Shark Population Assemblage Variation Overall there were no significant differences (at the p<0.05 significance level) in shark species assemblages between sampling areas (Dampier and Penemu) or between no-take and

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 33 fished sites, according to the four-factor PERMANOVA test, although there was a significant

(Area x Status) interaction effect (

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 34

Table 4). Depth was the most important factor influencing shark population assemblages in this study (

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 35

Table 4).

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Table 4 PERMANOVA table of results showing differences shark assemblage structures for the Penemu and Dampier protected areas with respect to Area (AR), Status (ST), Depth (DE) and their interactions. Source df SS MS Pseudo-F P(perm) Unique perms AR 1 656.24 656.24 2.2128 0.0975 9957 ST 1 217.97 217.97 0.73495 0.518 9954 DE 2 6959.4 3479.7 11.733 0.0001 9946 ARxST 1 1119.4 1119.4 3.7745 0.0235 9955 ARxDE 2 472.43 236.22 0.79649 0.5414 9936 STxDE 2 130.06 65.028 0.21926 0.9444 9949 ARxSTxDE 2 712.19 356.09 1.2007 0.3036 9954 Res 102 30250 296.57 Total 113 40515 Note . Significant results are presented in bold. Significance considered at the p<0.05 level.

Species-related area variation. It was apparent that although Penemu has greater numbers of sharks on average, Dampier area has higher overall diversity (Figure 13 ). Both areas contained the three most frequently observed sharks in the study: Carcharhinus melanopterus, Nebrius ferrugineus , and Triaenodon obesus. Interestingly, Carcharhinus amblyrhynchos was observed in Penemu and not in Dampier, while Dampier contained Sphyrna lewini, Hemipristis elongata, Eucrossorhinus daypogon ,

Chaenogaleus macrostoma and Carcharhinus limbatus.

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Figure 13. Mean relative abundance (MaxN ±SE) of shark species in Dampier versus Penemu sampling areas. Note . Unidentified species are included as Carcharhinus sp.

Species-related Area x Status interaction effect. There was a significant Area x Status interaction the assemblage structure of shark populations (

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 38

Table 4; p=0.0235). Pairwise comparisons of assemblages by area and by status show that this significance is due to the assemblages being similar between Dampier and Penemu within UZs, but different between areas within NTZs (

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 39

Table 5

; p=0.01; Figure 14 ; Figure 15 ). This significant result is driven by the relative abundance of blacktip reef sharks (Figure 14 ; Figure 15 ).

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 40

Table 5 Pairwise PERMANOVA table of results showing differences in shark assemblages for the Penemu (P) and Dampier (D) protected areas with respect to Area (AR) and with respect to Status (ST) from the ARxST interaction Groups t P(perm) Within NTZ D, P 2.1494 0.0109 Within UZ D, P 0.7463 0.6113 Within Dampier Area NTZ, UZ 1.5146 0.0926 Within Penemu Area NTZ, UZ 1.4955 0.1039 Note . Significant results are presented in bold. Significance considered at the p<0.05 level.

Figure 14. Mean relative abundance (MaxN ±SE) of shark species in no-take versus fished status areas in Penemu MCA area. Note . Unidentified species are included as Carcharhinus sp.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 41

Figure 15. Mean relative abundance (MaxN ±SE) of shark species in no-take versus fished status areas in Dampier Strait MPA area. Note . Unidentified species are included as Carcharhinus sp..

Species-related Variation in Depth Shark species assemblages varied significantly between depths according to the four- factor PERMANOVA test (

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 42

Table 4; p=<0.001 for DE). SIMPER testing (Table 6) shows the major contributing species to dissimilarities between depth groups. Carcharhinus melanopterus is clearly a major contributor to the assemblages at each depth group.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 43

Table 6 SIMPER results showing differences in contributions of species with high influence on shark assemblages for the Penemu and Dampier areas with respect to Depth (DE). Species Grp D Grp M Av. Diss/SD Contrib Cum.% Av. Av. Diss % Abund Abund Groups D & M Av.dissimilarity: 89.16 Carcharhinus melanopterus 0.12 0.23 48.03 1.27 53.86 53.86 Carcharhinus sp. 0.02 0.07 17.31 0.57 19.42 73.28 Carcharhinus 0.01 0.02 6.19 0.30 6.95 80.23 amblyrhynchos Triaenodon obesus 0.00 0.04 5.65 0.32 6.33 86.56 Nebrius ferrugineus 0.04 0.01 4.18 0.32 4.68 91.24 Groups D & S Grp D Grp S Av. Diss/SD Contrib Cum.% Av.dissimilarity: 82.93 Av. Av. Diss % Abund Abund Carcharhinus melanopterus 0.12 0.52 67.63 1.84 81.55 81.55 Nebrius ferrugineus 0.04 0.03 4.59 0.38 5.54 87.09 Carcharhinus sp. 0.02 0.01 3.24 0.28 3.91 91.00 Groups M & S Grp M Grp S Av. Diss/SD Contrib Cum.% Av.dissimilarity: 72.27 Av. Av. Diss % Abund Abund Carcharhinus melanopterus 0.23 0.52 53.20 1.44 73.62 73.62 Carcharhinus sp. 0.07 0.01 8.14 0.47 11.27 84.89 Triaenodon obesus 0.04 0.02 4.97 0.38 6.88 91.77 Note . Resemblance used S17 Bray Curtis similarity with cut-off for low contributions set at 90.00%.

Though there is significantly greater overall relative abundance of sharks in general in shallow depth, there is a strong depth effect in species richness, with greater shark diversity at the deeper samples (Figure 16 ). There were only three species of shark identified throughout shallow (2 – 12 m) replicates (and also one unidentifiable species), while eleven identifiable species were observed in deeper (> 15 m) samples (comprising six species in medium and seven species in deep replicates, with some overlap of species). Six of the species found in deeper samples never occurred in the shallow samples: Carcharhinus amblyrhynchos , Sphyrna lewini ,

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 44

Hemipristis elongata, Chaenogaleus macrostoma, Carcharhinus limbatus , and Eucrossorhinus daypogon .

Figure 16. Depth variation in relative abundance (sum MaxN) and shark species diversity (for deep (D), medium (M) and shallow (S) depths).

Counts at all depth levels were dominated by Carcharhinus melanopterus (~52%, ~59% and 90% for D, M and S samples respectively). Making up the remaining ~10% of counts in shallow samples were Nebrius ferrugineus and Triaenodon obesus . Though Triaenodon obesus was not present at the deepest depth, Nebrius ferrugineus was present in greater numbers in deep samples (accounting for ~14% of counts). Figure 17 visually depicts the mean relative abundance of shark species observed in the study by depth.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 45

Figure 17. Mean relative abundance (MaxN ±SE) of shark species in shallow (S), medium (M) and deep (D) samples.

Field Work Effort and Efficiency Fieldwork trips using a mother ship as a base minimized costs and maximized efficiency.

