Crowdsourced data reveal multinational connectivity, population demographics, and possible nursery ground
of endangered oceanic manta rays in the Red Sea
Item Type Article
Authors Knochel, Anna;Cochran, Jesse;Kattan, Alexander;Stevens, Guy M.
W.;Bojanowksi, Elke;Berumen, Michael L.
Citation Knochel, A. M., Cochran, J. E. M., Kattan, A., Stevens, G. M. W., Bojanowksi, E., & Berumen, M. L. (2022). Crowdsourced data reveal multinational connectivity, population demographics, and possible nursery ground of endangered oceanic manta rays in the Red Sea. Aquatic Conservation: Marine and Freshwater Ecosystems. Portico. https://doi.org/10.1002/aqc.3883
Eprint version Publisher's Version/PDF
DOI 10.1002/aqc.3883
Publisher Wiley
Journal Aquatic Conservation: Marine and Freshwater Ecosystems Rights Archived with thanks to Aquatic Conservation: Marine and
Freshwater Ecosystems under a Creative Commons license, details at: http://creativecommons.org/licenses/by-nc-nd/4.0/
Download date 2023-10-31 05:08:03
Item License http://creativecommons.org/licenses/by-nc-nd/4.0/
Link to Item http://hdl.handle.net/10754/681586
R E S E A R C H A R T I C L E
Crowdsourced data reveal multinational connectivity, population demographics, and possible nursery ground of endangered oceanic manta rays in the Red Sea
Anna M. Knochel
1| Jesse E. M. Cochran
1| Alexander Kattan
1| Guy M. W. Stevens
2| Elke Bojanowksi
3| Michael L. Berumen
11Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Saudi Arabia
2The Manta Trust, Catemwood House, Norwood Lane, Corscombe, Dorset, UK
3Red Sea Sharks, UK
Correspondence
Anna M. Knochel, Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia.
Email:[email protected]
Funding information
King Abdullah University of Science and Technology, Grant/Award Number: MLB
Abstract
1. Despite the large size and economic value of the species, populations of oceanic manta ray (Mobula birostris) are often poorly studied and almost completely undescribed in the Red Sea. Here, photo-identification (photo-ID) was used to provide the first description of
M. birostrismovement patterns and population demographics for the northern Red Sea.
2. Images collated from social media, researchers, and photo-ID databases from 2004 to 2021 identified 267 individual
M. birostrisfrom 395 sightings in Egypt, Israel, Jordan, Saudi Arabia, and Sudan. Sexual parity was observed in the population with 134 females, 111 males, and 22 individuals of undetermined sex.
Nearly half of the individuals in this study were first identified through social media searches, highlighting the value of the sightings data collected by the public.
3. The regular presence of juveniles in Sharm el-Sheikh, Egypt, indicates that this area is a potential nursery, which is the second identified for this species globally and the first in the Indo-Pacific. Encounter data from this study recorded the first known movements of juvenile
M. birostrisand demonstrate that they can travel long distances of at least 525 km.
4. Within the recorded population, 24.7% (n
=67) of individuals were resighted, including 21 oceanic manta rays that were encountered in more than one location. These records reveal long-distance migrations of up to 700 km and confirm the international connectivity of
M. birostrisin the Red Sea. The lagged identification rate data are best fitted with an open-population model, implying that the northern Red Sea is represented by one well-mixed population.
5. The baseline data presented here should encourage the expansion of directed research and citizen science initiatives for
M. birostris. Increased knowledge ofmovement patterns and site use will be crucial to successfully protecting this
This is an open access article under the terms of theCreative Commons Attribution-NonCommercial-NoDerivsLicense, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2022 The Authors.Aquatic Conservation: Marine and Freshwater Ecosystemspublished by John Wiley & Sons Ltd.
Aquatic Conserv: Mar Freshw Ecosyst.2022;1–13. wileyonlinelibrary.com/journal/aqc 1
endangered species in a region characterized by high levels of shipping traffic, unregulated fisheries, and extensive coastal development.
K E Y W O R D S
coastal, distribution, Egypt, endangered species, fish, marine megafauna, ocean, photo-ID
1 | I N T R O D U C T I O N
Citizen science and scientific ecotourism have emerged as mainstream, cost-effective strategies for collecting information on wildlife at a range of spatial and temporal scales (Silvertown,2009).
Although these methods have most frequently targeted easily accessible terrestrial or freshwater ecosystems (Theobald et al.,2015), the growth of snorkel and dive tourism has seen the practice increasingly applied in the marine environment (Spalding et al.,2017).
Crowdsourced data are particularly useful with respect to rare, remote, and wide-ranging megafauna species, such as sharks and rays (Ward-Paige & Lotze,2011; Chin & Pecl,2018; Giovos et al.,2019).
Scientific ecotourism programmes led by researchers and environmental organizations have greatly contributed to our understanding of the abundance, distribution, and demography of a growing number of threatened or endangered elasmobranchs, including the whale shark (Rhincodon typus) (Norman et al.,2017), reef manta ray (Mobula alfredi) (Germanov & Marshall,2014), smalltooth sawfish (Pristis pectinata) (Norton et al., 2012), and porcupine ray (Urogymnus asperrimus) (Chin, 2014). However, crowdsourced data can also be derived in a more opportunistic and resourceful way, namely via social media platforms that researchers can systematically scan to identify and connect with owners of relevant content. Social media search results have augmented the datasets for sightings of R. typus andM. alfredi (Kashiwagi et al.,2011; Davies et al.,2012;
Araujo et al., 2017; McCoy et al.,2018; Garzon et al.,2020), have helped to expand the known range of the ornate eagle ray (Aetomylaeus vespertilio) (Araujo et al.,2020), and have been used to identify potential seasonality in coastal pupping of the blue shark (Prionace glauca) in Italy (Boldrocchi & Storai,2021).
The oceanic manta ray (Mobula birostris) is a large marine planktivore with a circumtropical distribution that is poorly studied.
Mobula birostris is an ideal species to data-mine on social media because dedicated research efforts are time consuming and expensive, yet it is regularly sought out by dive tourists (O'Malley, Lee-Brooks & Medd,2013). Furthermore, individuals can be identified by their ventral spot patterns, which are unique to each individual and are stable through time (Marshall & Pierce, 2012). Although recent research has uncovered information about the diet (Burgess et al.,2016), population structure (Stewart et al.,2016a; Hosegood et al., 2020), and vertical distribution of M. birostris (Andrzejaczek et al.,2021), much remains unknown about their horizontal movement patterns, reproductive ecology, and life history.Mobula birostriswere previously hypothesized to undertake large-scale ocean migrations (Marshall, 2008), but recent research suggests M. birostris maintain
relatively limited regional home ranges and their movements are influenced by oceanographic processes tied to primary production, reproductive opportunities, and the avoidance of predators (Burgess et al.,2016; Stewart et al.,2016a; Beale et al.,2019). The resulting isolation of these populations may prevent stock replenishment from outside sources and leave M. birostris vulnerable to regional extirpations. Information on local-scale population dynamics and anthropogenic threats is therefore critical to the local and global-scale conservation of this species.
Like other elasmobranchs,M. birostrisfollows a conservative life history of low fecundity, long lifespan, and the delayed onset of maturity. Indeed,M. birostriswas recently updated to Endangered on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (Marshall et al., 2020), reflecting continuing population declines from targeted fisheries and accidental by-catch in gillnet and tuna purse seine net fisheries (Duffy et al.,2019). Juvenile survival and age at maturity are important biological parameters for measuring and estimating population growth (Yokoi et al.,2017). Yet, knowledge of early life stage habitat use, growth rates, and movement ecology, critical components for conservation mapping, is particularly lacking for all mobulids (manta and devil rays) (Stewart et al., 2018a). Therefore, identifying critical habitats of juvenile M. birostris remains a priority to inform effective conservation measures, obtain accurate life history data, and ensure population viability.
