Trends in sightings of the stingrays of southern Mozambique
Jennifer Keeping
A B C , Rosanna J. Milligan B , Katie Reeve-Arnold A and David Bailey B
+ Author Affiliations
- Author Affiliations
A All Out Africa Marine Research Centre, Praia do Tofo, Inhambane, Mozambique. Email: katie.reevearnold@gmail.com
B Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, G12 8QQ, UK. Email: r.milligan@nova.edu; david.bailey@glasgow.ac.uk
C Corresponding author. Email: jenniferakeeping@hotmail.co.uk
Marine and Freshwater Research 72(12) 1824-1837 https://doi.org/10.1071/MF21013
Submitted: 15 January 2021 Accepted: 23 August 2021 Published: 14 September 2021
Abstract
Understanding the drivers that influence abundance and distribution of marine species is essential to predict future trends in abundance and inform conservation efforts. This is vital in the largely unregulated coastline of Mozambique, where stingrays are afforded no protection by law and are caught by small-scale fishers. During SCUBA dives from 2012 to 2018, trained citizen scientists recorded 11 environmental, spatial and temporal variables along with the count of four stingray species (Megatrygon microps, Taeniurops meyeni, Neotrygon indica and Pateobatis jenkinsii) in the Inhambane region of Mozambique. By constructing bubble plots and generalised additive mixed models (GAMMs), we analysed the relationship between the probability of sightings of each species with the 11 variables. It is evident that the sightings for each of these four stingrays of the Inhambane region differ spatially and seasonally. The key findings include that T. meyeni and M. microps were found to increase in sighting frequency in different seasons (winter and summer respectively) at similar dive sites typically further from shore. Neotrygon indica commonly occupied the areas closer to shore. Identifying key habitats, and temporal and environmental conditions, is conducive to implementing effective conservation strategies in the region, such as, in this instance, all stingrays could be provided with a refuge in the same area.
Keywords: Dasyatidae, GAMM, citizen science, Mozambique.
References
Albouy, C., Velez, L., Coll, M., Colloca, F., le Loc’h, F., Mouillot, D., and Gravel, D. (2014). From projected species distribution to food-web structure under climate change. Global Change Biology 20, 730–741.| From projected species distribution to food-web structure under climate change.Crossref | GoogleScholarGoogle Scholar | 24214576PubMed |
Barker, M. J., and Schluessel, V. (2005). Managing global shark fisheries: suggestions for prioritizing management strategies. Aquatic Conservation 15, 325–347.
| Managing global shark fisheries: suggestions for prioritizing management strategies.Crossref | GoogleScholarGoogle Scholar |
Bernal, D., Carlson, J. K., Goldman, K. J., and Lowe, C. (2012). ‘Biology of Sharks and their Relatives.’ (Taylor and Francis Group.)
Boggio-Pasqua, A., Flam, A. L., and Marshall, A. D. (2019). Spotting the ‘small eyes’: using photo-ID methodology to study a wild population of smalleye stingrays (Megatrygon microps) in southern Mozambique. PeerJ 7, e7110.
| Spotting the ‘small eyes’: using photo-ID methodology to study a wild population of smalleye stingrays (Megatrygon microps) in southern Mozambique.Crossref | GoogleScholarGoogle Scholar | 31218135PubMed |
Cerutti-Pereyra, F., Meekan, M., Wei, N., O’Shea, O., Bradshaw, C. J. A., and Austin, C. M. (2012). Identification of rays through DNA barcoding : an application for ecologists. PLoS One 7, e36479.
| Identification of rays through DNA barcoding : an application for ecologists.Crossref | GoogleScholarGoogle Scholar | 22701556PubMed |
Chaikin, S., Belmaker, J., and Barash, A. (2020). Coastal breeding aggregations of threatened stingrays and guitarfish in the Levant. Aquatic Conservation 30, 1160–1171.
| Coastal breeding aggregations of threatened stingrays and guitarfish in the Levant.Crossref | GoogleScholarGoogle Scholar |
Chin, A., and Pecl, G. (2018). Citizen science in shark and ray research and conservation. In ‘Shark Research: Emerging Technologies and Applications for the Field and Laboratory’. (Eds J. C. Carrier, M. R. Heithaus, and C. A. Simpfendorfer.) pp. 299–318. (CRC Press: Boca Raton, FL, USA.)