Two teams were able to deploy on average 30 BRUVs per day total; 25/27 full days were used for sampling during two trips. The BRUV sampling was 91% successful (328 usable replicates from 360 required samples, from 400 planned replicate deployments (planned over-sampling to ensure enough replication, especially at the medium depth level, in anticipation of failed replicates). The discrepancy between usable and planned replicates was related in part to both field-related concerns and also to data analysis issues. Weather considerations made sampling impossible or unsafe due to extreme sea conditions at two sites, and logistical considerations of a lack of baitfish availability postponed sampling for an entire day. Data analysis was impossible

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 46 for videos where the frame was obstructed by coral (only occurred in one sample) or the BRUVs structure moved or inverted during the sample and completely changed the video view frame

(occurred in 3 samples); in such cases the sample was discounted. On several occasions the camera ran out of battery prior to 60 minutes; if the resultant video was less than 50 minutes, then it was discarded, otherwise it was still used (based on the fact that in all other full-length videos with sharks, both the first sighting and the MaxN occurred prior to 45 minutes).

Downloading memory cards and archiving data took a minimum of five hours in the evening each field day (30 sample videos using 5 computers simultaneously), averaging 1.2 replicate sample per hour; video-conversion took an average of 2 hours per 60-90 minute video.

Video analysis, once the process was learned, averaged 12 replicates analyzed per 8-hour day.

There was a substantial learning curve, especially for the local team, of several days, to reach this level of skill and efficiency.

Discussion The Effectiveness of MPAs for Conservation of Shark Populations in Raja Ampat This study provides an important baseline assessment of the shark populations in the protected areas of Dampier Strait and Penemu in Raja Ampat. Shark population depletion is particularly prevalent in the Indo-Pacific Biodiversity Triangle (Dulvy et al., 2014) and MPAs have been regarded as useful management measures which can have a positive impact on shark populations (Bond et al., 2012; Cappo et al., 2009a; Claudet et al., 2010; Espinoza et al., 2014;

Goetze & Fullwood, 2013; Grüss et al., 2011; Knip et al., 2012; Meekan et al. , 2006; Robbins et al ., 2006; Randall, 1977). The lack of striking differences between fished and protected areas in this study is likely due to date of inauguration of the no-take zones. The Dampier Strait MPA was declared in 2008, however, management and zonation plans are still in development, and

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 47 effective routine patrol and enforcement didn’t begin until November 2012 (M. Mongdong, personal communication, January 2014). Penemu MCA is even newer; it was signed into village- level law and effective enforcement began in December 2012 (H. Newman, personal communication, December 2012), only 14 months prior to the data collection for this study.

Other studies that have used BRUVs to demonstrate benefits of marine reserves for sharks have all sampled MPAs that were under effective management for at least 10 years (Espinoza et al.,

2014; Goetze & Fullwood, 2013; Knip et al., 2012; Meekan & Cappo, 2004; Meekan et al.,

2006). For example, Goetze et al. (2013) studied an MPA in Fiji that was protected for 12 years and Espinoza et al. (2014) detected positive changes over 10 years of sampling multiple no-take zones on the Great Barrier Reef. While the time period after effective enforcement in the Raja

Ampat MPAs is not considered enough to accrue positive benefits for reef sharks, such positive changes between no-take and control sites may also be obscured due to the region becoming a

“Sanctuary for Sharks and Rays” where there should also be no fishing for sharks outside these no-take zones. Although the law specifically protecting sharks throughout the region came into effect in September 2012, enforcement of this law is still not effective. This timeline indicates resultant data from this study may be best taken as constituting a near time zero MPA zonation implementation baseline, rather than suggesting that the MPA zoning has not been effective for conserving shark populations. The data in this thesis will prove vital for comparison in further monitoring of shark populations in Raja Ampat.

It is conceivable that the slightly higher mean abundance of sharks within the NTZ versus the UZ in Penemu, though not statistically significant, may be the beginning indication showing positive effects of the NTZ implementation and enforcement. Despite the absence of previous baselines, this may indicate a direct, or indirect, effect of fishing. Two reasons posited by Goetze

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 48 and Fullwood (2013) for observing greater shark abundance inside no-take zones may be (1) shark mortality outside the reserve is higher than inside NTZs and/or (2) mortality of shark’s prey is lower inside the reserve, causing a habitat conducive to shark populations thriving. Although I did not sample the reef fish community that provides prey for reef sharks, the fishing pressure at

Penemu was regarded as lower than other areas of Raja Ampat, even before the no-take zone establishment (local community members, personal communications). The condensed area of the

Penemu MCA does not constitute the traditional fishing grounds of the local Penemu fishers from

Pam and Saukabu villages and was never highly exploited by them as it encompasses a traditional sacred site. Only during foul weather when the local fishers could not reach their usual fishing grounds, would they sometimes fish it (local community members, personal communications). In contrast, the geography of the Dampier NTZ sampling was much more spread out, and included two separate NTZ areas, both of which constitute higher traffic areas known to have been extensively fished in the past (local fishermen, personal communications). It is therefore likely that greater numbers of prey fish (personal observations) combined with lower fishing pressure may have contributed to the greater numbers of sharks within the NTZ at

Penemu.

The findings of this study have some important implications for management strategies in

Raja Ampat, and throughout the Bird’s Head Seascape and Coral Triangle. There is strong evidence from many other locations to show that MPAs can protect and promote recovery of shark populations and biodiversity conservation, thus providing a strong argument for effective enforcement of the no-take zones and the prohibition of shark fishing. Meekan et al. (2006) and

Robbins et al . (2006) explored shark populations relative to management status of a marine area in more depth, and found that ‘no-go’ zones, or actively enforced ‘no-take’ zones, were required

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 49 to provide adequate protection for sharks in the Great Barrier Reef of Australia. The data presented here can serve as a baseline for comparison of shark populations in Raja Ampat over time, and by extension, the analysis of the efficacy of management regimes and enforcement of

MPA regulations.

The Effect of Depth on Shark Abundance The observed depth-related variations in shark population metrics were the most pronounced findings of this study. Greater shark abundance in shallow waters was contrary to studies in Fiji and northwestern Australia that found essentially no difference in the abundance of sharks between shallow and deep samples (Goetze & Fullwood, 2013; Meekan et al., 2006). The greater abundance of sharks in shallow waters than either medium or deep samples could be explained by the fact that these shallow areas may constitute sheltered pupping or nursery areas for shark species in the region. The shallow samples in this study constituted predominantly shallow reef flats and sea grass lagoons, both of which have been identified as nursery grounds for blacktip reef sharks (the most abundant species in the Raja Ampat from our surveys) and other reef sharks in studies in other geographic locations (Heupel, Carlson & Simpfendorfer,

2007; Mourier, Mills & Planes, 2013; Papastamatiou, Friedlander, Caselle & Lowe, 2010).

Because BRUV systems used in this study don’t allow for accurate assessment of shark size, we cannot be sure that the observances in the shallow samples are juvenile or smaller sharks, but from general observances of the videos of smaller sharks with more slender/narrower bodies, it seems this might be the case. Stereo-BRUVs, which allow accurate measures of fish size

(Harvey et al., 2012; Shortis, Harvey & Abdo, 2009), were not an available option for this study, but may provide useful data in this regard if the opportunity arises in the future. If shallow depths constitute important pupping and/or nursery grounds for these species, it would indicate

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 50 the importance of inclusion of some of these near-shore shallow habitats for shark species conservation efforts.