In the Red Sea, bothM. birostrisandM. alfredioccur (Kashiwagi et al., 2011; Stevens et al., 2018). Mobula alfredi were first documented in the region by Austrian explorer Hans Hass in his 1951 documentary film Adventures in the Red Sea(Hass,1951), but over 60 years passed before the first scientific work for either manta ray species was produced (Braun, 2013). Subsequent research has shed light on the movement (Braun et al.,2014; Braun et al.,2015;
Kessel et al., 2017) and feeding behaviour of M. alfredi (Gadig &
Neto,2014) in Saudi Arabia and Sudan, as well as providing the first evidence of possible hybridization betweenM. birostrisandM. alfredi (Walter et al., 2014). However, little else exists in the literature regarding the more pelagic-associatedM. birostrisin the Red Sea. The lack of data can be attributed to the preference that M. birostris demonstrates for less accessible oceanic habitats, the limited research infrastructure in some Red Sea countries, and the restrictive permitting systems and political instability in others (Berumen et al.,2013). Many of these barriers can be overcome by collecting data from the public. Most Red Sea countries have some level of ecotourism infrastructure and do not require permits to photograph animals.
Photo-identification (photo-ID) data were obtained from social media platforms, non-governmental organizations (NGOs), and academic researchers to describe the demographics and regional movement patterns of M. birostris within the Red Sea. These encounter records are used to fit maximum-likelihood population models, providing estimates of relative abundance, residency, and mortality. This study aims to provide baseline information for future research and management efforts on Red Sea M. birostris while highlighting the value of citizen science and social media platforms as data sources for understudied species.
2 | M E T H O D S 2.1 | Study area
A narrow semi-enclosed basin of 200–250 km in width and 2,000 km in length, the Red Sea is connected to the Gulf of Aden and the greater Western Indian Ocean through a narrow (26 km) and shallow (200 m in depth) sill known as the Bab el-Mandeb (Figure 1).
Considered a‘desert sea’, the Red Sea is the most oligotrophic ocean basin in the world and reaches a maximum depth of 2,867 m. The monsoon regulates the productivity of the region by facilitating the convection of deeper nutrient-rich water from the Gulf of Aden into the southern Red Sea (Raitsos et al., 2015). High levels of productivity, measured by proxy through remotely sensed concentrations of chlorophylla, occur along coastal sites in the spring and summer (Racault et al.,2015).
Several sites were identified as areas whereM. birostrisare most likely to be sighted by scuba divers. Sharm el-Sheikh is a popular tourist destination located along the coastline of the southern Sinai Peninsula, Egypt. This area includes a large expanse of reefs that extend 50 km along the coastline as well as Ras Mohammed National
Park, creating one of the top diving destinations in the entire Red Sea.
The area is characterized by a steep drop to 1,100–1,400 m depth less than 10 km from shore. Al Ikhwan (The Brothers) and Daedalus Reef are two seamounts located towards the centre of the northern Red Sea basin and are small, isolated, shallow reefs immediately surrounded by depths of 800 m. The other three high-encounter areas, Elphinstone Reef and St. John’s Reefs, Egypt, and Sabaa Akhwat, Saudi Arabia, are located along the shelf edge and are popular diving destinations.
2.2 | Data collection
Images of the ventral surface of Red Sea M. birostris were compiled from existing photo-ID databases belonging to the Manta Trust, Manta Matcher (Marshall & Holmberg, 2021), and independent researchers. Images were collected from local dive operations and extracted from social media sites such as YouTube, Facebook, Instagram, Flickr, and Vimeo by systematically using relevant keywords to search for the species (e.g. ‘manta’ and
‘manta ray’) and locations (e.g. ‘Red Sea’, ‘Egypt’, ‘Sharm el- Sheikh’, and‘Daedalus’). As a result of the opportunistic nature of the dataset, the availability and quality of the metadata varied among photos, so the best available time and location data were used in each case. Owners of socially sourced images were contacted to request missing information when it was not stated in the post. Most photos and videos were associated with exact encounter dates, or at least with a month and year. In cases where no timing information could be obtained, the day that the image was posted online was used as a proxy date to calculate a minimum time period between resightings. When exact coordinates were not available for an encounter, the listed reef or dive sites mentioned in the posts were used as a proxy (Data S1). All photos
F I G U R E 1 Left: map of greater Red Sea in relation to the Western Indian Ocean. Right: Northern Red Sea with boxed reefs/regions where oceanic manta rays (Mobula birostris) are typically encountered
were sorted by country of origin and assigned to specific high- occurrence regions (definedpost hoc), when possible.
2.3 | Photo analysis
The ranges of M. birostris and M. alfredi overlap in the Red Sea (Kashiwagi et al.,2011), so photographed animals were identified to species level using established morphometric characteristics (Marshall, 2008) and imagery of M. alfredi was removed.
Demographics such as sex, maturity, and colour morph were assessed for each sighting ofM. birostriswhere a photo-ID could be obtained.
Sex was determined by the presence (males) or absence (females) of claspers between the pelvic fins. For males, clasper morphology was used to define three life stages: juvenile (uncalcified claspers that did not extend to the pelvic margin); subadult (uncalcified claspers that were flush with or extended slightly past the pelvic margin); and mature (calcified claspers extended well past the pelvic margin) (Marshall,2008). Assessing the maturity status of female manta rays is more difficult than male manta rays because non-pregnant adult females can lack external indicators of maturation (Beale et al.,2019), such as the wingtip scarring that occurs during mating. For this reason, the percentage of adult female manta rays in studied populations is likely to be underestimated. To obtain a more insightful assessment of female M. birostris demographics for this study, life stages were classified based on size estimation: juvenile (wingspan less than 4 m), adult (wingspan greater than 4 m), and unknown.
Direct measurements were not possible, so female maturation status was estimated from the photos and videos where associated fish species, such as remoras, or humans were present within the frame and could be used as a size reference (Bucair et al.,2021). Where these associations were not present, the status of the female was left as unknown. However, females showing clear signs of pregnancy (highly distended abdominal region) or mating scars were classified as adults. Lastly, individuals were grouped into one of three colour- morph classifications: melanistic (black dorsal surface with mostly black ventral surface); leucistic (white patchy ventral shading), or chevron (distinct V-shaped shading on ventral surface of the pectoral wings).
The ventral coloration of M. birostris, typically white with scattered black spots posterior to the gill slits, was used as a marker for individual photo-ID (Marshall & Pierce,2012). The size, shape, and relative position of the ventral spots were used to manually look for matches between individuals. This matching process created a library of identifiedM. birostriswith a history of sightings and resightings.
2.4 | Encounter pattern analysis
Encounter coordinates were grouped together if they occurred within 40 km and mapped, whereas bar plots were created to show the monthly distributions of sightings in addition to the numbers of captures and recaptures that occurred from 2004 to 2021. A binomial
test was used to analyse both overall and site-specific sex ratios. The number of resightings was evaluated between juvenile and adult manta rays and between males and females with a Mann–WhitneyU- test to determine whether life stage or sex impacted the resighting rate. To visualize sighting patterns of juveniles and adultM. birostris, the coordinate data of the encounters were analysed with 2D kernel density estimation and latitudinal density curves in R 3.6.3 (R Development Core Team, 2020). Movement patterns were assessed for resighted individuals by calculating and mapping the shortest-over-water distance between successive encounters. In addition to these spatial analyses, photographic captures and recaptures with known encounter dates were used to calculate a lagged identification rate (LIR), providing the probability curve of resighting a known individual over time. Encounter dates that only contained the month and year of the sighting were included in this modelling and were given an estimated date of encounter from the middle of the month (the 15th). Once calculated, a series of maximum- likelihood population models with varying degrees of assumed population closure were fitted to the LIR data. The most parsimonious model was selected based on the lowest Akaike information criterion (AIC) and bootstrapped 100 times to produce 95% confidence intervals for parameter estimates. Both the LIR calculation and population modelling were performed for the Red Sea dataset and for regional subsets of the data containing enough encounters, such as Daedalus Reef and Sharm el-Sheikh.
