Manta Alfredi Research Articles

The History and Characteristics of the Mobulid Ray Fishery in the Bohol Sea, Philippines.

The fishery for mobulid rays, also known as devil rays, has been practiced in the Bohol Sea for over a century yet very little is known about its history and characteristics. This study provides the first detailed description of the mobulid ray fishery in the Bohol Sea, Philippines. It describes the history and evolution of the fishery from the 19th century to 2013. It characterizes the fishery based on the species targeted, gears used, the organization, catch distribution, processing, monetary value, and the market of its by-products. This paper also analyses the changes that occurred through time, the management of the fishery and the drivers of the fishery. A multi-disciplinary approach was employed by combining ethno-historical research methods and catch landing monitoring in four primary sites within the Bohol Sea. This fishery began as an artisanal fishery using sail and row boats equipped with harpoons and gaff hooks practiced in at least four coastal villages in Bohol, Camiguin and Limasawa. The fishing fleet has decreased since the beginning of the 20th century however, with the motorization of the fishery and shift to the use of gillnets, the extent of the fishing grounds and market of the products have expanded. Four species of mobulid rays are caught in the Bohol Sea: Manta birostris, Mobula japanica, Mobula thurstoni and Mobula tarapacana. A fifth species, targeted by a fishing community off Dinagat as an off-shoot of the Bohol fishery is most likely the Manta alfredi. Currently, the fishery for mobulids is centered in Bohol Province where it has been practiced longest. The monetary value of mobulids in this region has increased and the dependence of fishing communities for their livelihood is significant. The unique characteristics of this fishery and the socio-cultural context within which it operates merits a thorough investigation in order to design the appropriate management strategy.

Effects of yearling, juvenile and adult survival on reef manta ray (Manta alfredi) demography

BackgroundThe trade in manta ray gill plates has considerably increased over the last two decades. The resulting increases in ray mortality, in addition to mortality caused by by-catch, has caused many ray populations to decrease in size. The aim of this study was to ascertain how yearling and juvenile growth and survival, and adult survival and reproduction affect reef manta ray (Manta alfredi) population change, to increase our understanding of manta ray demography and thereby improve conservation research and measures for these fish.MethodsWe developed a population projection model for reef manta rays, and used published life history data on yearling and juvenile growth and adult reproduction to parameterise the model. Because little is known about reef manta ray yearling and juvenile survival, we conducted our analyses using a range of plausible survival rate values for yearlings, juveniles and adults.ResultsThe model accurately captured observed variation in population growth rate, lifetime reproductive success and cohort generation time in different reef manta ray populations. Our demographic analyses revealed a range of population consequences in response to variation in demographic rates. For example, an increase in yearling or adult survival rates always elicited greater responses in population growth rate, lifetime reproductive success and cohort generation time than the same increase in juvenile survival rate. The population growth rate increased linearly, but lifetime reproductive success and cohort generation time increased at an accelerating rate with increasing yearling or adult survival rates. Hence, even a small increase in survival rate could increase lifetime reproductive success by one pup, and cohort generation time by several years. Elasticity analyses revealed that, depending on survival rate values of all life stages, the population growth rate is either most sensitive to changes in the rate with which juveniles survive but stay juveniles (i.e., do not mature into adults) or to changes in adult survival rate. However, when assessing these results against estimates on population growth and adult survival rates for populations off the coasts of Mozambique and Japan, we found that the population growth rate is predicted to be always most sensitive to changes in the adult survival rate.DiscussionIt is important to gain an in-depth understanding of reef manta ray life histories, particularly of yearling and adult survival rates, as these can influence reef manta ray population dynamics in a variety of ways. For declining populations in particular, it is crucial to know which life stage should be targeted for their conservation. For one such declining population off the coast of Mozambique, adult annual survival rate has the greatest effect on population growth, and by increasing adult survival by protecting adult aggregation sites, this population’s decline could be halted or even reversed.