Another potential factor contributing to the higher-observed abundance of sharks in shallow samples could be due to vertical movement on the reef in a diurnal cycle; Vianna,

Meekan, Meeuwig and Speed (2013) identified a cyclical pattern of depth use by C. amblyrhynchos, with use of shallower waters during the day and deeper sites at dusk and during the night. Diel patterns of spatial use by reef shark species have been documented in other studies as well, using both BRUVs and acoustic telemetry (Barnett, Abrantes, Seymour & Fitzpatrick

(2012); Field, Meekan, Speed, White & Bradshaw, 2010). Papastamatiou et al. (2010) found a similar diel influence in blacktip reef shark movements in the Palmyra Atoll, and the majority of sharks observed throughout Penemu and Dampier areas in this study were blacktip reef sharks.

My study sampled exclusively during daylight hours, avoiding any dawn or dusk effects, so it is possible that the sharks sampled during the day came from deeper waters.

The pronounced depth-effect in abundance may also indicate the impact of fisheries. I believe the probable fishery-related effect is that these shallow shark populations (2 - 12 m) may be less affected by fishing than the deeper sites and populations (> 15 m), as the majority of fishing activities happen off-shore; this includes local hand-lining, subsistence fishing, as well as larger scale fisheries where sharks may be caught in nets as by-catch, or in shark-targeting long- lining fishing vessels. Because blacktip reef sharks (the primary contributor to shark populations observed in this study) spend the majority of their time preferentially in shallow reef flat and sheltered lagoon habitats (Papastamatiou et al., 2010), they would be less affected by such fisheries activities. Although depth refuge for fish populations has been identified for coral reef fisheries where fishing methods preferentially target the shallowest depths (Goetze, Langlois,

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 51

Egli & Harvey, 2011; Lindfield, McIlwain & Harvey, 2014). Given the reach of deep-sea fisheries surpassing the maximum depth attainable by chondrichthyans, deeper waters are no longer a refuge for sharks (Priede et al., 2006). In order to protect any species, it is necessary to protect it throughout its lifecycle, including pupping/breeding grounds, as well as mating and migratory area. As many sharks move off the reef flats/into deeper waters where they may be more susceptible to fishing as they mature, some of these areas should also be included in NTZs in order to conserve the breeding adult populations.

The beginnings of positive impact of protected areas in Raja Ampat also glimmer when looking more deeply at the differences between shark abundance in NTZs and UZs with respect to depth, especially given the observed trend of greater shark abundance within protected zones compared to fished zones in the medium and deep depth groups but not at the shallow depth. It is likely that shark populations in uncommonly fished shallow nursery grounds remain fairly intact in both NTZs and UZs, yet the influence of protection is seen when looking at populations at the deeper depths (which would constitute the loci of fishing efforts in UZs).

Shark Diversity Recorded in Raja Ampat The shark diversity observed in this study may be a preliminary indication of the importance of Raja Ampat as a haven of biodiversity for regional shark populations, mirroring its importance as the heart of coral and reef fish biodiversity in the Coral Triangle (Allen &

Erdmann, 2012). The number of shark species observed in the study (nine from five families in only one month and two areas) was considerably greater than that recorded in Fiji where five species from three families were observed in one month (Goetze & Fullwood, 2013). In comparison 21 species were identified (from five families) in Australia’s Great Barrier Marine

Park, however this was recorded over a ten-year period (Espinoza et al., 2014). It is expected that

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 52 if sampling continues over a longer time period, a greater number of shark species will be observed. Considering the variety of habitats and depths sampled: this study in Raja Ampat was limited to primarily reef habitat between 2 – 80 m with 328 BRUVs, whereas Espinoza et al.

(2014) sampled a range of habitat types (including reefs, inter-reef areas, shoals and lagoons) between 7 – 115 m with over 2400 BRUVs. Another distinctive difference with respect to the shark diversity sampled with these two studies is the lack of Carcharhinus melanopterus on the

GBR (1 individual in 2471 BRUVs), though it was noted that logistical constraints prevented sampling of habitat commonly used by these blacktips, thus potentially underestimating their abundance (Espinoza et al., 2014).

Seven of the shark species observed in this study have been previously recorded in Raja

Ampat (Appendix 2); with an additional 15 species are known to inhabit this region, yet were not observed during this study. The most likely explanation for this is that this study only sampled the areas of Penemu MCA and Dampier MPA, which together comprise only 32 % of the total area in protection within Raja Ampat (Appendix 1). With this qualifier, I consider the methodology to be a great success, sampling 41 % of the known species to the region in only 32

% of the area within a period of one month (compared to the lifetime record list of previously observed species). BRUVs sampling will be conducted in the remaining MPAs in Raja Ampat to provide a more complete picture of the shark population metrics and richness for the entire region. The species richness sampled with the BRUVs method supports the implementation of this protocol for future use as the basis for shark monitoring programs.

Another level of explanation for unobserved species that may be present likely relates to the species of sharks themselves. The unobserved sharks can be broken into three general categories related to their generalized habitat and behaviour to help explain their absence in this

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 53 study: (1) several of the species are predominantly ground-dwelling (including Orectolobus ornatus , Chiloscyllium punctatum , Hemiscyllium freycineti and Atelomycterus sp . (Raja catshark)), and due to their limited home range, movement and food preference, would be unlikely to be observed by BRUVs unless their home territory was within the relatively immediate area of the bait dispersal (as may be the case for the two observed in the study:

Eucrossorhinus daypogon and Nebrius ferrugineus ); (2) nocturnally-active sharks, such as the above-named nurse-, bamboo-, carpet- and cat-sharks, would also be less-likely observed due to the fact that the sampling was exclusively done during daylight hours; (3) most of the unobserved species are of the order of requiem or mackerel sharks ( Stegostoma fasciatum (zebra shark),

Carcharinus albimarginatus (silvertip shark), Carcharinus leucas (bull shark), Carcharinus longimanus (oceanic whitetip shark), Carcharinus sorrah (spot-tail shark), Galeocerdo cuvier

(tiger shark), Prionace glauca (blue shark), Sphyrna mokkaran (great hammerhead), Alopias pelagicus (pelagic thresher shark), Isurus oxyrinchus (shortfin mako)) – although many of these species tend to be wide-ranging species, they may not have been observed for a couple reasons: either due to their declining populations on a global scale (most of the species are listed as threatened or near-threatened on the IUCN Red List (Dulvy et al., 2014; IUCN, 2012b); and/or due to the fact that they are not necessarily resident in the area, but previously observed during a migration (as was thought to be the case for the rare observation of the whale shark Rhincodon typus (M. Allen, personal communications)). Additionally, observations of whale sharks would be unlikely with BRUVs (except in an incidental observation, such as the manta rays from this study) as these sharks are primarily filter feeders (Compagno, Dando & Fowler, 2005), and thus should not be attracted by the bait plume. Requiem and mackerel shark families may be more prevalent in the region than sampling in this study show. As these species tend to have large

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 54 ranges without a high degree of territorial overlap, it could explain why those known to the area were not observed, and also provide an alternative possible explanation for their observation in such low numbers with BRUVs.

