Andrea D. Marshall

Biology, ecology and conservation of the Mobulidae

The Mobulidae are zooplanktivorous elasmobranchs comprising two recognized species of manta rays (Manta spp.) and nine recognized species of devil rays (Mobula spp.). They are found circumglobally in tropical, subtropical and temperate coastal waters. Although mobulids have been recorded for over 400 years, critical knowledge gaps still compromise the ability to assess the status of these species. On the basis of a review of 263 publications, a comparative synthesis of the biology and ecology of mobulids was conducted to examine their evolution, taxonomy, distribution, population trends, movements and aggregation, reproduction, growth and longevity, feeding, natural mortality and direct and indirect anthropogenic threats. There has been a marked increase in the number of published studies on mobulids since c. 1990, particularly for the genus Manta, although the genus Mobula remains poorly understood. Mobulid species have many common biological characteristics although their ecologies appear to be species-specific, and sometimes region-specific. Movement studies suggest that mobulids are highly mobile and have the potential to rapidly travel large distances. Fishing pressure is the major threat to many mobulid populations, with current levels of exploitation in target fisheries unlikely to be sustainable. Advances in the fields of population genetics, acoustic and satellite tracking, and stable-isotope and fatty-acid analyses will provide new insights into the biology and ecology of these species. Future research should focus on the uncertain taxonomy of mobulid species, the degree of overlap between their large-scale movement and human activities such as fisheries and pollution, and the need for management of inter-jurisdictional fisheries in developing nations to ensure their long-term sustainability. Closer collaboration among researchers worldwide is necessary to ensure standardized sampling and modelling methodologies to underpin global population estimates and status.

How large is the world's largest fish? Measuring whale sharks Rhincodon typus with laser photogrammetry

Laser photogrammetry was found to be a promising new cost-effective technique for measuring free-swimming whale sharks Rhincodon typus. Photogrammetric measurements were more precise than visual size estimates by experienced researchers, with results from the two methods differing by 9· 8 ± 1· 1% (mean ±s.e.). A new metric of total length and the length between the fifth gill and first dorsal fin (r² = 0· 93) is proposed to facilitate easy, accurate length measurements of whale sharks in the field.

Reproductive ecology of the reef manta ray Manta alfredi in southern Mozambique

The application of a photographic identification methodology using the unique ventral surface markings (natural spot patterns) of an observed population in southern Mozambique enabled many aspects of the reproductive ecology of reef manta rays Manta alfredi to be examined. The region encompassing the study site was identified as a mating ground for M. alfredi based on observations of mating events and fresh mating scars on females. The distribution of these pectoral fin scars was highly biased and indicated a strong lateralized behavioural trait, with 99% of these scars occurring only on the left pectoral fin. No other elasmobranch has been reported to display behavioural lateralization. The study region also acts as a birthing ground, with individuals typically giving birth in the austral summer period after a gestation of c. 1 year. Reproductive periodicity in M. alfredi was most commonly biennial, but a few individuals were pregnant in consecutive years, confirming an annual ovulatory cycle. The production of a single pup appears to be the normal situation, although observations in the wild as well as during opportunistic dissections of individuals killed by fisheries revealed that two pups are conceived on occasion. Many aspects of the study have contributed to the limited baseline data currently available for this species and have highlighted the potential need for more conservative conservation strategies.

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.

Habitat segregation and mosaic sympatry of the two species of manta ray in the Indian and Pacific Oceans, Manta alfredi and M. birostris

Habitat use of Manta alfredi and M. birostris was assessed at 20 localities in the Indian and Pacific Oceans based upon 3328 photographic observations. Geographical relationships of the two species were scored as either microallopatry, microparapatry or microsympatry at each locality. Our study revealed a mosaic habitat occupancy by the two species within their macrosympatric range.