3 | R E S U L T S
3.1 | Data characteristics
After removing images ofM. alfredi, the remaining dataset consisted of 395 encounters ofM. birostriswith 267 unique individuals. These data included encounters from Egypt (n=358), Saudi Arabia (n=20), Israel (n = 5), Sudan (n = 4), Jordan (n= 1), and seven unknown locations (Figure 2a). Most encounters (n = 351) could be further subcategorized into specific regions, which included Sharm el-Sheikh (n = 147), Elphinstone Reef (n = 23), Daedalus Reef (n = 115), St. John’s Reefs (n = 27), Sabaa Akhwat (n = 14), and Al Ikhwan (n = 27) (Figure 2a). The exact date was known for 79% of the encounters (n = 313). Another 7.1% were associated with specific month–year combinations (n=28) and 1.8% were reported with only the year of the encounter (n=7). The remaining 11.9% (n=47) of encounters lacked any information for when the individual was sighted and the day before the posting date was used as a proxy for calculating possible resighting intervals. The highest number of encounters occurred during the spring and summer months, peaking in May (Figure 2b). Most encounters were of newly identified individuals, although recaptures occurred every year from 2009 to 2021, except 2020 (Figure2c).
The largest proportion of photo-IDs was obtained through social media content, accounting for 46.8% of all contributed IDs (n=125;
Table 1). Researcher observations accounted for another 27.3%
(n=73), whereas NGO-owned databases contributed the final 25.8%
of the identified individuals in the database (n=69). Both the Manta Matcher and Manta Trust databases rely heavily on public submissions (citizen science), so collectively between these platforms and social media content, citizen scientists contributed up to 72.7%
(n=194) of the total photo-IDs (Table1).
3.2 | Population demographics
From all encounters, 267 individuals were identified: 134 females, 111 males, and 22 individuals of unknown sex. This resulted in a ratio of female-to-male sightings of 1.2:1. The slight female bias was not statistically significant for the Red Sea overall (P = 0.16, female proportion=0.547, 95% CI 0.48–0.61), or for most regions in isolation (P> 0.05 for Sharm el-Sheikh, Al Ikhwan, and Daedalus Reef; Table2).
There were two exceptions: Elphinstone Reef, where females were significantly dominant (P=0.0072, female proportion=0.82, 95% CI 0.60–0.95) and St. John’s Reefs, where males were significantly dominant (P=0.019, female proportion=0.21, 95% CI=0.06–0.46;
Table2). Colour morphology was clearly visible for all 267M. birostris, with chevron being the dominant morphotype throughout the Red Sea (261 individuals, 97.8%), whereas melanism was rare (six individuals, 2.2%) and leucism was entirely absent from the dataset.
Life stage was determined for 110 males and 73 females (99%
and 54% of their respective samples). Of these, 58 males and 39 females were classified as juveniles (53% and 53%, respectively;
n = 97 total juveniles), whereas 31 males and 34 females were classified as adults (28% and 47%, respectively;n=65 total adults).
An additional 23 males (20.1%) were classified as subadults. Some regions (Daedalus Reef and St. John’s Reefs) showed roughly the same patterns as the Red Sea overall, with the number of adult individuals (in combination with subadults in males) being roughly equal to the number of juveniles. Sharm el-Sheikh, however, was F I G U R E 2 Summary ofMobula birostrissightings in the Red Sea with: (a) spatial map of encounters; (b) seasonality of sightings; and (c) the number ofM. birostrissighted every year that were either newly captured or recaptured individuals
T A B L E 1 List of the data sources in which each individualMobula birostriswas first identified, including the Manta Trust and Manta Matcher, researcher observations, and sightings extracted from social media sites. Some photo-IDs were acquired through direct contact via social media and are considered to have been sourced from these platforms
Source Individuals
Percentage of total
Manta Matcher 47 17.6%
Researcher 73 27.3%
Manta Trust 22 8.2%
Social Media 125 46.8%
YouTube 86 32.2%
Facebook/Vimeo/Instagram/
Flickr
25 9.4%
Social media contacts 14 5.2%
Total 267
dominated by juvenileM. birostris(58 juveniles, four subadults, and nine adults), which made up 82% of the sighted individuals. Of the males sighted in Sharm el-Sheikh, 27 were deemed to be juveniles out of the 37 males observed in the area (73% male juvenile proportion;
Table 2). Of the 31 females where a size estimate was confidently obtained, 29 were deemed to be juveniles and two were estimated to be adults (94% female juvenile proportion). In contrast, Al Ikhwan was dominated solely by adult males (n = 9) and females (n = 11) (Table 2). Large adult females accounted for 64% of all sighted M. birostris individuals at Elphinstone Reef (n = 14), including four visibly pregnant females. Only a few adult males (n = 2), subadult males (n=1), and juvenile males (n=1) were encountered here. Overall, kernel and latitudinal distributions indicate both spatial segregation and overlap in juvenile and adult encounters (Figure3).
Ontogenetic shifts were observed in three individuals. The first was a male originally identified as a juvenile in 2017 before being
resighted in 2021 as a subadult (RS0087B). The second was a juvenile male first identified some time before August 2009, sighted a second time in the juvenile stage in 2013 at St. John’s Reefs, Egypt, and sighted most recently in Eilat, Israel, in 2021 with extended claspers (adult stage, RS0067B). The third was an adult female first identified in 2009, observed pregnant in 2015, and encountered again in 2016 being no longer pregnant (RS0075B).
Three maleM. birostriswere observed 4 years apart with clasper development that had not resulted in a change of juvenile maturity status. The first male (RS0067B) was observed in Sharm el-Sheikh in 2009 and 2011 before being resighted at St. John’s Reefs in 2013 with still undeveloped claspers. The second was RS0019B, sighted in Sharm el-Sheikh in 2009, 2011, 2012, and 2013 as a juvenile. The third was RS0266B, first sighted in 2017 in Sharm el-Sheikh with very small claspers (Figure S1). It was next sighted at Daedalus Reef in 2021 and its claspers had slightly extended but the animal was still considered a juvenile (Figure S1).
T A B L E 2 Population demographics at six sites with more than 10 identified individuals. Note that the table double-counts nine individuals because they were observed at least once in two locations. The only male without an assigned maturity status was sighted in Daedalus Reef, which is why only 37 of 38 males were assessed there
Females (size) Males (claspers)
Region Total F M U Sex Ratio Juvenile Adult Unknown Juvenile Sub-adult Adult
Sharm el-Sheikh 89 45 37 7 1.22F:1M 29 2 14 27 4 6
Al Ikhwan 26 16 9 1 1.78F:1M 0 11 5 0 0 9
Elphinstone Reef 22 18 4 0 4.25F:1M 0 14 4 1 1 2
Daedalus Reef 79 35 38 6 0.92F:1M 6 7 22 14 15 8
St. John’s Reefs 20 5 14 1 0.36F:1M 0 2 3 6 4 4
Sabaa Akhwat 13 5 7 1 0.71F:1M 3 0 2 4 2 1
Abbreviations: F, females; M, males; U, undetermined Sex.