Coll, M., Piroddi, C., Albouy, C., Lasram, F. B. R., Cheung, W. W. L., Christensen, V., Karpouzi, V. S., Guilhaumon, F., Mouillot, D., Paleczny, M., Palomares, M. L., Steenbeek, J., Trujillo, P., Watson, R., and Pauly, D. (2012). The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecology and Biogeography 21, 465–480.
| The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves.Crossref | GoogleScholarGoogle Scholar |
Couturier, L. I. E., Jaine, F. R. A., Townsend, K. A., Weeks, S. J., Richardson, A. J., and Bennett, M. B. (2011). Distribution, site affinity and regional movements of the manta ray, Manta alfredi (Krefft, 1868), along the east coast of Australia. Marine and Freshwater Research 62, 628–637.
| Distribution, site affinity and regional movements of the manta ray, Manta alfredi (Krefft, 1868), along the east coast of Australia.Crossref | GoogleScholarGoogle Scholar |
Davidson, L. N. K., and Dulvy, N. K. (2017). Global marine protected areas to prevent extinctions. Nature Ecology & Evolution 1, 0040.
| Global marine protected areas to prevent extinctions.Crossref | GoogleScholarGoogle Scholar |
Desbiens, A. A., Roff, G., Robbins, W. D., Taylor, B. M., Castro-Sanguino, C., Dempsey, A., and Mumby, P. J. (2021). Revisiting the paradigm of shark-driven trophic cascades in coral reef ecosystems. Ecology 102, 1–13.
| Revisiting the paradigm of shark-driven trophic cascades in coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar |
Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J. V., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S., and White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
| Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |
Dulvy, N. K., Simpfendorfer, C. A., Davidson, L. N. K., Fordham, S. V., Brautigam, A., Sant, G., and Welch, D. J. (2017). Challenges and priorities in shark and ray conservation. Current Biology 27, R565–R572.
| Challenges and priorities in shark and ray conservation.Crossref | GoogleScholarGoogle Scholar | 28586694PubMed |
Fahmi, White, W. T., Manjaji-Matsumoto, B. M., and Pierce, S. J. (2016). Smalleye stingray Megatrygon microps. In ‘The IUCN Red List of Threatened Species 2016’. e.T161582A104166533. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/161582/104166533
Flowers, K. I., Heithaus, M. R., and Papastamatiou, Y. P. (2021). Buried in the sand: uncovering the ecological roles and importance of rays. Fish and Fisheries 22, 105–127.
| Buried in the sand: uncovering the ecological roles and importance of rays.Crossref | GoogleScholarGoogle Scholar |
Frisk, M. G., Miller, T. J., and Dulvy, N. K. (2005). Life histories and vulnerability to exploitation of elasmobranchs: inferences from elasticity, perturbation and phylogenetic analyses. Journal of Northwest Atlantic Fishery Science 35, 27–45.
| Life histories and vulnerability to exploitation of elasmobranchs: inferences from elasticity, perturbation and phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Garza-Gisholt, E., Kempster, R. M., Hart, N. S., and Collin, S. P. (2015). Visual specialisations in five sympatric species of stingrays from the family Dasyatidae. Brain Behaviour Evolution 85, 217–232.
| Visual specialisations in five sympatric species of stingrays from the family Dasyatidae.Crossref | GoogleScholarGoogle Scholar |
Gauthier, A. R. G., Whitehead, D. L., Tibbetts, I. R., and Cribb, B. W. (2018). Morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays: morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays. Journal of Fish Biology 92, 504–514.
| Morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays: morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays.Crossref | GoogleScholarGoogle Scholar |
Halsey, L. G., Curran-Everett, D., Vowler, S. L., and Drummond, G. B. (2015). The fickle P value generates irreproducible results. Nature Methods 12, 179–185.
| The fickle P value generates irreproducible results.Crossref | GoogleScholarGoogle Scholar | 25719825PubMed |
Hameed, S. N. (2018). The Indian Ocean Dipole. In ‘Oxford Research Encyclopedia of Climate Science’. (Oxford University Press.) Available at https://oxfordre.com/climatescience/view/10.1093/acrefore/9780190228620.001.0001/acrefore-9780190228620-e-619 [Verified 30 August 2021].
Heupel, M. R., and Hueter, R. (2002). Importance of prey density in relation to the movement patterns of juvenile blacktip sharks (Carcharhinus limbatus) within a coastal nursey area. Marine and Freshwater Research 53, 543–550.
| Importance of prey density in relation to the movement patterns of juvenile blacktip sharks (Carcharhinus limbatus) within a coastal nursey area.Crossref | GoogleScholarGoogle Scholar |
Hoffmann, M., Hilton-Taylor, C., Angulo, A., Bohm, M., and Brooks, T. M. (2010). The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509.
| The impact of conservation on the status of the world’s vertebrates.Crossref | GoogleScholarGoogle Scholar | 20978281PubMed |
Jaine, F. R. A., Couturier, L. I. E., Weeks, S. J., Townsend, K. A., Bennett, M. B., Fiora, K., and Richardson, A. J. (2012). When giants turn up: sighting trends, environmental influences and habitat use of the manta ray Manta alfredi at a coral reef. PLoS One 7, e46170.
| When giants turn up: sighting trends, environmental influences and habitat use of the manta ray Manta alfredi at a coral reef.Crossref | GoogleScholarGoogle Scholar |
Keeping, J., Reeve-Arnold, K. E., Burns, N. M., Catarina, N., Bailey, D. M., and McNeill, D. C. (2020). Computer-aided photo-identification of a rare stingray, Megatrygon microps. Journal of Fish Biology 96, 815–819.
| Computer-aided photo-identification of a rare stingray, Megatrygon microps.Crossref | GoogleScholarGoogle Scholar | 31856322PubMed |
Kosmala, M., Wiggins, A., Swanson, A., and Simmons, B. (2016). Assessing data quality in citizen science. Frontiers in Ecology and the Environment 14, 551–560.
| Assessing data quality in citizen science.Crossref | GoogleScholarGoogle Scholar |
Kyne, P. M., and White, W. T. (2015). Blotched fantail ray Taeniurops meyeni. In ‘The IUCN Red List of Threatened Species 2015’. e.T60162A68646736. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/60162/68646736
Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia.)
Le Port, A., Lavery, S., and Montgomery, J. C. (2012). Conservation of coastal stingrays: seasonal abundance and population structure of the short-tailed stingray Dasyatis brevicaudata at a Marine Protected Area. ICES Journal of Marine Science 69, 1427–1435.
| Conservation of coastal stingrays: seasonal abundance and population structure of the short-tailed stingray Dasyatis brevicaudata at a Marine Protected Area.Crossref | GoogleScholarGoogle Scholar |
Manjaji-Matsumoto, B. M., Fahmi, and White, W. T. (2016). Jenkins’ whipray Pateobatis jenkinsii. In ‘The IUCN Red List of Threatened Species 2016’. e.T161744A104229717. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/161744/176850023
Marshall, A. D., Kyne, P. M., and Bennett, M. B. (2008). Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller and Henle and Urolophus kapalensis Yearsley and Last): Evidence of ontogenetic shifts and possible resource partitioning. Journal of Fish Biology 72, 883–898.
| Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller and Henle and Urolophus kapalensis Yearsley and Last): Evidence of ontogenetic shifts and possible resource partitioning.Crossref | GoogleScholarGoogle Scholar |
Meekan, M. G., Trevitt, L., Simpfendorfer, C. A., and White, W. (2016). The piggybacking stingray. Coral Reefs 35, 1011.
