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Friday, 2 December 2016
First records of the reef manta ray Manta alfredi in the Bohol Sea, Philippines, and its implication for conservation
Published Date 1 December 2016, Vol.9(4):489–493,doi:10.1016/j.japb.2016.07.002 Open Access, Creative Commons license,Funding information Short Communication Author
Joshua Maniriniaina Rambahiniarison,
Gonzalo Araujo
Mary Jane Lamoste
Jessica Labaja
Sally Snow
Alessandro Ponzo
Large Marine Vertebrates Research Institute Philippines, Cagulada Compound, Tejero, Jagna, 6308, Bohol, Philippines
Received 9 May 2016. Revised 22 June 2016. Accepted 1 July 2016. Available online 20 July 2016.
Abstract
We report the occurrence of the reef manta rayManta alfrediKrefft 1868 in the Bohol Sea, Philippines, based on photographic evidence from boat-based surveys and a fishery specimen. Despite previous anecdotal reports from the diving industry and over a century of extensive targeted fisheries for mobulid rays in the Philippines, it was not until recently that the species was first confirmed in the country at the Tubbataha Reefs Natural Park, Palawan. Our results confirm the presence ofM. alfrediin the Visayas region of the Philippines, extending the current range for the species from the Sulu Sea over 600 km eastwards. Its presence in a region with an active mobulid fishery has important implications for the conservation and management ofM. alfrediin the country. We highlight the need to understand the distribution ofM. alfrediin the region and make management recommendations based on the present study.
Keywords
Bohol Sea
fisheries
Manta alfredi
Mobulidae
Philippines
Introduction
Mobulids (family Mobulidae), commonly referred to as devil rays, are cartilaginous fishes (Chondrichthyes) found circumglobally in tropical, subtropical, and warm temperate waters. These pelagic species exhibit low fecundity and slow maturation; however, their life history remains poorly understood, while these species are highly exploited worldwide (Croll et al 2015). This family includes the genus Manta and the genus Mobula with 11 identified species (Couturier et al 2012). In 2009, the genus Manta was reclassified into two separate species; the oceanic manta Manta birostrisWalbaum 1792 and the reef manta Manta alfredi Krefft 1868 (Marshall et al 2009). This separation is reflected both in morphological and ecological differences between the two species. Manta birostris presents very distinctive white shoulder patches shape as a posterior facing hook and the anterior edge of these patches parallel to the edge of the upper jaw, while M. alfredi shoulder patches curve medially (Marshall et al 2009). Differences can be observed on the ventral patterns, where M. alfredipresents dark spots between the gill slits, while M. birostris does not (Marshall et al 2009). Manta birostris is associated with offshore and oceanic environments (Marshall et al 2009), while M. alfredi is generally associated with coastal environments and is more commonly seen by divers in feeding grounds and cleaning stations (Couturier et al., 2012 and Marshall et al., 2009).
Mobulid populations are facing high exploitation worldwide to supply an increasing international trade for their highly valuable gill rakers (Croll et al., 2015 and Dulvy et al., 2014). Their aggregation sites make them an ideal target for wildlife watching tourism, as well as unregulated and illegal fisheries. Moreover, because of the slow population growth of these species (Dulvy et al 2014) any fishing pressure would increase the risk of local extinction (Dulvy et al 2014). Manta alfredi is already classified as “vulnerable” in the International Union for Conservation of Nature Red List (Marshall et al 2011). In the Philippines, unregulated fisheries have targeted mobulids for over a century for local consumption (Acebes, 2013 and Alava et al., 2002) and, more recently, also to supply the gill raker trade (Acebes 2013). Despite fishing for M. birostris being banned in 1998 by the Fisheries Administrative Order 193 (FAO 193) and the recent listing in the Convention on International Trade in Endangered Species (CITES) Appendix II (https://www.cites.org) of both species of Manta, unselective fisheries around the Bohol Sea still remain unregulated. Today, the town of Jagna in the southeast of Bohol Island remains the main dedicated mobulid fishery and landing site in the Philippines, with over 2,000 mobulids landed per season.