A historical and contemporary consideration of the diet of the reef manta ray (Manta alfredi) from the Great Barrier Reef, Australia

The preserved stomach contents from the manta ray, collected in 1935, that provided the basis for the 2009 taxonomic resurrection of the species Manta alfredi, were examined. The majority of the material comprised calanoid copepods (61.7%) and trypanorhynch cestodes (34.6%), with minor contributions by arrow worms, a barnacle larva and a nematode. Comparison of the size-frequency distributions of stomach contents with that of zooplankton from the Great Barrier Reef region suggest that this manta ray preferentially ingested large copepods, or that the filter mechanism used to extract prey from the water was selective for prey items over 0.8mm in length. This is the first description of the diet of M. alfredi from stomach contents, and is consistent with previous inferences about what this species consumes.

First records of the reef manta ray Manta alfredi in the Bohol Sea, Philippines, and its implication for conservation

We report the occurrence of the reef manta ray Manta alfredi Krefft 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 of M. alfredi in 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 of M. alfredi in the country. We highlight the need to understand the distribution of M. alfredi in the region and make management recommendations based on the present study.

Prey Density Threshold and Tidal Influence on Reef Manta Ray Foraging at an Aggregation Site on the Great Barrier Reef.

Large tropical and sub-tropical marine animals must meet their energetic requirements in a largely oligotrophic environment. Many planktivorous elasmobranchs, whose thermal ecologies prevent foraging in nutrient-rich polar waters, aggregate seasonally at predictable locations throughout tropical oceans where they are observed feeding. Here we investigate the foraging and oceanographic environment around Lady Elliot Island, a known aggregation site for reef manta rays Manta alfredi in the southern Great Barrier Reef. The foraging behaviour of reef manta rays was analysed in relation to zooplankton populations and local oceanography, and compared to long-term sighting records of reef manta rays from the dive operator on the island. Reef manta rays fed at Lady Elliot Island when zooplankton biomass and abundance were significantly higher than other times. The critical prey density threshold that triggered feeding was 11.2 mg m-3 while zooplankton size had no significant effect on feeding. The community composition and size structure of the zooplankton was similar when reef manta rays were feeding or not, with only the density of zooplankton changing. Higher zooplankton biomass was observed prior to low tide, and long-term (~5 years) sighting data confirmed that more reef manta rays are also observed feeding during this tidal phase than other times. This is the first study to examine prey availability at an aggregation site for reef manta rays and it indicates that they feed in locations and at times of higher zooplankton biomass.

Manta ray tourism management, precautionary strategies for a growing industry: a case study from the Ningaloo Marine Park, Western Australia

Localised population declines and increased pressure from fisheries have prompted the promotion of manta ray interaction tourism as a non-consumptive, yet economically attractive, alternative to the unsustainable harvesting of these animals. Unfortunately, however, wildlife tourism activities have the potential to adversely impact focal species. In order to be sustainable, operations must be managed to mitigate negative impacts. A preliminary assessment of reef manta ray, Manta alfredi, behaviour identified short-term behavioural responses during a third of tourism interactions in the Ningaloo Marine Park, Western Australia. Although it remains unknown whether these responses translate to biologically significant impacts on the population as a whole, it is proposed that the precautionary principle be used to guide management intervention in the absence of conclusive evidence of the magnitude of tourism impacts. The principle supports the implementation of precautionary strategies to protect species and their environment from harm, even when the extent of the harm is yet to be confirmed. An increase in the level of industry management is recommended, including the implementation of a licensing system and adherence of all operators to a mandatory code of conduct during manta ray interactions. Considering the well designed and precautionary-driven management program of the Ningaloo whale shark tourism industry operating within the same marine park, a management program with the same underlying principles and objectives is deemed to be an ideal framework to build a comprehensive management plan for the manta ray interaction industry.

Movements of the reef manta ray (Manta alfredi) in the Red Sea using satellite and acoustic telemetry