The fossil shark, Hemipristis elongata and the hooktooth shark Chaenogaleus macrostoma constitute new species distribution records, as they have never been recorded in Raja

Ampat waters before. The sharks were carefully identified by a team comparing video and screen shots to available reference books and diagnostic characteristics for identification, especially the FAO Shark Catalogue (Compagno, 2001). The previously known distribution for

Hemipristis elongata includes the “Indo-West Pacific of South Africa, Madagascar,

Mozambique, Tanzania, Aden, Red Sea, the Persian Gulf, Pakistan, India, Thailand, Vietnam,

China, the Philippines, and Australia (Queensland and Western Australia)” (Compagno, 2001).

The previously known distribution for Chaenogaleus macrostoma includes the “Indo-Pacific from the Persian Gulf to India and Sri Lanka, and off Singapore, Thailand, Vietnam, China

(including Taiwan Province), Java and Sulawesi” (Compagno, 2001). Given the breadth of previously known distribution, which is geographical centered on West Papuan waters, these species are likely native to Raja Ampat, yet due to the lack of previous studies on sharks in the region, these samples constitute the first recorded indication of their existence there. The fact that two new species distributions ( Hemipristis elongata and Chaenogaleus macrostoma ) were recorded in this study also indicate that further studies should be conducted in the area, as Raja

Ampat may constitute a haven of biodiversity for shark species, as it is for fish biodiversity in general (Allen & Erdmann, 2009, 2012), and also supports the case for implementation of the

BRUVs methodology as appropriate for a basis for monitoring shark populations in the area.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 55

Shark Assemblages in Raja Ampat Depth has been found to have a powerful effect on shark assemblages (Guisande et al.,

2013; Menni, Jaureguizar, Stehmann & Lucifora, 2009); contrary to the results of the study by

Espinoza et al. (2014) who found that depth was not a major factor predicting shark assemblages in the Great Barrier Marine Park of Australia. The strong depth effect in shark species richness observed in this study, with greater overall diversity (though lower numbers) at depth, is similar to results from northwestern Australia (Meekan & Cappo, 2004; Meekan et al ., 2006). Meekan et al. (2006) found less than half the total shark species observed occurring in shallow BRUVs in

Australian MPAs.

The difference in the make up of assemblages of sharks found at the different depths is notable. The sharks dominating the entire study, but especially the samples in shallow waters

(most notably Carcharhinus melanopterus, but also Nebrius ferrugineus and Triaenodon obesus ) are reef sharks that have been shown to exhibit site-fidelity to some extent (Bond et al., 2012;

Espinoza et al., 2014; Papastamatiou et al., 2010; Rizzari, Frisch and Magnenat, 2014). Sharks found in the deeper samples in this study also included larger, wider-ranging species as well as rare species (most of the species are listed as threatened or near-threatened on the IUCN Red List

(Dulvy et al., 2014; IUCN, 2012b)). Species targeted in global shark-fin fisheries tend to be the larger, deeper-water dwelling pelagic/oceanic sharks (Maguire, Sissenwine, Csirke, Grainger, &

Garcia, 2006; Oceana, 2010; Vannuccini, 1999; Whitecraft et al., 2014), some of which were observed in this study. This provides excellent justification of the need to include a variety of depths within NTZs intended to contribute to shark conservation, as it could help protect the entire range of shark species in a region.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 56

Blacktip reef sharks ( Carcharhinus melanopterus) are the dominant species for structuring shark assemblages in this study. The blacktip reef shark was first described in the scientific literature by Quoy and Gaymard [1824], and has been extensively studied in other areas within its range. Blacktip reef sharks are commonly the mostly abundant generalist apex predators in many coral reef dominated locations (Compagno et al., 2005). As such, they could play a key role in assessing shark populations in an area. This may be important in that, if they perhaps play a main role in top-down predator control (Vignaud et al., 2014), they would have a significant influence on fisheries and could be used as an indicator of the state of certain fisheries in an area. Though their populations are not in immediate danger of significant depletion globally, blacktip reef sharks are considered near threatened (NT) by the IUCN (IUCN, 2012a), and listing on the IUCN Red List warrants their protection. Studies from other parts of the Indo-

Pacific region have found probable fishing pressures on these and other reef sharks (Field et al.,

2010; Heupel et al., 2009; Robbins et al., 2006; Vignaud et al., 2014), further making the case for urging protecting the pocket of abundance of Carcharhinus melanopterus found in Raja Ampat.

Blacktip reef sharks are one of several species of shark that have been studied to show a high degree of site-fidelity (Chin, Tobin, Heupel, & Simpfendorfer, 2013; Mourier et al., 2013;

Papastamatiou et al., 2010; Vignaud et al., 2014), lending them to protection through MPA no- take zones.

Many shark species have been shown to exhibit habitat preferences. Rizzari et al. (2014b) concluded that reef sharks showed non-homogeneous use of habitats. The most abundant species found in this study ( Carcharhinus melanopterus, Nebrius ferrugineus and Triaenodon obesus ) have “ distinctive, yet over-lapping habitat associations with coral reefs” (Vignaud et al., 2014).

It is recommended that future studies also assess habitat use of sharks taking into consideration

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 57 depth-use patterns in order to prove that habitat is not driving the influence in shark assemblage structures.

Significance of the Research and Implication for Conservation Efforts This study advances research into shark populations and is relevant to current conservation ecology and marine protected area management. The results of this study will have extensive practical applications and future benefits in Raja Ampat. Information on the current status of shark populations is needed to test effectiveness of marine protected area management in the future, and will have implications for adaptive management with respect to zonation, enforcement, outreach and education programs in the region. The results of the study constitute an original contribution to the theoretical knowledge in the field of shark conservation and could serve as a case to strengthen support and justification for adoption of similar management strategies in other location in Indonesia and worldwide as a means for protection of shark populations.

Ensuring effective marine protection for shark species is a multi-faceted undertaking, which should be based on sound science. The establishment of MPAs, zonation, management plans and enforcement should be complimented with capacity-building, outreach and education programs. In order to achieve the above, an understanding of the shark populations is required.

Assessing populations inside and outside no-take zones within the MPAs and at varying depths using BRUVs provides a good start to understanding the population dynamics of shark species in the region, but could be augmented by acoustic telemetry studies to garner a more in-depth understanding of the shark species movements, their range, habitat use and foraging ecology.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 58

Lessons and Recommendations for Studying Shark Populations in Raja Ampat The BRUVs methodology and sampling protocol were found to be an efficient and cost- effective means of monitoring shark populations in Raja Ampat. While BRUVs are a good, fisheries-, and diver-independent approach to assessing the effect of spatial closures in protected area management on shark species, adoption by the local Papuan monitoring team presents a challenge: they proved highly competent at conducting the field work itself, but the incredibly time-consuming data management and highly complicated data analysis cannot be done without extensive guidance and dedicated time in their annual workplan.