The Bohol Sea (9°0′0″N; 124°0′0″E) represents an important habitat for large marine vertebrates such as whale sharks Rhincodon typus Smith 1828 (Araujo et al., 2014and Araujo et al., 2016a), at least 18 species of cetaceans (Ponzo et al 2011), and sea turtles (Araujo et al 2016b). Moreover, due to a seasonal upwelling of cold, nutrient-rich water from the deep to the upper layers, important planktonic productivity occurs from November to April in these waters (Cabrera et al., 2011 and Gordon et al., 2011). This coincides with the seasonal occurrence of large planktivorous elasmobranchs, such as mobulids (Rayos et al 2012) and whale sharks (Araujo et al 2016a). After being misidentified as the oceanic manta ray M. birostris, it was not until recently that M. alfredi was confirmed in the Philippines by Aquino et al (2015), at the Tubbataha Reefs Natural Park, east off Palawan Island in the Sulu Sea. With the exception of this publication, information on the occurrence of M. alfredi in the Philippines is lacking, resulting in gaps in the knowledge necessary for the management and conservation of the species. Here, we report the occurrence of M. alfredi in the Bohol Sea as a means to fill these gaps. Moreover, the report of its presence in an active mobulid fishing ground has important implications for the conservation and management of M. alfredi in the Philippines.
Material and methods
Boat-based whale shark surveys (n = 111; Araujo et al 2016a) were conducted between April and June 2013 in the waters off Panaon Island (Southern Leyte) on the eastern entrance to the Bohol Sea (9°54′55″N; 125°16′44″E; Figure 1). The island lays on the eastern shores of Sogod Bay, a key biodiversity area (Ambal et al 2012), reaching depths of over 1,400 m. Opportunistic in-water photo identification (photo ID) data of M. alfredi collected were visually matched and uploaded onto the online database (Table 1) of manta rays “MantaMatcher” (http://www.mantamatcher.org) to verify any possible matches worldwide with other previously identified individuals. Photo ID uses photographs from the ventral side of the manta rays, as individuals can be identified through their unique pattern of spots (Couturier et al., 2011, Couturier et al., 2014, Deakos et al., 2011, Kitchen-Wheeler, 2010 and Marshall et al., 2008) and other characteristic marks (e.g. scars). Photographs also allow the collection of other life history parameters, such as sex, based on the presence or absence of claspers, and in some cases sexual maturity.
Figure 1. Sites of interest in the Philippines. A, Manta alfredi reported sightings across the country; B, mobulid fishing ground (red circle) of the Jagna fishery in the Bohol Sea; C, M. alfrediencounters in Sogod Bay, Southern Leyte for which GPS points were recorded. Other encounters occurred in the same area.
Table 1. Dates, GPS waypoints, MantaMatcher individual ID number, and sex of Manta alfrediencountered in Sogod Bay.
Date
GPS point
MantaMatcher individual number
Sex
Apr 28, 2013
–
PV-MA-0002
Female
May 10, 2013
–
PV-MA-0004
–
May 14, 2013
9°54′665″N; 125°17′293″E
–
–
May 18, 2013
9°54′551″N; 125°16′449″E
–
–
Jun 07, 2013
9°54′349″N; 125°16′991″E
PV-MA-0003
Male
Jun 06, 2013
–
PV-MA-0005
Female
Mobulid fishery monitoring was conducted daily at the fishing port of barangay Bunga Mar (9°38′29″N; 124°22′52″E) in the municipality of Jagna, Philippines (Figure 1) from January 2013 to June 2013, December 2013 to May 2014, February 2015 to June 2015, and from November 2015 to April 2016. Mobulid fishers travel up to 50 km offshore within the Bohol Sea (Figure 1), dropping driftnets at night with up to 8 hours soak time. When specimens were landed, the disc width was recorded to the nearest 0.2 cm following Notarbartolo-di-Sciara (1987), and sexual maturity was assessed following the International Council for the Exploration of the Sea (ICES 2013). Identification of M. alfredi was based on morphological characteristics (Figure 2) provided by Marshall et al (2009) including:
•
Y-shaped black on white-colored shoulder patches on dorsal supra-branchial region;
•
distinctive dark spots on the ventral surface medially between the gill slits; and
•
no distinct caudal spine or calcified mass present at the base of the tail.