Populations of mobulid rays are declining globally through a combination of directed fisheries and indirect anthropogenic threats. Understanding the movement ecology of these rays remains an important priority for devising appropriate conservation measures throughout the world’s oceans. We sought to determine manta movements across several temporal and spatial scales with a focus on quantifying site fidelity and seasonality in the northern Farasan Banks, Red Sea. We fitted manta rays with acoustic transmitters (n = 9) and pop-up satellite archival transmitting (PSAT) tags (n = 9), including four with GPS capability (Fastloc), during spring 2011 and 2012. We deployed an extensive array of acoustic receivers (n = 67) to record movements of tagged mantas in the study area. All acoustically tagged individuals traveled frequently among high-use receiver locations and reefs and demonstrated fidelity to specific sites within the array. Estimated and realized satellite tag data indicated regional movements <200 km from the tagging location, largely coastal residency, and high surface occupation. GPS-tagged individuals regularly moved within the coastal reef matrix up to ~70 km to the south but continued to return to the tagging area near the high-occupancy sites identified in the acoustic array. We also tested the accuracy of several geolocation models to determine the best approach to analyze our light-based satellite tag data. We documented significant errors in light-based movement estimates that should be considered when interpreting tracks derived from light-level geolocation, especially for animals with restricted movements through a homogenous temperature field. Despite some error in satellite tag positions, combining results from PSAT and acoustic tags in this study yielded a comprehensive representation of manta spatial ecology across several scales, and such approaches will, in the future, inform the design of appropriate management strategies for manta rays in the Red Sea and tropical regions worldwide.

Notes on the presence of Manta alfredi in the Tubbataha Reefs Natural Park, Cagayancillo, Palawan, Philippines

In 2011, a review of 33 photographs of mantas taken at the Tubbataha Reefs Natural Park (TRNP), Cagayancillo, Palawan, Philippines revealed that most of the mantas photographed were clearly reef manta rays (Manta alfredi) with only one photograph of Manta birostris. Previously identified in surveys within the park as oceanic manta ray M. birostris, the presence of M. alfredi has never been established until now. Using various parameters, the pictures in the Tubbataha Management Office (TMO) database were reviewed and noted. The identification of M. alfredi was more consistently based on the presence of black marks located posterolateral to the last gill slits and between the rows of gill slits. The identification of the species was further validated by experts after viewing three photographs from the said database. This represents a new elasmobranch species record for the TRNP and, technically, for the Philippines as well. Furthermore, the confirmed presence of both globally significant species of manta rays should have a strong bearing on the conservation policies of the park as well as that of the country. Further research on population dynamics, structure and abundance is recommended. Contributing to global efforts to generate better understanding of the species through partnership with international organizations is also recommended.

Fisheries management and conservation of sharks in Indonesia

Indonesian waters have a high diversity of sharks and rays, with at least 118 species belonging to 25 families found throughout the vast archipelago. Indonesia also has the highest shark landings globally and nearly all high‑value shark species are overexploited and could be considered threatened. This situation is of international concern, especially among conservationists and elasmobranch scientists. Most of the shark catch in Indonesian waters is taken as bycatch of fisheries deploying various types of gear, including longlines, driftnets, handlines and purse‑seines. However, sharks are also targeted in several regions of eastern and southern Indonesia, where they are often the main source of livelihood for many artisanal fishers. Shark fishing, whether targeted or bycatch, occurs throughout most of Indonesia's waters, and the large size of the EEZ, which encompasses nearly 6 million km2, is a primary constraint regarding the effective management of shark fisheries. In 2009, 11 fisheries management zones were established through the gazetting of a regulation on regional fisheries, facilitating management by the Ministry of Marine Affairs and Fisheries. Here, we discuss how the implementation of a number of regulations gazetted by the Indonesian government to ensure sustainable utilisation of fisheries resources should take into account shark resources. We also examine recent elasmobranch conservation efforts by the government, including the recent designation of whale sharks Rhincodon typus and manta rays Manta alfredi and M. birostris as fully protected species, and a prohibition on exports of products of hammerhead Sphyrna spp. and oceanic whitetip sharks Carcharhinus longimanus.