F I G U R E 3 Spatial segregation and overlap of adult and juvenileMobula birostrisencounters from 2004 to 2021, depicted using 2D kernel utilization distributions (left) and latitudinal density distribution (right)
3.3 | Residency and regional connectivity
Of the 267 identifiedM. birostris, 67 (24.7%) were resighted. Most of these were only ever encountered in the region or site from which they were first identified, accounting for 135 total resightings of 46 individuals. Time intervals between these same-site encounters ranged from 1–2,194 days, indicating possible short-term residence in some M. birostris and interannual site fidelity in others. Twenty-one individuals were recorded making 23 movements between regions (Figure 4; Table S1). Straight-line distances over water between encounters ranged from 60 to 700 km, with time intervals ranging from 23 to > 4,426 days (12 years and 1 month). A juvenile male individual (RS0067B) moved 525 km between Sharm el-Sheikh and St. John’s Reefs, Egypt, after a minimum sighting interval of at least 1,377 days.
This individual was sighted again on 24 September 2021 in Eilat, Israel, as a mature male and had moved a minimum straight-line distance of 700 km. Several juveniles (n=7) moved straight-line distances of 60– 350 km. In total, four M. birostris individuals crossed national boundaries, establishing connectivity between Egyptian waters and those of several other Red Sea nations (Saudi Arabia, Jordan, and Israel).
There was no significant difference between the resighting rates of male (1.67 encounters per individual) and female (1.36 encounters per individual)M. birostris(Mann–WhitneyU-test,P=0.13), although
juveniles (1.76 encounters per individual) were significantly more likely to be resighted than adults (1.25 encounters per individual) (Mann–Whitney U-test, P = 0.005). This apparent demographic difference was largely driven by a single juvenile at Daedalus Reef that was sighted 12 times and by data from Sharm el-Sheikh where 58 juveniles produced 105 encounter records (1.81 encounters per individual). This included 14 individuals that were frequently resighted (between two and five times) over relatively short periods (from weeks to months) and 14 individuals that returned to the area over multiple years (Figure5).
The overall encounter record produced a linear discovery curve (Figure S2), meaning that new individuals continued to be regularly encountered throughout the study. This suggests an open population, which was corroborated by the LIR modelling. Of the eight tested models, the most parsimonious was an open population that accounted for migration and mortality (Table 3). The selected model fitted the data well (χ2=25.6.,P=0.22) and estimated an average abundance of 13.47 (95% CI 9.7–21.7)M. birostriswithin the survey zone (meaning any site whereM. birostriswere encountered in the Red Sea) on any given survey day. The model also predicted mean residence times of 48.3 days (95% CI 10.2–73.4 days) within the survey zone and 593.4 days (95% CI 66.5–1,765.0 days) outside it along with a mortality rate of 0.0010 (0.0005–0.0017) individuals per day.
F I G U R E 4 Map of movements for 21Mobula birostrisindividuals based on photo-ID data. Note that the edges represent connections between regions and do not represent the true movement paths of the individuals
Only Sharm el-Sheikh and Daedalus Reef produced enough encounters to calculate and model independent regional LIRs. Sharm el-Sheikh largely followed the same patterns exhibited by the Red Sea as a whole, resulting in a similar open-population model (Table 3). The selected model estimated an average abundance of 7.7 (95% CI 4.9–14.7) individuals per survey day, residence within the survey zone of 35.3 days (95% CI 6.6–82.3 days), residence outside the survey zone of 113.7 days (17.4–272.3 days), and a mortality of 0.0015 (0.0011–0.0024) individuals per day. Long-term site fidelity was less prevalent at Daedalus Reef, allowing for a simpler model focused on relatively short-term residence (Table 3).
This model did not include residence outside the survey area or mortality, but did estimate an average abundance of 6.0 (95% CI 3.9–21.2) and a mean residence time of 61.8 days (34.2– 134.5 days) within the area.
4 | D I S C U S S I O N
4.1 | Connectivity in the Red Sea
Despite being mostly derived from opportunistically sourced data, the recapture rate for Red SeaM. birostris(24.7%) falls within the range established by directed research efforts in Indonesia, Mexico, and Mozambique (16.8%–28.2%) (Marshall,2008; Stewart et al.,2018b;
Beale et al., 2019). The study area as a whole produced a linear discovery curve and an open-population model, indicating that observedM. birostrisare moving into unmonitored areas of the Red Sea and possibly into the wider Indian Ocean. Genetic analysis has shown no population structure across globalM. birostrispopulations (Hosegood et al., 2020), indicating that although M. birostris form distinct regional subpopulations and display limited movements
F I G U R E 5 Number of all known juvenileMobula birostris(female, male, and undetermined sex) in the database sighted each year in Sharm el-Sheikh. The coloured bars represent recaptured individuals with sightings across more than one year (n=14). Note that the effort is not consistent, nor standardized.
*There were no sightings of juvenile M. birostrisin 2020, and this is likely to be attributable to the lockdown that occurred during the COVID-19 pandemic
T A B L E 3 Maximum-likelihood model AIC results based on lagged identification rates (LIRs) ofMobula birostrisencounters in the Red Sea
Model Assumption ΔAIC Overall ΔAIC Sharm el-Sheikh ΔAIC Daedalus
A Closed 461.37 152.45 156.71
B Closed (a1=N) 461.37 152.45 156.71
C Emigration/mortality 116.79 10.13 0.00
D Emigration and mortality (a1=N;a2=mean residence time) 116.79 10.13 0.00
E Closed: emigration+re-immigration 32.20 11.29 2.00
F Emigration+re-immigration (a1=N;a2=mean time in study area;a3=mean time out of study area)
32.20 12.13 2.00
G Emigration+re-immigration+mortality 99.45 14.13 4.00
H Emigration+re-immigration+mortality (a1=N;a2=mean time in study area;a3=mean time out of study area;
a4=mortality)
0.00 0.00 2.82
(Stewart et al., 2016a), their ability to move long distances creates opportunity for gene flow. Similar methods could confirm the isolation of Red Sea M. birostris or establish their connectivity to nearby cohorts in the Gulf of Aden and the Indian Ocean. Regardless, the movement patterns described within the northern Red Sea mean that the basin is likely to host a single, well-mixed population of M. birostrisas opposed to several smaller ones. A single population is easier to conserve, but the international movements exhibited by some individuals in this study mean that cooperation between Red Sea countries may be necessary for protection to be effective (Gajdzik et al.,2021). Additionally, recent evidence suggests that cargo ship strikes could be an under-reported and significant contributor to whale shark mortality (Womersley et al., 2022). A high degree of surface occupation (Andrzejaczek et al., 2021) and the frequent movements of oceanic manta rays across one of the busiest shipping lanes in the world may also make this species vulnerable to similar threats (Braun,2013). Encouragingly though, this study has identified several key aggregation areas forM. birostrisin Egypt alone, meaning that any national protection policies introduced through the Egyptian government could have a significant positive impact on the conservation of this population.
4.2 | Proposed nursery ground
The ontogenetic demographics and residency behaviour shown for Sharm el-Sheikh fit the criteria for an elasmobranch nursery (Heupel, Carlson & Simpfendorfer, 2007). The first criterion is a high proportion of juveniles, which at Sharm el-Sheikh account for 82% of the sample for which life stages were assessed (58 juveniles out of 71 individuals assessed). Considering only male individuals, 27 were classified as juveniles and 10 were classified as subadults/adults (73%
juvenile males). This proportion of juvenile males was the highest at this site out of all areas studied in the Red Sea and the second highest proportion recorded at any site globally (Stewart et al., 2018b).