The advantages of BRUVs are that compared to other methods used to assess shark populations (i.e. long lines, etc.), BRUVs: produce the greatest accuracy of results, are fisheries- independent and thus are the least invasive to shark populations, are non-destructive to habitat, maximize range of use and carry the fewest additional bias. BRUVs have been found to sample greater species richness and obtain greater estimates of relative biomass of generalist carnivores than diver-operated video methods (Langlois et al., 2010). This may be as a result of one of the main advantages of BRUVs: the absence of shark diver-avoidance behaviour, which may confound abundance estimates, and is inherent to underwater visual census (UVC) techniques

(Cappo et al ., 2004; Willis et al., 2000), though Rizzari, Frisch and Connolly (2014) found there to be no diver-influence in reef sharks in a survey in Australia. Brooks et al. (2011) found that

BRUVs and long-line catch survey methods generated similar values of species richness, with long-line surveys being more efficient. However, capture surveys cause physiological stress and mortality to sharks (Skomal, 2007; Skomal & Mandelman, 2012), and due to the conservation focus of this research and the fishing regulations forbidding shark capture in the study area, longline surveys were inappropriate for studying these MPAs. In addition, given the findings that

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 59 a greater number of shark species were found below conventional scientific diving depths (< 30 m), UVC cannot be used to assess deeper waters. Although UVC has been used to sample reef sharks on the GBR (Robbins et al., 2006), it is likely that diversity would be underestimated.

Although the use of BRUVs has many advantages, potential biases may exist with the technique as well. Notably, the ‘area of attraction’ to the bait bag is unknown, thus making highly accurate density calculations impossible (Cappo et al., 2007). It is also not known whether sharks exhibit bait-preference, or altered behaviour in interactions in the presence of a bait-bag, thus this technique can only provide a relative estimate of abundance of shark populations. Potential bias also exists in the data analysis component of the study. Tape analysis by different enumerators has the potential to cause inconsistency in the data collected through misidentification of species or counting, but the tapes are a permanent record of data and can be independently re- interrogated to ensure this does not occur. A greater limitation is the time requirement for the

BRUV tape interrogation and data archival, although new software is available and advancing to make this process more efficient (Cappo et al., 2007). The researcher was aware of, and attempted to mitigate for these limitations and potential biases while conducting the research in the field.

The only subsequent improvement to the methodology used in the study would be adoption of stereo-BRUVs setups, as they would provide more-in-depth information about the composition of shark populations. The use of stereo video provides accurate and precise measurements of fish length (Harvey, Shortis, Stadler & Cappo, 2002; Shortis et al., 2009).

Through stereo-BRUVs, size estimates can be made which allow measurement of biomass, and thus insight into demographics of shark populations (for example if size of maturity is known).

Life history (i.e. maximum size and size at maturity, sex structure, residency and movement

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 60 patterns) of any given shark species may vary with environmental factors and geographic location

(Chin et al., 2013; Mucientes, Queiroz, Sousa, Tarroso & Sims, 2009; Papastamatiou et al., 2010;

Simpfendorfer, Heupel, White & Dulvy, 2011; Simpfendorfer & Milward, 1993), thus although size of maturity for sharks in Raja Ampat may be comparable to other areas in the region, no studies confirm this, and thus estimates of biomass based on stereo-BRUV data would be questionable. Although stereo-video can accurate measures of fish size, Santana-Garcon et al.

(2014) found highly mobile pelagic species, such as sharks, were difficult to measure with great accuracy due to their observance farthest from the camera systems. Stereo-video systems are also more complicated, requiring multiple specialized cameras and additional three-dimensional calibration software and expertise, and as such represents highly increased costs, neither of which are practical for application in this region at this time.

The BRUVs methodology and sampling protocol developed for this study should be adopted as the standard monitoring procedure for shark populations within the Marine Protected

Areas and Shark Sanctuary of Raja Ampat, and incorporated into the local marine science monitoring program work plan on a bi-annual basis with a dedicated expert project leader. The data collected from these studies should be complimented by UVC survey techniques which currently include sharks incidentally encountered during reef health and fish biomass surveys and fisher and market resource-use monitoring; the combination of data will thus include both diver- averse species, and species that do not respond to bait (either fishers or BRUVs). Further BRUVs studies are needed to investigate the distribution and variability of sharks within and between other protected areas in Raja Ampat (including Ayau-Asia Islands, Wayag-Sayang/Kawe, Raja

Ampat National (previously West Waigeo), Dampier Strait, Mayalibit Bay, Kofiau and Boo

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 61

Islands, and Southeast Misool) in order to complete the baseline dataset for the region and truly inform adaptive protected area management throughout the region that benefits shark species.

Conclusions This study sets an important baseline to detect changes in shark populations after recent

MPA zonation in two areas of Raja Ampat, West Papua. Depth was identified as an important factor influencing both shark abundance and biodiversity, and should remain a consideration for further studies. It is imperative that the monitoring of shark populations in Raja Ampat continues in order to assess shark populations and the contribution of MPA zonation and no-take zone enforcement on preservation and recovery of regional shark populations.

The results obtained in this study will be shared with Conservation International and BHS partners, PEMDA R4, and the protected areas management planning authorities, including management teams from Dampier Strait MPA and Penemu MCA in particular, in order to inform their management planning. An augmented collaboration between local government, communities, patrol and enforcement teams, as well as local universities should be explored to continue this work.

SHARK POPULATIONS IN MARINE PROTECTED AREAS IN RAJA AMPAT 62

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Appendix 1: Marine Protected Areas in Raja Ampat

Table 1. Raja Ampat Marine Protected Areas, their area and current legal status (under Indonesian law). The two areas included as a focus in this study are highlighted with a double asterix**, while those currently being sampled using this protocol are highlighted with a single asterix*.

Reserve Area Area (ha) Current Legal Status Kepulauan Ayau – Asia 101,440 Perda No. 27 Tahun * 2008 dan Peraturan Bupati No. 5 Tahun 2009 KKPD Kawe * 155,000 Perda No. 27 Tahun 2008 dan Peraturan Bupati No. 5 Tahun 2009 KKPD Teluk Mayalibit 53,100 Perda No. 27 Tahun 2008 dan Peraturan Bupati No. 5 Tahun 2009 KKPD Selat Dampier 336,200 Perda No. 27 Tahun ** 2008 dan Peraturan Bupati No. 5 Tahun 2009 KKPD Kofiau dan Boo 170,000 Perda No. 27 Tahun * 2008 dan Peraturan Bupati No. 5 Tahun 2009 KKPD Misool Timur- 343,200 Perda No. 27 Tahun Selatan * 2008 dan Peraturan Bupati No. 5 Tahun 2009 SML Kepulauan Raja 60,000 Ditetapkan dengan SK Ampat Menteri Kehutanan Penemu-Bamboo MCA 69,828 Peraturan Kampung ** Fam Saukabu Desember 2012 TOTAL 1,288,768

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Appendix 2: List of Shark Species Recorded in Raja Ampat

Table 2. List of all shark species that have been observed and reported in Raja Ampat, including scientific classification, latin name, common name, and Indonesian common name (Part 1 Adapted from Allen & Erdmann, 2009). An asterisk * denotes a species observed in this study.