Unique Sequence of Events Triggers Manta Ray Feeding Frenzy in the Southern Great Barrier Reef, Australia

Manta rays are classified as Vulnerable to Extinction on the IUCN Red List for Threatened Species. In Australia, a key aggregation site for reef manta rays is Lady Elliot Island (LEI) on the Great Barrier Reef, ~7 km from the shelf edge. Here, we investigate the environmental processes that triggered the largest manta ray feeding aggregation yet observed in Australia, in early 2013. We use MODIS sea surface temperature (SST), chlorophyll-a concentration and photic depth data, together with in situ data, to show that anomalous river discharges led to high chlorophyll (anomalies: 10–15 mg∙m−3) and turbid (photic depth anomalies: −15 m) river plumes extending out to LEI, and that these became entrained offshore around the periphery of an active cyclonic eddy. Eddy dynamics led to cold bottom intrusions along the shelf edge (6 °C temperature decrease), and at LEI (5 °C temperature decrease). Strongest SST gradients (&gt;1 °C∙km−1) were at the convergent frontal zone between the shelf and eddy-influenced waters, directly overlying LEI. Here, the front intensified on the spring ebb tide to attract and shape the aggregation pattern of foraging manta rays. Future research could focus on mapping the probability and persistence of these ecologically significant frontal zones via remote sensing to aid the management and conservation of marine species.

Levels of arsenic, cadmium, lead and mercury in the branchial plate and muscle tissue of mobulid rays

Mobulid rays are targeted in fisheries for their branchial plates, for use in Chinese medicine. Branchial plate and muscle tissue from Mobula japanica were collected from fish markets in Sri Lanka, and muscle tissue biopsies from Manta alfredi in Australia. These were analysed for arsenic, cadmium, lead and mercury and compared to maximum levels (MLs) set by Food Standards Australia and New Zealand (FSANZ), European Commission (EC) and Codex Alimentarius Commission. The estimated intake for a vulnerable human age group was compared to minimal risk levels set by the Agency for Toxic Substances and Disease Registry. The mean inorganic arsenic concentration in M. japanica muscle was equivalent to the FSANZ ML while cadmium exceeded the EC ML. The mean concentration of lead in M. alfredi muscle tissue exceeded EC and Codex MLs. There were significant positive linear correlations between branchial plate and muscle tissue concentrations for arsenic, cadmium and lead.

Correction: Running the Gauntlet: Regional Movement Patterns of Manta alfredi through a Complex of Parks and Fisheries.

[This corrects the article DOI: 10.1371/journal.pone.0110071.].

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

Manta and devil rays are an iconic group of globally distributed pelagic filter feeders, yet their evolutionary history remains enigmatic. We employed next generation sequencing of mitogenomes for nine of the 11 recognized species and two outgroups; as well as additional Sanger sequencing of two mitochondrial and two nuclear genes in an extended taxon sampling set. Analysis of the mitogenome coding regions in a Maximum Likelihood and Bayesian framework provided a well-resolved phylogeny. The deepest divergences distinguished three clades with high support, one containing Manta birostris, Manta alfredi, Mobula tarapacana, Mobula japanica and Mobula mobular; one containing Mobula kuhlii, Mobula eregoodootenkee and Mobula thurstoni; and one containing Mobula munkiana, Mobula hypostoma and Mobula rochebrunei. Mobula remains paraphyletic with the inclusion of Manta, a result that is in agreement with previous studies based on molecular and morphological data. A fossil-calibrated Bayesian random local clock analysis suggests that mobulids diverged from Rhinoptera around 30 Mya. Subsequent divergences are characterized by long internodes followed by short bursts of speciation extending from an initial episode of divergence in the Early and Middle Miocene (19–17 Mya) to a second episode during the Pliocene and Pleistocene (3.6 Mya – recent). Estimates of divergence dates overlap significantly with periods of global warming, during which upwelling intensity – and related high primary productivity in upwelling regions – decreased markedly. These periods are hypothesized to have led to fragmentation and isolation of feeding regions leading to possible regional extinctions, as well as the promotion of allopatric speciation. The closely shared evolutionary history of mobulids in combination with ongoing threats from fisheries and climate change effects on upwelling and food supply, reinforces the case for greater protection of this charismatic family of pelagic filter feeders.

Running the gauntlet: regional movement patterns of Manta alfredi through a complex of parks and fisheries.