Sightings of juvenileM. birostrisare rare at known aggregation sites in Ecuador (Harty et al., unpubl. data), Indonesia (Beale et al.,2019), and Mozambique (Marshall,2008). The only other location in the world with a higher proportion of encountered juvenile maleM. birostrisis in the Flower Garden Banks (juvenile male proportion = 8/9, 89%), located in the Gulf of Mexico (Stewart et al.,2018b). However, this site appears to be predominantly used by the putative third species of manta ray,M.cf. birostris(Hosegood et al.,2020), and not purely a nursery area forM. birostris. A high incidence of capture of juvenile M. birostrisdoes occur in Filipino and Sri LankanMobulafisheries, but the specific sites where these individuals are being fished currently remain unknown (Rambahiniarison et al., 2018; Fernando &
Stewart, 2021). The second criterion of an elasmobranch nursery is short-term residency, which ranges from approximately a week to several months at Sharm el-Sheikh, based on the LIR modelling and resighting patterns. The third and final criterion is long-term site fidelity, which has been demonstrated for Sharm el-Sheikh by the LIR modelling and resighting records that show immature M. birostris
returning to the area over multiple years at both the population level and the individual level. If these traits are confirmed by additional research efforts, Sharm el-Sheikh would become the first nursery site described forM. birostrisin the Indo-Pacific.
Although age at maturity forM. birostrisremains unknown, the 4-year time span over which three individual males were observed as juveniles suggests that M. birostris follows a similar timeline to sexual maturity as male M. alfredi, which is estimated to be 9– 10 years (Stevens, 2016). Male RS0067B was first sighted as a juvenile in 2009 and later as a mature adult in 2021; however, the age at which this individual reached sexual maturity during this time remains undetermined. Nevertheless, the high recapture rate of M. birostris in the Red Sea along with the high proportion of juvenile males at Sharm el-Sheikh and subadult males at Daedalus Reef provide a unique opportunity for the long-term monitoring of sexual maturation. Lastly, observations in this study provide some of the first recorded movements of juvenile M. birostris, indicating that these individuals can occupy a variety of habitats (offshore and coastal) and can move large distances. A significantly higher resighting rate for juveniles than adults indicate that juveniles may display higher residency in their preferred habitats (that happen to have high human–manta overlap) than adults, which may be more transient.
4.3 | Population demographics
Overall, M. birostris in the Red Sea appear to be at sexual parity.
This is in contrast to photo-ID studies from other areas in Australia, Indonesia, and Mozambique, which typically found significant female biases in both M. alfredi (Couturier et al., 2018) and M. birostris populations (Marshall, 2008; Beale et al., 2019). However, most of these other studies focused on data collection at cleaning stations, which disproportionately attract mature females (Stevens, 2016). In contrast, cleaning behaviours were rarely observed in the Red Sea, whereas foraging (including both surface and somersault feeding) and cruising were common. Elphinstone Reef was the sole exception, exhibiting both female bias and providing the only examples of cleaning behaviour in the dataset. Four out of five pregnant females identified in this study were also encountered at Elphinstone Reef. Very little is known about M. birostrisgestation and parturition (Rambahiniarison et al., 2018), and although it is difficult to draw firm conclusions from just four encounters, the site may serve an important reproductive function for this species in the Red Sea. Taken together, the female dominance at Elphinstone Reef, male dominance at St. John’s Reefs, along with the parity found at most other regions within the Red Sea suggests that segregation behaviour is likely to be site specific, depending on the ecological characteristics of each area.
Similar to the distribution of the sexes, sighting records for the Red Sea suggest a mixture of ontogenetically integrated and segregated habitats. Globally, encounters with immatureM. birostris are rare (Stewart et al., 2018a; Stewart et al., 2018b), causing
much of the available literature to be ontogenetically skewed. This makes the dominance of juveniles at both Daedalus Reef and Sharm el-Sheikh particularly interesting, as these sites could provide valuable insight into the early life stages of the species.
The shared and separate habitat use between juvenile and adult M. birostris in the Red Sea mirror findings from both the Philippines (Rambahiniarison et al.,2018), where individuals from all life stages were caught in the same net, and from other studies in Mozambique and Indonesia, where adult-dominated aggregations are typically described (Marshall,2008; Beale et al.,2019).
4.4 | Spatio-temporal patterns
This study does present limitations arising from the opportunistic way in which the data were collected. The use of publicly sourced data makes it impossible to standardize observer effort, so apparent seasonal trends in sightings may be explained by corresponding fluctuations in tourism (Norman et al., 2017) or other unknown factors. However, the seasonal patterns suggested by the data are also supported by anecdotal accounts from local dive guides. For instance, tour operators in Sharm el-Sheikh have reported consistent seasonal patterns ofM. birostrispresence/absence at dive sites, with higher encounter likelihoods beginning in April and lasting into summer (A.M. Knochel, unbuplished data). The seasonality of M. birostris presence has been documented in other regional populations in Mexico, with individuals shifting between offshore and inshore sites as well as vertically in the water column (Stewart et al., 2016b; Garzon et al., 2020). Confirming this apparent seasonality within the Red Sea will require dedicated boat-based surveys and/or acoustic telemetry studies, which can be used for future modelling techniques. Similar research has already been conducted on other Red Sea mega-planktivores, such asR. typusand M. alfredi in Saudi Arabia and Sudan (Braun et al., 2015; Cochran et al.,2019; Knochel et al.,2022), and these methods could also be applied toM. birostris.
When bathymetry is considered, there is a clear tendency for encounters to occur along the shelf edge and the central seamounts, likely reflecting areas of both high human–M. birostris overlap and preference for habitats close to deep water. Similarly, most encounters occur at popular dive sites along the Egyptian coast, likely in part because these areas receive a disproportionate level of human visitation. However, both Israel and Jordan attract high levels of dive tourism (Zakai & Chadwick-Furman,2002) but record relatively few M. birostrissightings. This may be attributed to their limited coastlines (roughly 12 and 26 km, respectively), as compared with Egypt (1,500 km) or Saudi Arabia (1,760 km). Finally, there are no records of M. birostrisencounters from Eritrea or Yemen. This may be because of geopolitical factors limiting both research and tourism activities (Gebreyohanns,2008) but could also be explained by less deep-water habitat in the southern Red Sea, as compared with the northern Red Sea. Consistent with this explanation is that most sightings of reef-associated M. alfredicome from the central and southern Red
Sea, despite reduced diving effort in these regions (Kashiwagi et al.,2011; Braun et al.,2015; Kessel et al.,2017).
5 | C O N C L U S I O N S
This research shows that a significant population of previously unstudiedM. birostrisinhabit the north-central Red Sea and extends its known range into the Gulf of Aqaba (Marshall et al.,2020). The imagery-derived data herein suggest that the population, particularly of juveniles, exhibits regional site fidelity. The absence of records in the southern Red Sea and the semi-isolation of this peripheral basin (DiBattista et al., 2016) may indicate limited connectivity to other populations in the Western Indian Ocean. Considering the putative isolation, conservative life history, and global vulnerability of oceanic mantas to anthropogenic threats, conservation management plans are urgently required to safeguard this endangered species in the Red Sea. Although elasmobranch populations have suffered steep declines from unsustainable fishing practices in the Red Sea (Spaet &
Berumen, 2015), there is no evidence that manta rays are directly targeted (Jabado & Spaet,2017). However,M. birostrismay still face growing threats from irresponsible tourism practices, vessel strikes, unmitigated coastal development, and entanglement in fishing gear and other marine debris. Member states of the Red Sea should consider implementing national protections for the species, prioritizing policies endorsed by the Convention of Migratory Species.