1. Sharks recorded from Raja Ampat

Class: Chondrichthyes Subclass: Elasmobranchii Subdivision Selachii (modern sharks) Order Orectolobiformes (carpet sharks) Family Orectolobidae (wobbegongs = hiu berbunga) Eucrossorhinus daypogon (tasseled wobbegong)* Orectolobus ornatus (ornate wobbegong) Family Hemiscyllidae (bamboo sharks = mandemor, kalabia) Chiloscyllium punctatum (brown-banded bamboo shark) Hemiscyllium freycineti (Raja Ampat walking shark = kalabia, mandemor) Family Ginglymostomatidae (nurse sharks) Nebrius ferrugineus (tawny nurse shark)* Family Stegostomatidae (zebra sharks) Stegostoma fasciatum (zebra shark) Family Rhincodontidae (whale sharks = gorano bintang, hiu bodoh) Rhincodon typus (gorango bintang) Order Carcharhiniformes (ground or requiem sharks) Family Scyliorhinidae (catsharks) Atelomycterus sp . (Raja catshark) Family Carcharhinidae (reef and requiem sharks like blacktip) Carcharinus albimarginatus (silvertip shark) Carcharhinus amblyrhynchos (grey reef shark)* Carcharinus leucas (bull shark) Carcharhinus limbatus (blacktip shark)* Carcharinus longimanus (oceanic whitetip shark) Carcharhinus melanopterus (blacktip reef shark)* Carcharinus sorrah (spot-tail shark) Galeocerdo cuvier (tiger shark) Prionace glauca (blue shark) Triaenodon obesus (whitetip reef shark)* Family Sphyrnidae (hammerhead sharks = hiu martel) Sphyrna lewini (scalloped hammerhead)* Sphyrna mokkaran (great hammerhead) Order Lamniformes (mackerel sharks) Family Alopiidae (thresher sharks) Alopias pelagicus (pelagic thresher shark) Family Lamnidae (mackerel sharks) Isurus oxyrinchus (shortfin mako)

2. Sharks observed in this study not previously recorded from Raja Ampat Class: Chondrichthyes Subclass: Elasmobranchii Subdivision Selachii (modern sharks) Order Carcharhiniformes Family Hemigaleidae Hemipristis elongata (snaggletooth shark)* Chaenogaleus macrostoma (hooktooth shark)*

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Appendix 3: Shark Monitoring Protocol for Raja Ampat MPA Network using baited remote underwater video stations (BRUVS)

Version 2.0

Revised by Angela Beer & Steve Lindfield upon completion of CI BRUVS R4 Shark Monitoring Trip – January 2014

Purpose

This document provides technical specifications and instructions for conducting BRUVS (baited remote underwater video stations) monitoring in Raja Ampat.

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Introduction

Sharks are essential elements for healthy marine ecosystems and require conservation.

While a new law has been passed for their protection in Raja Ampat, there is a lack of knowledge about their current status in the region. These survey techniques will quantify diversity and relative abundance of shark populations in Raja Ampat, Indonesia to provide a comprehensive baseline for the area to evaluate management strategies. Surveys of shark populations in no-take zones and fished areas, and across gradients of depth and geographic locations will provide important knowledge on the distribution of these valuable, yet poorly understood apex predators in Raja Ampat, West Papua.

Among available methods used to assess shark populations, BRUVS (baited remote underwater video stations) are a non-destructive method that can be deployed over a large depth range. This method has been successfully used to quantify shark populations around world (Bond et al., 2012; Brooks et al., 2011; Goetze & Fullwood, 2013; Meekan & Cappo, 2004). The use of bait can attract the sharks and compared to diving surveys, the remote camera avoids any behavioral effects of sharks avoiding divers. The use of multiple BRUVS simultaneously can also increase the sampling replication and coverage compared to other techniques. BRUVS also provide a permanent video record that can help with species identification and re-analyzed for additional data.

Background This protocol document, builds on a previous BRUVS pilot study conducted in April

2013 (Cerutti-Pereyra, 2013). This study expands on the previous study by incorporating recommendations but improves efficiency and replication by utilizing a structured hierarchical design with BRUVS replicates grouped within sites, depth groups, MPA status and areas. This

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allows robust statistical analysis between these factors of interest and creates a dataset that can be used as a baseline on shark populations in R4 to monitor changes over time. This dataset is also highly comparable to other regions around the world where similar sampling designs have been implemented (i.e.Australia, Mariana Islands, Fiji and Palau) and can be used in worldwide meta-analysis studies on shark abundance.

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BRUVS design and preparation

Building upon previous designs, especially those by the Australian Institute of Marine Science (AIMS) (Harvey et al., 2012; Cappo et al. 2004), customised, lightweight BRUVS were built locally for the pilot version of this study in Raja Ampat (Figures 1, 2).

Each frame has an attachment of a bait-bag at the end of a detachable 1.5m-long PVC pole. Each BRUVS has attached a rope and surface float.

Ropes should be 7mm floating polypropylene rope. The length of rope should be at least 1.5x the max depth of water sampled. For example in the January 2014 study, mid depths (20-30m) required ropes of 45m length. In strong currents or deep deployments, 2 surface floats should be used.

Bait bags should be attached semi-permanently to the PVC pole with cable ties. Bait bags are plastic coated wire and red in colour. These can be open and closed by bending by hand and bait replaced by placing the pole upright in a bucket. Bait bags were purchased in Australia, but have since have been sourced locally, and are standard use for other BRUVS surveys.

Bait should be purchased in bulk at the start of the trip from local markets (preferably skipjack tuna - Katsuwonus pelamis ). Allow 800g -1kg per BRUVS deployment. Bait should be defrosted overnight, then cut and crushed before placing into bait bag. GoPro cameras (Hereo 3 or 3+) were utilised in this study and provided a wide field of view and high definition quality needed for BRUVS. Settings: o 1920x1080 resolution, o Wide setting, o 25 fps (PAL format) • These settings can provide 1hr 40mins of footage on an 8GB SD card and was the optimal balance between quality and video size. • Time and date should be set on each camera at the start of the trip.

Fig. 1: Photograph of BRUVS on seafloor (Image credit: Steve Lindfield)

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Fig. 2. Design by Tertius (Papua Divers). Note: steel pegs at the bottom of the BRUVS were removed and not included for new BRUVS.

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Sampling design

January 2014 study:

This study utilised a structured hierarchical design with BRUVS replicates grouped within sites, depth groups, MPA status and area. This will form the basis for Angela Beer’s MSc. thesis and provide a through baseline for future BRUVS surveys in Raja Ampat. The level of replication (30 BRUVS per factor of interest) was decided from power analysis on shark abundance at other locations (Mariana Islands) and consistent with other researchers in Hawaii. The use of 3 replicates per site and 10 sites was used in order to have more representative sampling of large areas (rather than the originally planned 5 sites and 6 replicates per site) and can allow the pooling replicates to Site level with some degree of statistical power.

The full design consisted of 4 factors: • Area: o Dampier Strait o Wayag/Kawe o PyaiNemo/Fam • Fishing Status: o No-Take Zone (NTZ) o Use-Zone (UZ) • Depth: o Shallow (2-10m) o Mid (20-30m) o Deep (50-80m) • Site o 10 sites selected haphazardly o Sites separated by at least 1.5km o 3 replicates per site, per depth group (i.e.9 BRUVS per Site) o BRUVS replicate samples separated from each by approximately 500 m.