Manta rays (Genus Manta) are economically important for fisheries and tourism in Indonesia. These species have been listed by the International Union for the Conservation of Nature Red List as Vulnerable to extinction; therefore, human exploitation of manta rays must be regulated. A better understanding of the habitat use and movement patterns of manta rays in Indonesia is needed in order to employ effective conservation measures. To gain better insight into the movements of Manta alfredi we used ‘Manta Matcher’, an online database with an integrated automated matching algorithm, to compare photographs from 2,604 encounters of M. alfredi collected by recreational divers and dive operators throughout Indonesia over a nine-year period. This photographic comparison revealed that manta rays migrated between regional sanctuaries such as Nusa Penida, the Gili Islands, and the Komodo National Park (up to 450 km straight-line distance). The areas between these sanctuaries are heavily fished and trafficked by ships, and when manta rays travel through these regions they risk being fished and injured by ship strikes. These long-range manta ray movements suggest connectivity between M. alfredi populations in neighboring islands and raise concerns about the future management of regional populations. It is recommended that a national conservation strategy be developed to protect the remaining populations in the country.

Movements and habitat use of reef manta rays off eastern Australia: offshore excursions, deep diving and eddy affinity revealed by satellite telemetry

Manta rays (Manta spp.) are plankton-feeding elasmobranchs classified as vulnerable to extinction on the IUCN Red List for Threatened Species. Despite increasing public and scientific interest in manta rays, major knowledge gaps concerning their movement ecology and dispersal capabilities remain. Here, we used pop-off satellite-linked archival transmitting tags to examine the horizontal movements and habitat use patterns of reef manta rays (M. alfredi) departing Lady Elliot Island in the southern Great Barrier Reef, Australia. Tagged individuals moved across a latitudinal range of 1035 km, travelling up to 2441 km in 118 d, diving down to 294.5 m and venturing up to 155 km off the continental shelf. Using random walk simulations, we showed that manta rays spent significantly more time in an offshore region characterised by the mesoscale cyclonic Capricorn Eddy than would be expected by chance. A behaviour-switching state-space model suggested this area to be an important foraging ground for M. alfredi off eastern Australia. We document the movements of 1 individual using offshore waters between 2 known aggregation regions off eastern Australia. Reef manta rays thus not only occupy inshore continental shelf and shelf-edge waters but also use offshore environments to exploit productive hotspots and travel long distances. Our findings highlight the need to better understand their movement ecology for effective management.

Reliance of mobile species on sensitive habitats: a case study of manta rays (Manta alfredi) and lagoons

Quantifying the ecological importance of individual habitats to highly mobile animals is challenging because patterns of habitat reliance for these taxa are complex and difficult to observe. We investigated the importance of lagoons to the manta ray, Manta alfredi, a wide-ranging and vulnerable species in a less-disturbed atoll ecosystem. Lagoons are highly sensitive to anthropogenic disturbance and are known to be ecologically important to a wide variety of mobile species. We used a novel combination of research tools to examine the reliance of M. alfredi on lagoon habitats. Stable isotope analysis was used to assay the recent energetic importance of lagoons to M. alfredi; high-resolution tracking data provided information about how M. alfredi utilised lagoonal habitats over long and short time periods; acoustic cameras logged patterns of animal entrances and departures from lagoons; and photo identification/laser photogrammetry provided some insight into why they may be using this habitat. M. alfredi showed strong evidence of energetic dependence on lagoon resources during the course of the study and spent long periods of residence within lagoons or frequently transited into them from elsewhere. While within lagoons, they demonstrated affinities for particular structural features within this habitat and showed evidence of temporal patterning in habitat utilization. This work sheds light on how and why M. alfredi uses lagoons and raises questions about how this use may be altered in disturbed settings. More generally, these observations contribute to our knowledge of how to assess the ecological importance of particular habitats situated within the broader home range of mobile consumers.

Population dynamics of the reef manta ray Manta alfredi in eastern Australia

The reef manta ray Manta alfredi aggregates at several sites along the east coast of Australia. Photographic identification and mark–recapture methods were used to report on the site affinity, size and structure of this population of M. alfredi. A total of 716 individuals were identified in 1982–2012, including 636 at Lady Elliot Island (LEI), southern Great Barrier Reef. Over 60 % of individuals identified were resighted at least once during the study period. Multiple resightings within and among years imply a high degree of site affinity by individuals to aggregation sites. One individual was sighted 11 times at LEI over a 30-yr period. The sex ratio of this population was significantly biased towards females (1.2:1 female-to-male ratio), and females were more commonly resighted than males. Robust design population models were used to estimate the population size of the winter aggregation at LEI over a 4-yr period. The models estimated up to 456 (95 % CI 399–535) M. alfredi individuals in the population within one winter season and a high annual apparent survival. This study demonstrated that waters around LEI form a key aggregation site for a large portion of the M. alfredi population in east Australian waters.