Specifically, spatial protections regarding fishing and tourism practices around currently identified key aggregation sites should be explored.
Such plans may consider vessel speed restrictions (Rohner et al., 2020) and the implementation of tourism codes of conduct (Venables et al.,2016; Murray et al.,2020).
This study would not have been possible without sourcing photo- IDs from social media platforms, which accounted for nearly half of all identified individuals. Along with researcher and NGO records, these data helped to describe the movements and demographics of M. birostris within the Red Sea for the first time. The results underscore the utility of social platforms as an expanding source of ecologically relevant data and the volume of potential data that could be collected via citizen science programmes. Increased participation throughout the Red Sea dive community through more directed outreach programmes could significantly improve both the spatial and temporal coverage of tourism-based monitoring, offering researchers a tangible benefit for outreach efforts to tour operators and other local stakeholders (DiBattista et al., 2021). In addition, this social media data-mining methodology is broadly applicable and could be employed across a wide variety of charismatic species (Halloran, Murdoch & Becker, 2015; Cerutti-Pereyra et al., 2017; Bargnesi, Lucrezi & Ferretti, 2020) in most habitats. However, although the preliminary insights provided by crowdsourced data can be invaluable, they should be confirmed and further explored through formal study.
Citizen science cannot replace dedicated research effort, but is an inexpensive tool for guiding field plans and directing experimental design.
A C K N O W L E D G E M E N T S
We are grateful for the countless number of people that sent us information about their oceanic manta ray encounters, including: Adi Barash and her Facebook group, Sharks in Israel; Estelle Gay with Red Sea Diving Safari; Abdulelah Bashrahil with Dolphin Divers in Saudi Arabia; Nina Eschner with Blue Planet Liveaboards; the team at Circle Divers and the Camel Dive Club in Sharm el-Sheikh; and Libby Bowels and Catherine Bates for their many submissions to Manta Matcher.
C O N F L I C T O F I N T E R E S T
The authors declare that they have no conflicts of interest associated with this work.
D A T A A V A I L A B I L I T Y S T A T E M E N T
Photo-ID images captured by the authors or where explicit permission from data owners has been given are deposited to Manta Matcher and the Manta Trust. Images and videos taken from social media are linked Data S3. The full archive of photo-ID data annotation is available from Data S1 and Data S2. As a result of copyright of original media content, the entire collection of raw photo-ID images has not been published in the Supporting Information, but is available upon reasonable request.
O R C I D
Anna M. Knochel https://orcid.org/0000-0002-7396-4586 Jesse E. M. Cochran https://orcid.org/0000-0002-6027-5052 Alexander Kattan https://orcid.org/0000-0001-7587-3584 Guy M. W. Stevens https://orcid.org/0000-0002-2056-9830 Michael L. Berumen https://orcid.org/0000-0003-2463-2742
R E F E R E N C E S
Andrzejaczek, S., Schallert, R.J., Forsberg, K., Arnoldi, N.S., Cabanillas- Torpoco, M., Purizaca, W. et al. (2021). Reverse diel vertical movements of oceanic manta rays off the northern coast of Peru and implications for conservation.Ecological Solutions and Evidence, 2(1), e12051.https://doi.org/10.1002/2688-8319.12051
Araujo, G., Legaspi, C., Matthews, K., Ponzo, A., Chin, A. & Manjaji- Matsumoto, B.M. (2020). Citizen science sheds light on the cryptic ornate eagle rayAetomylaeus vespertilio.Aquatic Conservation: Marine and Freshwater Ecosystems, 30(10), 2012–2018. https://doi.org/10.
1002/aqc.3457
Araujo, G., Snow, S., So, C.L., Labaja, J., Murray, R., Colucci, A. et al. (2017).
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, 27(1), 237–252.https://doi.org/10.1002/aqc.
2636
Bargnesi, F., Lucrezi, S. & Ferretti, F. (2020). Opportunities from citizen science for shark conservation, with a focus on the Mediterranean Sea.The European Zoological Journal, 87(1), 20–34.https://doi.org/10.
1080/24750263.2019.1709574
Beale, C.S., Stewart, J.D., Setyawan, E., Sianipar, A.B. & Erdmann, M.V.
(2019). Population dynamics of oceanic manta rays (Mobula birostris) in the Raja Ampat archipelago, West Papua, Indonesia, and the impacts of the El Niño–southern oscillation on their movement ecology.
Diversity and Distributions, 25(9), 1472–1487. https://doi.org/10.
1111/ddi.12962
Berumen, M.L., Hoey, A.S., Bass, W.H., Bouwmeester, J., Catania, D., Cochran, J.E.M. et al. (2013). The status of coral reef ecology research in the Red Sea.Coral Reefs, 32(3), 737–748.https://doi.org/10.1007/
s00338-013-1055-8
Boldrocchi, G. & Storai, T. (2021). Data-mining social media platforms highlights conservation action for the Mediterranean critically endangered blue sharkPrionace glauca.Aquatic Conservation: Marine and Freshwater Ecosystems, 31(11), 3087–3099. https://doi.org/10.
1002/AQC.3690
Braun, C.D. (2013).Movement ecology of the reef manta ray Manta alfredi in the eastern Red Sea. King Abdullah University of Science and Technology.
Braun, C.D., Skomal, G.B., Thorrold, S.R. & Berumen, M.L. (2014). Diving behavior of the reef manta ray links coral reefs with adjacent deep pelagic habitats. PLoS ONE, 9(2), e88170. https://doi.org/10.1371/
journal.pone.0088170
Braun, C.D., Skomal, G.B., Thorrold, S.R. & Berumen, M.L. (2015).
Movements of the reef manta ray (Manta alfredi) in the Red Sea using satellite and acoustic telemetry.Marine Biology, 162(12), 2351–2362.
https://doi.org/10.1007/s00227-015-2760-3
Bucair, N., Venables, S.K., Balboni, A.P. & Marshall, A.D. (2021). Sightings trends and behaviour of manta rays in Fernando de Noronha archipelago, Brazil.Marine Biodiversity Records, 14(1), 10. https://doi.
org/10.1186/s41200-021-00204-w
Burgess, K.B., Couturier, L.I.E., Marshall, A.D., Richardson, A.J., Weeks, S.J.
& Bennett, M.B. (2016). Manta birostris, predator of the deep? Insight into the diet of the giant manta ray through stable isotope analysis.
Royal Society Open Science, 3(11), 160717.https://doi.org/10.1098/
rsos.160717
Cerutti-Pereyra, F., Bassos-Hull, K., Arvizu-Torres, X., Wilkinson, K.A., García-Carrillo, I., Perez-Jimenez, J.C. et al. (2017). Observations of spotted eagle rays (Aetobatus narinari) in the Mexican Caribbean using photo-ID.Environmental Biology of Fishes, 101(2), 237–244.https://
doi.org/10.1007/S10641-017-0694-Y
Chin, A. (2014). “Hunting porcupines”: citizen scientists contribute new knowledge about rare coral reef species.Pacific Conservation Biology, 20(1), 48–53.https://doi.org/10.1071/pc140048
Chin, A. & Pecl, G. (2018). Citizen science in shark and ray research and conservation: strengths, opportunities, considerations and pitfalls. In:
Carrier, J.C., Heithaus, M.R. & Simpfendorfer, C.A. (Eds.) Shark research: Emerging technologies and applications for the field and laboratory: CRC Press, pp. 299–317.