Note : During the Inbekwan cruise from the 16 th -31 st January 2014, at the Penemu (PyaiNemo)/Fam area, only the mid depth was sampled. Deep and shallow depths will be sampled the following month by Angela Beer with assistance from Sea Sanctuaries Trust.

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Due to logistical reasons, 10 BRUVS were generally deployed at each site (1 more than the required 9). As each speedboat can carry 5 BRUVS, then 2 sets of 5 were deployed so the boat does not need to travel between sites. The extra BRUVS (generally deployed at the mid depth) can be used if there was any problem such as a BRUVS falling over and view being obstructed.

Future sampling design

Depending on the results of January 2014 BRUVS survey, the sampling design may change. If there is little difference in shark abundance and diversity between depths, then future monitoring may just focus on one depth (mid depth: 20-30m). Additional power analysis on this survey will determine if the level of replication is adequate to assess change over time. o Focusing on one depth group (i.e.mid depth) will allow faster sampling and post processing and can allow more temporal replication o It is recommended to repeat this sampling design annually at the same time of year (January) o In addition, if time permits one area may be chosen for regular sampling both within seasons (weeks apart) and between seasons (6 months apart). This can partition differences between short term temporal variation and variation between seasons o Sampling should be expanded to include other areas such as Misool o If sampling only the mid depth, then it is recommended for each speedboat to carry 6 BRUVS, therefore during one set of deployments can sample 2 sites (with 3 replicates per site).

Mono-BRUVs (systems with a single camera) were used in the January 2014 survey, although the use of stereo- BRUVs is becoming more widely utilised. Stereo video provide the means to standardise sampling area, as well as calculate fish size and biomass. Such technology could be implemented in future surveys if budget constraints allow.

Field work It can be expected that 20 BRUVS can be deployed per speedboat each day. A minimum of 15 deployments should be completed, with the probability of 25 deployments if starting early and good weather conditions. Three teams of three people each should be formed, and work in rolling tasks: 2 teams will be on the water for the day (in speedboats 1 & 2); 1 team will be on the mothership doing logistics preparation, data entry and analysis.

Process Summary

• The sampling site should be chosen from GIS or Google earth and given a Site name (i.e.DUZ-01); A waypoint is created (using site name) centred on coordinates at the approximate centre point of the site then uploaded into the GPS for each team. • An overall site sampling map is produced, as well as a planned schedule of which teams are sampling which sites each day. Teams need to be familiar with what Sites they need to sample each day. • At each site, 3 BRUVS should be deployed at each depth, each spaced a minimum of 500m apart. The GPS is used to show distance from the nearest surrounding BRUVS locations. • Ideally 2 sets (10 BRUVS) can be completed in the morning and 2 sets (10 BRUVS) can be completed in the afternoon.

Process details: Following the January 2014 trip with the Inbekwan

• Sequence of activities for each MORNING. 1. Ensure all batteries fully charged 2. Prep one set of cameras with SD cards and batteries loaded into housings, placed with extra housings into housing box (“Milo Box”) 3. Prepare each speedboat camera box with the following:

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a. Enough cameras, memory cards and extra batteries for the team’s planned sites (i.e.20 cards and 20 batteries). b. GPS with freshly charged batteries and extra set of batteries c. 1 set small cable ties d. 2 sharp pencils 4. Prepare each speedboat drybox with the following: a. 1 clipboard with enough data sheets to complete the planned sites (i.e. 4 sheets) and a list of the sites to be sampled b. 1 portable depth sounder c. 2 shammies and one super-dry towel d. 1 exacto-knife cutter e. 1 multi-tool knife f. 2 sets of cable ties (1 releasable; 1 permanent) g. Permanent Marker h. Duct tape i. Fishing nylon j. 1 thermometer k. 1 segidisk l. 1 current meter m. 1 salinometer n. snacks for the day; pocari sweat electrolyte replacement packets o. 2 extra spark plugs 5. Prepare each speedboat with the following: a. 1 HT Radio with charged battery b. 1 speedboat camera box (as above) & 1 speedboat housings box c. 1 speedboat drybox (as above) d. 1 bucket of fresh water e. 1 bucket of bait fish (enough for day’s activities- i.e. 20kg) f. 5 BRUV structures (ensure camera mounts OK & ‘shark’ clips (for bait poles) in place) g. 6 sets of bait poles and bags h. Ropes: 5 medium-length (45m); 3 short (12m); 2 long (110m) i. Buoys: 8 j. Enough fuel for day’s activities k. 1 galon drinking water and cup

• Sequence of activities for each DROP SET deployment. 1. Arrive at planned site using the proposed GPS coordinates 2. Cut bait and prepare bait bag/pole 3. Check depth using sounder 4. Record replicate info, BRUVS & Camera ID# on datasheet 5. Prepare camera, on, recording video 6. Film data sheet (point to replicate name) 7. Deploy one BRUVS (ensure speed maintains position with rope straight down, when structure reaches depth, readjust to ensure upright) 8. Mark a GPS waypoint (using Site name plus replicate; i.e. DUZ-01-S1) and Record GPS WP# / coord of deployment site and time on datasheet 9. Fill in additional information on datasheet 10. Confirm that buoy is visible (if strong current, attach another buoy) 11. Check temperature, visibility and current at least once per SITE, fill in datasheet 12. Go to next site and repeat

• Planned sequence of activities for recoveries (After the 5 th BRUVS is deployed).

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1. After 60min from time of first deployment return to 1st deployment location using the GPS coords 2. Retrieve the BRUVS structure 3. Rinse the camera in fresh water 4. Replace camera’s battery 5. Replace camera’s SD card 6. Fill in datasheet with data of battery and SD card 7. Move to next site and repeat if time allows

• Sequence of activities for END of Day : 1. Recharge all batteries (cameras, GPS, HT Radios) 2. Ensure all SD cards downloaded into the relevant folders on hard drive 3. Ensure all videos backed-up on two separate hard drives 4. Format memory cards ready for next day 5. Ensure all GPS points from drops downloaded from units and synchronized 6. Make a plan for the next day (organize which teams to which site) 7. Ensure GPS points for following day uploaded to GPS units

References

Cerutti-Pereyra, F. 2013. Monitoring protocol for assessing sharks and rays assemblages using baited remote underwater video surveys (BRUVS). Version 1.0 CI Indonesia Marine Program Report. 16 p.