The frequency and effect of shark-inflicted bite injuries to the reef manta ray Manta alfredi

Shark bite injuries on reef manta rays Manta alfredi off the coast of Inhambane, Mozambique, were examined over a three-year period (2003–2006). The frequency and seasonality of attacks, the rate of wound healing, and the possible identities of attackers were explored. This study presents the first examination of bite wounds on manta rays in the wild and the role sharks may play in the natural mortality of this species. The reported incidence of shark-inflicted injuries is high with over three-quarters of the sampled population affected. In total, 571 bite injuries were observed on 283 identified individuals. The number of bite injuries varied from one to seven, with a mean of 1.54 bite wounds. There was no significant difference in the frequency of bite injuries in male and female rays. The majority (96%) of the observed bite wounds were healed. Fresh wounds occurred throughout the year, with no obvious seasonality. The bull shark Carcharhinus leucas and tiger shark Galeocerdo cuvier are suggested as the primary mediators of attacks, although up to 11 other shark species are listed as potential attackers. The majority of the bite marks (96%) occurred to the most posterior region of the body, specifically the posterior edges of the pectoral and pelvic fins, with many injuries likely having a negative impact on the reproductive abilities and fitness of the rays.

Laser photogrammetry improves size and demographic estimates for whale sharks.

Whale sharks Rhincodon typus are globally threatened, but a lack of biological and demographic information hampers an accurate assessment of their vulnerability to further decline or capacity to recover. We used laser photogrammetry at two aggregation sites to obtain more accurate size estimates of free-swimming whale sharks compared to visual estimates, allowing improved estimates of biological parameters. Individual whale sharks ranged from 432–917 cm total length (TL) (mean ± SD = 673 ± 118.8 cm, N = 122) in southern Mozambique and from 420–990 cm TL (mean ± SD = 641 ± 133 cm, N = 46) in Tanzania. By combining measurements of stranded individuals with photogrammetry measurements of free-swimming sharks, we calculated length at 50% maturity for males in Mozambique at 916 cm TL. Repeat measurements of individual whale sharks measured over periods from 347–1,068 days yielded implausible growth rates, suggesting that the growth increment over this period was not large enough to be detected using laser photogrammetry, and that the method is best applied to estimating growth rates over longer (decadal) time periods. The sex ratio of both populations was biased towards males (74% in Mozambique, 89% in Tanzania), the majority of which were immature (98% in Mozambique, 94% in Tanzania). The population structure for these two aggregations was similar to most other documented whale shark aggregations around the world. Information on small (<400 cm) whale sharks, mature individuals, and females in this region is lacking, but necessary to inform conservation initiatives for this globally threatened species.

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.

Manta birostris, predator of the deep? Insight into the diet of the giant manta ray through stable isotope analysis

The characterization of diet for the giant manta ray Manta birostris has been problematic given their large-scale movement patterns and the difficulty in obtaining stomach contents from this species. The large majority of existing information is based on observational data limited to feeding events at the sea surface during daylight. Recently discovered aggregation sites for the giant manta ray off mainland Ecuador are some of the most accessible to date and provide a unique opportunity for researchers to gather much needed information on this elusive species. To assess how important surface zooplankton is to giant manta ray diet, we conducted stable isotope analysis (15N and 13C) on M. birostris muscle and surface zooplankton. Trophic position estimates placed M. birostris overall at a secondary consumer level of approximately 3.4 but there was large variation in δ15N and δ13C values among individuals. Manta birostris muscle tissue δ13C values were also not consistent with this species feeding predominantly on surface zooplankton and suggest that the majority of dietary intake is of mesopelagic origin. Given the conservative life history and fisheries pressure on large planktivores, knowledge of their trophic role and foraging strategies is essential to better understand their ecology and develop effective conservation measures.

Elasmobranchs of the Galapagos Marine Reserve

The Galapagos Marine Reserve is home to at least 50 species of sharks and rays. Although these species are protected in the marine reserve, they are vulnerable to industrial fishing outside the protected waters, to unintentional bycatch by local fishers inside the reserve, and to illegal fishing. Our knowledge of shark ecology in Galapagos has increased dramatically in the last decade, due to the creation of an interinstitutional research program, which focuses on the spatial ecology of hammerhead and whale sharks. Hammerheads are resident at restricted locations where they school during the day and disperse to sea most nights. Alternatively, mostly large, pregnant female whale sharks visit the northern islands from June through November for only a few days, as part of a large-scale migration.