Cochran, J.E.M., Braun, C.D., Cagua, E.F., Campbell, M.F., Jr., Hardenstine, R.S., Kattan, A. et al. (2019). Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea. PLoS ONE, 14(9), e0222285.https://doi.org/10.1371/journal.pone.0222285
Couturier, L.I.E., Newman, P., Jaine, F.R.A., Bennett, M.B., Venables, W.N., Cagua, E.F. et al. (2018). Variation in occupancy and habitat use of Mobula alfredi at a major aggregation site. Marine Ecology Progress Series, 599, 125–145.https://doi.org/10.3354/meps12610
Davies, T.K., Stevens, G., Meekan, M.G., Struve, J. & Rowcliffe, J.M.
(2012). Can citizen science monitor whale-shark aggregations?
Investigating bias in mark–recapture modelling using identification photographs sourced from the public.Wildlife Research, 39(8), 696– 704.https://doi.org/10.1071/WR12092
DiBattista, J.D., Howard Choat, J., Gaither, M.R., Hobbs, J.-P.A., Lozano- Cortés, D.F., Myers, R.F. et al. (2016). On the origin of endemic species in the Red Sea.Journal of Biogeography, 43(1), 13–30.https://
doi.org/10.1111/jbi.12631
DiBattista, J.D., West, K.M., Hay, A.C., Highes, J.M., Fowler, A.M. &
McGrouther, M.A. (2021). Community-based citizen science projects can support the distributional monitoring of fishes. Aquatic Conservation: Marine and Freshwater Ecosystems, 31(12), 3580–3593.
https://doi.org/10.1002/aqc.3726
Duffy, L.M., Lennert-Cody, C.E., Olson, R.J., Minte-Vera, C.V. &
Griffiths, S.P. (2019). Assessing vulnerability of bycatch species in the tuna purse-seine fisheries of the eastern Pacific Ocean. Fisheries Research, 219, 105316. https://doi.org/10.1016/j.fishres.2019.
105316
Fernando, D. & Stewart, J.D. (2021). High bycatch rates of manta and devil rays in the “small-scale” artisanal fisheries of Sri Lanka. PeerJ, 9, e11994.https://doi.org/10.7717/PEERJ.11994
Gadig, O.B.F. & Neto, D.G. (2014). Notes on the feeding behaviour and swimming pattern ofManta alfredi(Chondrichthyes, Mobulidae) in the Red Sea.Acta Ethologica, 17(2), 119–122.https://doi.org/10.1007/
s10211-013-0165-1
Gajdzik, L., Green, A.L., Cochran, J.E.M., Hardenstine, R.S., Tanabe, L.K. &
Berumen, M.L. (2021). Using species connectivity to achieve coordinated large-scale marine conservation efforts in the Red Sea.
Marine Pollution Bulletin, 166, 112244. https://doi.org/10.1016/j.
marpolbul.2021.112244
Garzon, F., Graham, R.T., Witt, M.J. & Hawkes, L.A. (2020). Ecological niche modeling reveals manta ray distribution and conservation priority areas in the Western Central Atlantic. Animal Conservation, 24(3), 322–334.https://doi.org/10.1111/acv.12663
Gebreyohanns, M.Z. (2008). The state of tourism in Eritrea: tourism development in the Dahlak Islands [University of Pretoria]. https://
repository.up.ac.za/handle/2263/29317
Germanov, E.S. & Marshall, A.D. (2014). Running the gauntlet: regional movement patterns ofManta alfredithrough a complex of parks and fisheries.PLoS ONE, 9(10), e115660.https://doi.org/10.1371/journal.
pone.0110071
Giovos, I., Stoilas, V.-O., Al-Mabruk, S.A.A., Doumpas, N., Marakis, P., Maximiadi, M. et al. (2019). Integrating local ecological knowledge, citizen science and long-term historical data for endangered species conservation: additional records of angel sharks (Chondrichthyes:
Squatinidae) in the Mediterranean Sea.Aquatic Conservation: Marine and Freshwater Ecosystems, 29(6), 881–890.https://doi.org/10.1002/
aqc.3089
Halloran, K.M., Murdoch, J.D. & Becker, M.S. (2015). Applying computer- aided photo-identification to messy datasets: a case study of Thornicroft's giraffe (Giraffa camelopardalis thornicrofti).African Journal of Ecology, 53(2), 147–155.https://doi.org/10.1111/AJE.12145 Hass, H. (1951). Adventures in the Red Sea.
Heupel, M.R., Carlson, J.K. & Simpfendorfer, C.A. (2007). Shark nursery areas: concepts, definition, characterization and assumptions.Marine Ecology Progress Series, 337, 287–297. https://doi.org/10.3354/
meps337287
Hosegood, J., Humble, E., Ogden, R., de Bruyn, M., Creer, S., Stevens, G.M.W. et al. (2020). Phylogenomics and species delimitation for effective conservation of manta and devil rays.
Molecular Ecology, 29(24), 4783–4796.https://doi.org/10.1111/MEC.
15683
Jabado, R.W. & Spaet, J.L.Y. (2017). Elasmobranch fisheries in the Arabian seas region: characteristics, trade and management.Fish and Fisheries, 18(6), 1096–1118.https://doi.org/10.1111/faf.12227
Kashiwagi, T., Marshall, A.D., Bennett, M.B. & Ovenden, J.R. (2011).
Habitat segregation and mosaic sympatry of the two species of manta ray in the Indian and Pacific oceans:Manta alfredi andM. Birostris.
Marine Biodiversity Records, 4(e53), 1–8. https://doi.org/10.1017/
S1755267211000479
Kessel, S.T., Elamin, N.A., Yurkowski, D.J., Chekchak, T., Walter, R.P., Klaus, R. et al. (2017). Conservation of reef manta rays (Manta alfredi) in a UNESCO world heritage site: large-scale island development or sustainable tourism?PLoS ONE, 12(10), e0185419.https://doi.org/10.
1371/journal.pone.0185419
Knochel, A.M., Hussey, N.E., Kessel, S.T., Braun, C.D., Cochran, J.E.M., Hill, G. et al. (2022). Home sweet home: spatiotemporal distribution and site fidelity of the reef manta ray (Mobula alfredi) in Dungonab
Bay, Sudan. Movement Ecology, 10(1), 22. https://doi.org/10.1186/
s40462-022-00314-9
Marshall, A.D. (2008).Biology and population ecology of Manta birostris in southern Mozambique. University of Queensland.
Marshall, A.D., Barreto, R., Carlson, J., Fernando, D., Fordham, S., Francis, M.P. et al. (2020).Mobula birostris, Giant manta ray.IUCN Red List of Threatened Species2020: e.T198921A68632946. https://doi.
org/10.2305/IUCN.UK.2020-3.RLTS.T198921A68632946.en [Accessed 2 Nov 2021].
Marshall, A.D. & Holmberg, J.A. (2021).Manta Matcher Photo-Identification Library.https://www.mantamatcher.org[Accessed 31 Mar 2021].
Marshall, A.D. & Pierce, S.J. (2012). The use and abuse of photographic identification in sharks and rays.Journal of Fish Biology, 80(5), 1361– 1379.https://doi.org/10.1111/j.1095-8649.2012.03244.x
McCoy, E., Burce, R., David, D., Aca, E.Q., Hardy, J., Labaja, J. et al. (2018).
Long-term photo-identification reveals the population dynamics and strong site Fidelity of adult whale sharks to the coastal waters of Donsol, Philippines.Frontiers in Marine Science, 5, 271.https://doi.org/
10.3389/fmars.2018.00271
Murray, A., Garrud, E., Ender, I., Lee-Brooks, K., Atkins, R., Lynam, R. et al.
(2020). Protecting the million-dollar mantas; creating an evidence- based code of conduct for manta ray tourism interactions.Journal of Ecotourism, 19(2), 132–147.https://doi.org/10.1080/14724049.2019.