| The piggybacking stingray.Crossref | GoogleScholarGoogle Scholar |
National Institute for Fisheries Research (2020). Boletim da República, publicação official da Republica de Moçambique, Quinta-fiera 8 de Outubro de 2020, 1 Série – Número 192, Decree 89/2020. (Sea Fisheries Regulation (REPMAR): Maputo, Mozambique.) Available at https://www.portaldogoverno.gov.mz/por/Governo/Legislacao/Boletins-da-Republica/Boletins-da-Republica-2020/BR-N.1-192-III-SERIE-2020
Navia, A. F., Maijia-Falla, P. A., Lopez-Garcia, J., Giraldo, A., and Cruz-Escalona, V. H. (2016). How many trophic roles can elasmobranchs play in a marine tropical network? Marine and Freshwater Research 68, 1–12.
O’Shea, O. R., Thums, M., van Keulen, M., and Meekan, M. (2012). Bioturbation by stingrays at Ningaloo Reef, Western Australia. Marine and Freshwater Research 63, 189–197.
| Bioturbation by stingrays at Ningaloo Reef, Western Australia.Crossref | GoogleScholarGoogle Scholar |
O’Shea, O. R., Thums, M., van Keulen, M., Kempster, R. M., and Meekan, M. (2013). Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82, 1805–1820.
| Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs.Crossref | GoogleScholarGoogle Scholar | 23731138PubMed |
Parra, G. J., Corkeron, P. J., and Marsh, H. (2006). Population sizes, site fidelity and residence patterns of Australian snubfin and Indo-Pacific humpback dolphins: Implications for conservation. Biological Conservation 129, 167–180.
| Population sizes, site fidelity and residence patterns of Australian snubfin and Indo-Pacific humpback dolphins: Implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Pavan-Kumar, A., Kumar, R., Pitale, P., Shen, K., and Borsa, P. (2018). Neotrygon indica sp. nov., the Indian Ocean blue-spotted maskray (Myliobatoidei, Dasyatidae). Comptes Rendus Biologies 341, 120–130.
| Neotrygon indica sp. nov., the Indian Ocean blue-spotted maskray (Myliobatoidei, Dasyatidae).Crossref | GoogleScholarGoogle Scholar | 29415869PubMed |
Pierce, S. J., White, W. T., and Marshall, A. D. (2008a). New record of the smalleye stingray, Dasyatis microps (Myliobatiformes: Dasyatidae), from the western Indian Ocean. Zootaxa 1734, 65–68.
| New record of the smalleye stingray, Dasyatis microps (Myliobatiformes: Dasyatidae), from the western Indian Ocean.Crossref | GoogleScholarGoogle Scholar |
Pierce, S. J., Trerup, M., Williams, C., Tilley, A., Marshall, A. D., and Raba, N. (2008b). Shark fishing in Mozambique: a preliminary assessment of artisanal fisheries. Report, Eyes on the Horizon, Maputo, Mozambique.
Rohner, C. A., Pierce, S. J., Marshall, A. D., Weeks, S. J., Bennett, M. B., and Richardson, A. J. (2013). Trends in sightings and environmental influences on a coastal aggregation of manta rays and whale sharks. Marine Ecology Progress Series 482, 153–168.
| Trends in sightings and environmental influences on a coastal aggregation of manta rays and whale sharks.Crossref | GoogleScholarGoogle Scholar |
Rohner, C. A., Richardson, A. J., Jaine, F. R. A., Bennett, M. B., Weeks, S. J., Cliff, G., Robinson, D. P., Reeve-Arnold, K. E., and Pierce, S. J. (2018). Satellite tagging highlights the importance of productive Mozambican coastal waters to the ecology and conservation of whale sharks. PeerJ 6, e4161.