Figure 2. Morphological characteristics for the identification of Manta alfredi. A, distinctive dark spots on the ventral surface medially between the gill slits; B, Y-shaped black on white-colored shoulder patches on dorsal supra-branchial region. Both pictures present the specimen encountered on June 7, 2013. The ventral pattern is used for photo-ID.
Results and discussion
During boat surveys in Sogod Bay, 6 individual M. alfredi were photographed and identified on 5 different surveys in 2013. Some individuals were feeding, swimming horizontally with an open mouth, and barrel rolling (Couturier et al 2012). GPS locations were recorded for three of these encounters (Table 1). Manta alfredi and other mobulids, such as Mobula japanica Müller and Henle 1841 and Mobula thurstoni Lloyd 1908 have been encountered occasionally since 2013, but were not photographed.
On November 30, 2015, one M. alfredi specimen was landed in Bunga Mar (Figure 3). This specimen was a mature male with a 329 cm disc width. Fishers reportedly caught it near Pamilacan Island, Bohol. This catch is unusual, as M. birostris was the only manta ray species previously recorded during four seasons of monitoring at this landing site. As this specimen was caught along with three M. birostris individuals, it remains unclear whether the species are sharing the habitat for different purposes as suggested by Marshall et al (2009), or whether they are travelling and/or foraging together.
Figure 3. Photos of Manta alfredi landed on November 30, 2015, in Bunga Mar, Bohol, Philippines. A, whole specimen (1-m-long stick); B, left part of the ventral pattern between the gill slits with dark spots; C, white-colored shoulder patches on dorsal supra-branchial region (1-m-long stick); D, base of the tail with the dorsal fin and the left clasper.
Despite regular fishing trips close to Sogod Bay, and the presence of M. alfredi in the area reported here, no previous catch of this species was ever confirmed. However, this catch underlines the potential threat for the species in the area, based on our monitoring of a single fishery site. GPS tracks from Jagna's fishing boats showed that their main fishing ground lies offshore in the deep waters of the Bohol Sea, while M. alfredi is predominantly a coastal species, spending much of its time on reefs and close to the coast (Kashiwagi et al., 2011 and Marshall et al., 2009). However, previous studies reported offshore movements connecting various aggregation sites or foraging areas for extended distances and times (Braun et al., 2014, Clark, 2010, Couturier et al., 2014 and Jaine et al., 2014). Thus, excursions across the fishing ground may occur, unless movements of individuals are restricted by the bathymetry or the regional oceanography in the area as suggested by Deakos et al (2011). Manta alfredi tends to show deep-water diving behavior at night when moving offshore (Braun et al., 2014 and Clark, 2010), while mobulid fishing boats deploy nets during the night at maximum depths of 40 m, and thus potentially not overlapping. This ecological connection between the surface waters and the mesopelagic zone are known to be linked with feeding behavior when prey migrate from deeper pelagic zones (Gliwicz 1986). Deep foraging dive profiles have also been reported for Mobula tarapacana Philippi 1893 in Azores (Thorrold et al 2014), which could also explain why this species is not caught often by Jagna's mobulid fishing boats in the Bohol Sea. In contrast, smaller mobulids such as M. japanica are reported to spend most of their foraging time at the surface during the night (Croll et al 2012), and M. thurstoni is likely to exhibit similar behavior as these two species represent the most commonly caught species in Jagna.
Examining the habitat use and the distribution of M. alfredi in the Philippines is a priority to be able to assess its vulnerability to existing fisheries. In Sogod Bay, tracking of individual M. alfredi would highlight connectivity with other areas of ecological importance and potentially with this known fishing area.
Manta alfredi is now known to exhibit long-term site fidelity (Couturier et al., 2011, Couturier et al., 2014 and Deakos et al., 2011) with regular and seasonal movements between aggregation area, defining these sites as critical habitats for the species (Couturier et al 2014). This behavior makes local subpopulations extremely vulnerable to anthropogenic threats, especially fisheries and habitat degradation. In Limasawa Island, Southern Leyte, the Magallanes mobulid fishery was hunting in Sogod Bay until the late 1990s when the ban was introduced (Acebes 2013). Considering M. alfredi site fidelity, this century-old targeted fishery is likely to have impacted heavily on M. alfredi subpopulation in Sogod Bay.