1659802
Norman, B.M., Holmberg, J.A., Arzoumanian, Z., Reynolds, S.D., Wilson, R.
P., Rob, D. et al. (2017). Undersea constellations: the global biology of an endangered marine Megavertebrate further informed through citizen science. Bioscience, 67(12), 1029–1043. https://doi.org/10.
1093/biosci/bix127
Norton, S.L., Wiley, T.R., Carlson, J.K., Frick, A.L., Poulakis, G.R. &
Simpfendorfer, C.A. (2012). Designating critical habitat for juvenile endangered Smalltooth sawfish in the United States. Marine and Coastal Fisheries, 4(1), 473–480.https://doi.org/10.1080/19425120.
2012.676606
O'Malley, M.P., Lee-Brooks, K. & Medd, H.B. (2013). The global economic impact of manta ray watching tourism. PLoS ONE, 8(5), e65051.
https://doi.org/10.1371/journal.pone.0065051
R Core Team. (2020). R: a language and environment for statistical computing. R Foundation for statistical computing.https://www.R- project.org/
Racault, M.F., Raitsos, D.E., Berumen, M.L., Brewin, R.J.W., Platt, T., Sathyendranath, S. et al. (2015). Phytoplankton phenology indices in coral reef ecosystems: application to ocean-color observations in the Red Sea.Remote Sensing of Environment, 160, 222–234.https://doi.
org/10.1016/j.rse.2015.01.019
Raitsos, D.E., Yi, X., Platt, T., Racault, M., Brewin, R.J.W., Pradhan, Y. et al.
(2015). Monsoon oscillations regulate fertility of the Red Sea.
Geophysical Research Letters, 42(3), 855–862. https://doi.org/10.
1002/2014GL062882
Rambahiniarison, J.M., Lamoste, M.J., Rohner, C.A., Murray, R., Snow, S., Labaja, J. et al. (2018). Life history, growth, and reproductive biology of four mobulid species in the Bohol Sea, Philippines. Frontiers in Marine Science, 5(AUG), 269. https://doi.org/10.3389/fmars.2018.
00269
Rohner, C.A., Cochran, J.E.M., Cagua, E.F., Prebble, C.E.M., Venables, S.K., Berumen, M.L. et al. (2020). No place like home? High residency and predictable seasonal movement of whale sharks off Tanzania.
Frontiers in Marine Science, 7, 423. https://doi.org/10.3389/fmars.
2020.00423
Silvertown, J. (2009). A new dawn for citizen science.Trends in Ecology &
Evolution, 24(9), 467–471.https://doi.org/10.1016/j.tree.2009.03.017 Spaet, J.L.Y. & Berumen, M.L. (2015). Fish market surveys indicate unsustainable elasmobranch fisheries in the Saudi Arabian Red Sea.
Fisheries Research, 161, 356–364. https://doi.org/10.1016/j.fishres.
2014.08.022
Spalding, M., Burke, L., Wood, S.A., Ashpole, J., Hutchison, J. & zu Ermgassen, P. (2017). Mapping the global value and distribution of coral reef tourism. Marine Policy, 82, 104–113. https://doi.org/10.
1016/j.marpol.2017.05.014
Stevens, G. (2016). Conservation and Population Ecology of Manta Rays in the Maldives. In:PhD thesis, University of York(Issue August, pp. 1– 207). University of York. https://etheses.whiterose.ac.uk/16981/1/
GuyStevens_DoctoralThesis_ConservationandPopulationEcologyof MantaRaysintheMaldives_2016.pdf
Stevens, G., Fernando, D., Dando, M. & Notarbartolo Di Sciara, G. (2018).
Guide to the manta and devil rays of the world. Wild Nature Press.
https://press.princeton.edu/books/paperback/9780995567399/
guide-to-the-manta-and-devil-rays-of-the-world
Stewart, J.D., Beale, C.S., Fernando, D., Sianipar, A.B., Burton, R.S., Semmens, B.X. et al. (2016a). Spatial ecology and conservation of Manta birostrisin the indo-Pacific.Biological Conservation, 200, 178– 183.https://doi.org/10.1016/j.biocon.2016.05.016
Stewart, J.D., Hoyos-Padilla, E.M., Kumli, K.R. & Rubin, R.D. (2016b).
Deep-water feeding and behavioral plasticity in Manta birostris revealed by archival tags and submersible observations. Zoology, 119(5), 406–413.https://doi.org/10.1016/j.zool.2016.05.010 Stewart, J.D., Jaine, F.R.A., Armstrong, A.J., Armstrong, A.O., Bennett, M.
B., Burgess, K. et al. (2018a). Research priorities to support effective manta and devil ray conservation.Frontiers in Marine.Science, 5(SEP), 1–27.https://doi.org/10.3389/fmars.2018.00314
Stewart, J.D., Nuttall, M., Hickerson, E.L. & Johnston, M.A. (2018b).
Important juvenile manta ray habitat at flower garden banks National Marine Sanctuary in the northwestern Gulf of Mexico.Marine Biology, 165(7), 111.https://doi.org/10.1007/s00227-018-3364-5
Theobald, E.J., Ettinger, A.K., Burgess, H.K., DeBey, L.B., Schmidt, N.R., Froehlich, H.E. et al. (2015). Global change and local solutions: tapping the unrealized potential of citizen science for biodiversity research.
Biological Conservation, 181, 236–244. https://doi.org/10.1016/j.
biocon.2014.10.021
Venables, S., McGregor, F., Brain, L. & van Keulen, M. (2016). Manta ray tourism management, precautionary strategies for a growing industry:
a case study from the Ningaloo Marine Park, Western Australia.Pacific Conservation Biology, 22(4), 295–300. https://doi.org/10.1071/
PC16003
Walter, R.P., Kessel, S.T., Alhasan, N., Fisk, A.T., Heath, D.D., Chekchak, T.
et al. (2014). First record of livingManta alfredi Manta birostris hybrid. Marine Biodiversity, 44(1), 1–2. https://doi.org/10.1007/
s12526-013-0183-2
Ward-Paige, C.A. & Lotze, H.K. (2011). Assessing the value of recreational divers for Censusing elasmobranchs. PLoS ONE, 6(10), e25609.
https://doi.org/10.1371/journal.pone.0025609
Womersley, F.C., Humphries, N.E., Quieroz, N., Vedor, M., da Costa, I., Furtado, M. et al. (2022). Global collision-risk hotspots of marine traffic and the world's largest fish, the whale shark.Proceedings of the National Academy of Sciences of the United States of America, 119(20), e2117440119.https://doi.org/10.1073/pnas.2117440119
Yokoi, H., Ijima, H., Ohshimo, S. & Yokawa, K. (2017). Impact of biology knowledge on the conservation and management of large pelagic sharks.Scientific Reports, 7(1), 1–14.https://doi.org/10.1038/s41598- 017-09427-3
Zakai, D. & Chadwick-Furman, N.E. (2002). Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea.Biological Conservation, 105(2), 179–187.https://doi.org/10.1016/S0006-3207 (01)00181-1
S U P P O R T I N G I N F O R M A T I O N
Additional supporting information can be found online in the Supporting Information section at the end of this article.
How to cite this article:Knochel, A.M., Cochran, J.E.M., Kattan, A., Stevens, G.M.W., Bojanowksi, E. & Berumen, M.L.
(2022). Crowdsourced data reveal multinational connectivity, population demographics, and possible nursery ground of endangered oceanic manta rays in the Red Sea.Aquatic Conservation: Marine and Freshwater Ecosystems, 1–13.
https://doi.org/10.1002/aqc.3883