| Satellite tagging highlights the importance of productive Mozambican coastal waters to the ecology and conservation of whale sharks.Crossref | GoogleScholarGoogle Scholar | 30065862PubMed |
Sætre, R., and Silva, A. J. (1984). The circulation of the Mozambican Channel. Deep-Sea Research 31, 485–508.
| The circulation of the Mozambican Channel.Crossref | GoogleScholarGoogle Scholar |
Schlaff, A. M., Heupel, M. R., and Simpfendorfer, C. A. (2014). Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review. Reviews in Fish Biology and Fisheries 24, 1089–1103.
| Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review.Crossref | GoogleScholarGoogle Scholar |
Schwartz, F. J. (2007). Survey of tail spine characteristics of stingrays frequenting African, Arabian to Chagos-Maldive Archipelago waters. Smithiana Bulletin 8, 41–52.
Stamoulis, K. A., Delevaux, J. M. S., Williams, I. D., Friedlander, A. M., Reichard, J., Kamikawa, K., and Harvey, E. S. (2020). Incorporating reef fish avoidance behavior improves accuracy of species distribution models. PeerJ 8, e9246.
| Incorporating reef fish avoidance behavior improves accuracy of species distribution models.Crossref | GoogleScholarGoogle Scholar | 32547871PubMed |
Stasinopoulos, D. M., and Rigby, R. A. (2007). Generalized Additive Models for Location Scale and Shape (GAMLSS) in R. Journal of Statistical Software 23, 1–46.
| Generalized Additive Models for Location Scale and Shape (GAMLSS) in R.Crossref | GoogleScholarGoogle Scholar |
Stevens, J. D., Bonfil, R., Dulvy, N. K., and Walker, P. A. (2000). The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.
| The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems.Crossref | GoogleScholarGoogle Scholar |
Temple, A. J., Wambiji, N., Poonian, C. N. S., Jiddawi, N., Stead, S. M., Kiszka, J. J., and Berggren, P. (2019). Marine megafauna catch in southwestern Indian Ocean small-scale fisheries from landings data. Biological Conservation 230, 113–121.
| Marine megafauna catch in southwestern Indian Ocean small-scale fisheries from landings data.Crossref | GoogleScholarGoogle Scholar |
van der Elst, R., and Everett, B. (2015). Offshore fisheries of the southwest Indian Ocean: their status and the impact on vulnerable species. Special publication. (Oceanographic Research Institute.) Available at http://cordioea.net/outputs-results/swiofp-offshore-fisheries-report/%5Cnhttp://www.swiofp.net/
Venables, S., Winstanley, G., Bowles, L., and Marshall, A. (2016). A giant opportunity: the economic impact of manta rays on the Mozambican tourism industry – an incentive for increased management and protection. Tourism in Marine Environments 12, 51–68.
| A giant opportunity: the economic impact of manta rays on the Mozambican tourism industry – an incentive for increased management and protection.Crossref | GoogleScholarGoogle Scholar |
Ward-Paige, C. A., Mora, C., Lotze, H. K., Pattengill-Semmens, C., McClenachan, L., Arias-Castro, E., and Myers, R. A. (2010). Large-scale absence of sharks on reefs in the greater Caribbean: a footprint of human pressures. PLoS One 5, e11968.
| Large-scale absence of sharks on reefs in the greater Caribbean: a footprint of human pressures.Crossref | GoogleScholarGoogle Scholar | 20700530PubMed |
Williams, J. L., Pierce, S. J., Rohner, C. A., Fuentes, M. M. P. B., and Hamann, M. (2017). Spatial distribution and residency of green and loggerhead sea turtles using coastal reef habitats in southern Mozambique. Frontiers in Marine Science 3, 288.
| Spatial distribution and residency of green and loggerhead sea turtles using coastal reef habitats in southern Mozambique.Crossref | GoogleScholarGoogle Scholar |
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M. (2009). ‘Mixed Effects Models and Extensions in Ecology with R.’ (Springer Science+Business Media LLC: New York, NY, USA.)
| Crossref |