Analysis

For more detailed information on the analysis of BRUVs data, see Raja Ampat BRUVs Monitoring Analysis Standard Operating Procedure (SOP) (Parts 1 – 3) . Video analysis

• 60 minutes of each video will be analysed from the moment the BRUVS settles on the bottom. Analysis will use EventMeasure software from SeaGIS. Data analysis

• Interrogation of each tape provided the time the BRUVS settled on the seabed and, for each shark: its species; the time of first sighting; time of first feeding at the bait; a coarse initial estimate of length; and a list of fish species. This enabled the identification of different sharks on each tape for cumulative summaries of shark visits (MaxN) to be developed for each BRUVS set. Coarse measurements of the total length of the largest individuals of some species were made by comparing them with the scale grids on the bait arm (Meekan & Cappo, 2004)

• To avoid repeat counts of individual sharks continuously re-entering the field of view, the maximum number of individuals of the same species appearing at the same time (MaxN) was used as a relative abundance measure. MaxN is a conservative estimate of relative abundance, which is essential as the variability in attraction of the bait has the potential to overestimate abundance (Dorman et al., 2012)

• All shark species are counted as well as the time of their first arrival (t1st) and the maximum number viewed at any one time (MaxN). Sharks will only be recorded if they come within an estimated 5 m from the bait. (This may be adjusted, but kept consistent, depending on the minimum visibility recorded during the study.)

• PERMANOVAs were used to test species richness and relative abundance using the numbers of individuals (sum of MaxN’s) averaged to the site level. For these univariate measures, a Euclidean distance measure on fourth-root transformed data was performed (Harvey et al., 2012)

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References (Shark Monitoring Protocol Doc)

Bond, M. E., E. A. Babcock, E. K. Pikitch, D. L. Abercrombie, N. F. Lamb, and D. D. Chapman. 2012. Reef Sharks Exhibit Site-Fidelity and Higher Relative Abundance in Marine Reserves on the Mesoamerican Barrier Reef. PLoS ONE 7:e32983. Brooks, E. J., K. A. Sloman, D. W. Sims, and A. J. Danylchuk. 2011. Validating the use of baited remote underwater video surveys for assessing the diversity, distribution and abundance of sharks in the Bahamas. Endangered species research 13 :231-243. Dorman, S. R., E. Harvey, and S. J. Newman. 2012. Bait Effects in Sampling Coral Reef Fish Assemblages with Stereo- BRUVs. PLoS ONE 7:e41538-e41538. Goetze, J. S., & Fullwood, L. A. F. (2013). Fiji’s largest marine reserve benefits reef sharks. Coral Reefs, 32(1), 121–125. doi:10.1007/s00338-012-0970-4 Harvey, E. S., S. R. Dorman, C. Fitzpatrick, S. J. Newman, and D. L. McLean. 2012. Response of diurnal and nocturnal coral reef fish to protection from fishing: an assessment using baited remote underwater video. Coral Reefs 31 :939-950. Meekan, M. and M. Cappo. 2004. Non-destructive Techniques for Rapid Assessment of Shark Abundance in Northern Australia. . Australian Government and AIMS, Townsville.

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Appendix 4: Annotated Bibliography

Bond, M. E., Babcock, E. A., Pikitch, E. K., Abercrombie, D. L., Lamb, N. F., & Chapman, D. D. (2012). Reef Sharks Exhibit Site-Fidelity and Higher Relative Abundance in Marine Reserves on the Mesoamerican Barrier Reef. (V. Laudet, Ed.) PLoS ONE, 7(3), e32983. doi:10.1371/journal.pone.0032983 A study similar to the research herein (different geographical focus). The BRUV methodology and raw data was clearly described and provided a good idea of the challenges that might be expected during field work and data collection. The Bond study also implemented a mixed-methods approach, using acoustic tagging to enhance the data from BRUVs; this combination allowed demonstration of site-fidelity in addition to the positive correlation of abundance to management status. This may be a “next step” for research in Raja Ampat.

Cappo, M., De’ath, G., Stowar, M., Johansson, C., & Doherty, P. (2009). The influence of zoning (closure to fishing) on fish communities of the deep shoals and reef bases of the southern Great Barrier Reef Marine Park. Part 2 - Development of protocols to improve accuracy in baited video techniques used to detect effects of zoning. Report to the Marine and Tropical Sciences Research Facility. Cairns: Reef and Rainforest Research Centre Limited. Contains excellent detail on protocol development for BRUVs as well as key notes for avoiding bias in the design and sampling strategy.

Goetze, J. S., & Fullwood, L. A. F. (2013). Fiji’s largest marine reserve benefits reef sharks. Coral Reefs, 32(1), 121–125. doi:10.1007/s00338-012-0970-4 Recent study contributing to knowledge positive correlational relationship between management status and shark populations; sharks benefit from reserves. Highly pertinent to current research in terms of potential practical application.

Mangubhai, S., Erdmann, M. V., Wilson, J. R., Huffard, C. L., Ballamu, F., Hidayat,….. Wen, W. (2012). Papuan Bird’s Head Seascape: Emerging threats and challenges in the global center of marine biodiversity. Marine Pollution Bulletin , 64(11), 2279–2295. doi:10.1016/j.marpolbul.2012.07.024 This is the most comprehensive article about the status of the marine realm and conservation initiatives and issues in Bird’s Head Seascape in Eastern Indonesia, which includes Raja Ampat. References several of the programs I have been working on over the past few years! ***Also the key “call to arms” delineating the need for the current research and situating it within the context of shark conservation in Raja Ampat.

Robbins, W. D., Hisano, M., Connolly, S. R., & Choat, J. H. (2006). Ongoing Collapse of Coral-Reef Shark Populations. Current Biology, 16(23), 2314–2319. doi:10.1016/j.cub.2006.09.044 Furthers the information on the importance of marine reserves for shark protection, showing true ‘no-go’ zones (not just no-take) or enforced no-take zones are needed to slow the decline of shark populations. Posits a new hypothesis that greater shark abundance in reserves may not be due to decreased fishing pressures, but site fidelity due to availability of food source – interesting idea.

Worm, B., Davis, B., Kettemer, L., Ward-Paige, C. A., Chapman, D., Heithaus, M. R., Kessel, S. T., et al . (2013). Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy , 40 , 194–204. doi:10.1016/j.marpol.2012.12.034 This is the most recent, most comprehensive study on the state of the world’s shark populations to date. It paints a dire picture, and makes the research herein feel increasingly urgent. It is timely in that it was published just prior to the Plenary meeting of the IUCN, where 5 species of sharks were added to the CITES Appendix II list of species which are under threat and now, formally forbidden for international trade.

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Appendix 5: Abbreviations

ANOVA – Analysis of variance BHS – Bird’s Head Seascape (BHS); a region in Eastern Indonesia BRUVS – Baited Remote Underwater Video Station CII – Conservation International Indonesia CII-R4 – Conservation International Indonesia, Raja Ampat Program df – Degrees freedom F – F-ratio GBR – Great Barrier Reef (of Australia) GPS – Global Postioning System IUCN – International Union for the Conservation of Nature km – Kilometers m – Metres min – Minutes mm – Millimetres MCA – Marine Concession Area MPA – Marine Protected Area n – Sample size nMDS – Non-metric Multidimensional Scaling P – Probability level PEMDA R4 – Pemerintah Daerah Raja Ampat (in Indonesian); translated: Raja Ampat Regional Government PERMANOVA – Permutational multivariate analysis of variance PRIMER-E – A multivariate statistical software package SCUBA – Self Contained Underwater Breathing Apparatus SE – Standard error (standard deviation / square root of sample size) SIMPER - Similarity percentages t - t-statistic (ratio of the coefficient to its standard error) UVC – Underwater Visual Census