Preliminary data from citizen science, including the use of pictures from tourists and divers, indicate the presence of M. alfredi in several other sites across the Philippines including Monad Shoal off Malapascua Island, Cebu, Manta Bowl in Masbate, and in El Nido, Palawan, but dedicated surveys are needed to confirm these reports. Manta alfredi has only been officially reported at Tubbataha Reefs Natural Park (Aquino et al 2015) and the present study represents the first official record from the Visayas region and from the Bohol Sea.
The presence of 2 species of mobulids has previously been confirmed in the Bohol Sea: the oceanic manta ray M. birostris (Alava et al., 2002 and Rayos et al., 2012), and the bentfin devil ray M. thurstoni (Rayos et al 2012). The spinetail devil ray M. japanica and the sicklefin devil ray M. tarapacana are also landed at Bunga Mar, Jagna. The pygmy devil ray Mobula eregoodootenkee Bleeker 1959, has also been reported (Rayos et al 2012) but not confirmed in the Bohol Sea. With the addition of M. alfredi confirmed here, the Bohol Sea hosts one of the highest mobulid diversity reported globally, such as off the Saint Peter and Saint Paul Archipelago (Equatorial Atlantic; Mendonça et al 2012).
Conclusion
Here, we report the occurrence of M. alfredi in the Bohol Sea, extending its range from the Sulu Sea eastwards. The presence of M. alfredi in Sogod Bay adds significance to this key biodiversity area, which should be protected and sustainably managed. Moreover, the recent listing of M. alfredi in the CITES Appendix II reinforces the urgent need to assess the distribution of its populations and to determine the sustainability of the fisheries. The occurrence of this second species of Manta in an area of targeted mobulid fisheries highlights the necessity to protect the species nationally. We therefore recommend the amendment of FAO 193 for the inclusion of M. alfredi. Further efforts are now in place to better assess the presence and distribution of Manta species in the Philippines, in collaboration with national and international non-governmental organizations, and with the support of the national government.
Acknowledgments
We would like to thank members of the KASAKA organization for their support in Sogod Bay, all the volunteers of the Large Marine Vertebrates Project for the data collection, Christoph Rohner (Marine Megafauna Foundation) for his advices and comments, Anna Flam (Marine Megafauna Foundation) for her help on the MantaMatcher database (http://www.mantamatcher.org), Tam Sawers and Guy Stevens (Manta Trust) for the support in the creation of the national identification catalogue, Shannon Arnold and Maita Verdote (Manta Trust Philippines), and Jo Marie Acebes (Balyena.org) for the support, advice, and shared information during the mobulid fishery monitoring project in Bohol. This work would not have been possible without the support of the Department of Agriculture-Bureau of Fisheries and Aquatic Resources of Region 7, the Department of Environment and Natural Resources, and the Local Government Units of Jagna (Bohol), Pintuyan and San Ricardo (Southern Leyte). This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Fishery and trade of whale sharks and manta rays in the Bohol Sea, Philippines
Elasmobranch biodiversity, conservation and management: proceedings of the international seminar and workshop, Sabah, Malaysia, July 1997, S.L. Fowler, T.M. Reed, F.A. Dipper, 2002, pp. 132–148Occasional paper of the IUCN Species Survival Commission no. 25
Population structure, residency patterns and movements of whale sharks in Southern Leyte, Philippines: results from dedicated photo-ID and citizen science
Aquatic Conservation: Marine and Freshwater Ecosystems, 2016, doi:10.1002/aqc.2636
Record of a pregnant Mobula thurstoni and occurrence of Manta birostris(Myliobatiformes: Mobulidae) in the vicinity of Saint Peter and Saint Paul Archipelago (Equatorial Atlantic). Scientific note
Pan-American Journal of Aquatic Sciences, Volume 7, 2012, pp. 21–26
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