Diving Behavior of the Reef Manta Ray Links Coral Reefs with Adjacent Deep Pelagic Habitats

Recent successful efforts to increase protection for manta rays has highlighted the lack of basic ecological information, including vertical and horizontal movement patterns, available for these species. We deployed pop-up satellite archival transmitting tags on nine reef manta rays, Manta alfredi, to determine diving behaviors and vertical habitat use. Transmitted and archived data were obtained from seven tagged mantas over deployment periods of 102–188 days, including three recovered tags containing 2.6 million depth, temperature, and light level data points collected every 10 or 15 seconds. Mantas frequented the upper 10 m during daylight hours and tended to occupy deeper water throughout the night. Six of the seven individuals performed a cumulative 76 deep dives (>150 m) with one individual reaching 432 m, extending the known depth range of this coastal, reef-oriented species and confirming its role as an ecological link between epipelagic and mesopelagic habitats. Mean vertical velocities calculated from high-resolution dive data (62 dives >150 m) from three individuals suggested that mantas may use gliding behavior during travel and that this behavior may prove more efficient than continuous horizontal swimming. The behaviors in this study indicate manta rays provide a previously unknown link between the epi- and mesopelagic layers of an extremely oligotrophic marine environment and provide evidence of a third marine species that utilizes gliding to maximize movement efficiency.

Stable Isotope and Signature Fatty Acid Analyses Suggest Reef Manta Rays Feed on Demersal Zooplankton

Assessing the trophic role and interaction of an animal is key to understanding its general ecology and dynamics. Conventional techniques used to elucidate diet, such as stomach content analysis, are not suitable for large threatened marine species. Non-lethal sampling combined with biochemical methods provides a practical alternative for investigating the feeding ecology of these species. Stable isotope and signature fatty acid analyses of muscle tissue were used for the first time to examine assimilated diet of the reef manta ray Manta alfredi, and were compared with different zooplankton functional groups (i.e. near-surface zooplankton collected during manta ray feeding events and non-feeding periods, epipelagic zooplankton, demersal zooplankton and several different zooplankton taxa). Stable isotope δ15N values confirmed that the reef manta ray is a secondary consumer. This species had relatively high levels of docosahexaenoic acid (DHA) indicating a flagellate-based food source in the diet, which likely reflects feeding on DHA-rich near-surface and epipelagic zooplankton. However, high levels of ω6 polyunsaturated fatty acids and slightly enriched δ13C values in reef manta ray tissue suggest that they do not feed solely on pelagic zooplankton, but rather obtain part of their diet from another origin. The closest match was with demersal zooplankton, suggesting it is an important component of the reef manta ray diet. The ability to feed on demersal zooplankton is likely linked to the horizontal and vertical movement patterns of this giant planktivore. These new insights into the habitat use and feeding ecology of the reef manta ray will assist in the effective evaluation of its conservation needs.

A Report of Symbiotic Siphonostomatoida (Copepoda) Infecting Mobulids (Rajiformes: Mobulidae) Off the KwaZulu-Natal Coast, South Africa

Though South Africa is rich in aquatic species, little is known about the diversity and distribution of copepods that parasitize different hosts ranging from invertebrates to marine mammals. A total of 43 mobulids (34 Mobula kuhlii; two Mobula eregoodootenkee and seven Manta alfredi) were examined for infection by symbiotic copepods at the KwaZulu-Natal Sharks Board (KZNSB). Collected copepod specimens were fixed and preserved in 70% ethanol and studied with the stereo- and light microscopes. Most of the examined hosts (38) were infected with symbiotic siphonostomatoids. Ten different species representing five families were identified. Of these, seven represent new host records while four are new geographical records. The highest prevalences (>60%) were calculated for Eudactylina oliveri and Pupulina cliffi on M. eregoodootenkee and M. kuhlii while E. oliveri also exhibited the highest mean intensity values on these hosts.