Abstract
Understanding how individual behavior shapes the structure and ecology of populations is key to species conservation and management. Like many elasmobranchs, manta rays are highly mobile and wide-ranging species threatened by anthropogenic impacts. In shallow water environments, these pelagic rays often form groups and perform several apparently socially mediated behaviors. Group structures may result from active choices of individual rays to interact or passive processes. Social behavior is known to affect spatial ecology in other elasmobranchs, but this is the first study providing quantitative evidence for structured social relationships in manta rays. To construct social networks, we collected data from more than 500 groups of reef manta rays (Mobula alfredi) over 5 years in the Raja Ampat Regency of West Papua. We used generalized affiliation indices to isolate social preferences from non-social associations, the first study on elasmobranchs to use this method. Longer lasting social preferences were detected mostly between female rays. We detected assortment of social relations by phenotype and variation in social strategies, with the overall social network divided into two main communities. Overall network structure was characteristic of a dynamic fission-fusion society, with differentiated relationships linked to strong fidelity to cleaning station sites. Our results suggest that fine-scale conservation measures will be useful in protecting social groups of M. alfredi in their natural habitats and that a more complete understanding of the social nature of manta rays will help predict population responses to anthropogenic pressures, such as increasing disturbance from dive tourism.
Significance statement
In social animals, relationships between individuals have important implications for species conservation. Like many other sharks and rays, manta rays are threatened species, and little is known about their natural behavior or how their populations are structured. This study provides evidence of social structure in a wild, free-ranging population of reef manta rays. We show for the first time that individual manta rays have preferred relationships with others that are maintained over time, and structured societies. This study extends our knowledge of elasmobranch ecology and population structuring. Results suggest that understanding social relationships in manta rays will be important in protecting populations from human impacts and developing sustainable, localized conservation and management initiatives.
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Data availability
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request. Photographs of each encounter are available in the MantaMatcher online repository www.mantamatcher.org
References
Anderson RC, Shiham AM, Kitchen-Wheeler A-M, Stevens G (2011) Extent and economic value of manta ray watching in Maldives. Tour Mar Environ 7:15–27. https://doi.org/10.3727/154427310X12826772784793
Ari C (2011) Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives. Open Anat J 3:1–13. https://doi.org/10.2174/1877609401103010001
Ari C, D’Agostino DP (2016) Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness? J Eth 34 (2):167-174. https://doi.org/10.1007/s10164-016-0462-z
Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396. https://doi.org/10.1126/science.7466396
Baird RW, Whitehead H (2000) Social organization of mammal-eating killer whales: group stability and dispersal patterns. Can J Zool 78:2096–2105. https://doi.org/10.1139/z00-155
Bass NC, Mourier J, Knott NA, Day J, Guttridge T, Brown C (2017) Long-term migration patterns and bisexual philopatry in a benthic shark species. Mar Freshw Res 68:1414–1421. https://doi.org/10.1071/MF16122
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social Media. Accessed October 18, 2018, from https://gephi.org/
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bejder L, Fletcher D, Bräger S (1998) A method for testing association patterns of social animals. Anim Behav 56:719–725. https://doi.org/10.1006/anbe.1998.0802
Berger-Tal O, Polak T, Oron A, Lubin Y, Kotler BP, Saltz D (2011) Integrating animal behavior and conservation biology: a conceptual framework. Behav Ecol 22:236–239. https://doi.org/10.1093/beheco/arq224
Blonder B, Wey TW, Dornhaus A, James R, Sih A (2012) Temporal dynamics and network analysis. Methods Ecol Evol 3:958–972. https://doi.org/10.1111/j.2041-210X.2012.00236.x
Bode NWF, Wood AJ, Franks DW (2011) The impact of social networks on animal collective motion. Anim Behav 82:29–38. https://doi.org/10.1016/j.anbehav.2011.04.011
Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225. https://doi.org/10.1017/S1464793104006645
Bradbury JW (1986) Social complexity and cooperation behavior in delphinids. In: Schusterman RJ, Thomas JA, Wood FG (eds) Dolphin cognition and behavior: a comparative approach. Erlbaum, Hilsdale, pp 361–372
Braun CD, Skomal GB, Thorrold SR, Berumen ML (2014) Diving behavior of the reef manta ray links coral reefs with adjacent deep pelagic habitats. PLoS One 9:e88170. https://doi.org/10.1371/journal.pone.0088170
Brena PF, Mourier J, Planes S, Clua EE (2018) Concede or clash? Solitary sharks competing for food assess rivals to decide. Proc R Soc B 285:2018006. https://doi.org/10.1098/rspb.2018.0006
Brown C, Laland K, Krause J (eds) (2011) Fish cognition and behavior. Wiley, Chichester. https://doi.org/10.1002/9781444342536
Bruck JN (2013) Decades-long social memory in bottlenose dolphins. Proc R Soc B 280:20131726. https://doi.org/10.1098/rspb.2013.1726
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Socio Meth Res 33(2), 261-304. https://doi.org/10.1177/0049124104268644
Byrnes EE, Pouca CV, Chambers SL, Brown C (2016) Into the wild: developing field tests to examine the link between elasmobranch personality and laterality. Behaviour 153:1777–1793. https://doi.org/10.1163/1568539X-00003373
Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469. https://doi.org/10.1016/S0003-3472(87)80018-0
Cantor M, Wedekin LL, Guimaraes PR, Daura-Jorge FG, Rossi-Santos MR, Simoes-Lopes PC (2012) Disentangling social networks from spatiotemporal dynamics: the temporal structure of a dolphin society. Anim Behav 84:641–651. https://doi.org/10.1016/j.anbehav.2012.06.019
Chivers DP, Brown GE, Smith RJF (1995) Familiarity and shoal cohesion in fathead minnows (Pimephales promelas): implications for antipredator behaviour. Can J Zool 73:955–960. https://doi.org/10.1139/z95-111
Couturier LI, Marshall AD, Jaine FRA, Kashiwagi T, Pierce SJ, Townsend KA, Richardson AJ (2012) Biology, ecology and conservation of the Mobulidae. J Fish Biol 80:1075–1119. https://doi.org/10.1111/j.1095-8649.2012.03264.x
Couturier LI, Dudgeon CL, Pollock KH, Jaine FRA, Bennett MB, Townsend KA, Richardson AJ (2014) Population dynamics of the reef manta ray Manta alfredi in eastern Australia. Coral Reefs 33:329–342. https://doi.org/10.1007/s00338-014-1126-5
Couzin ID (2006) Behavioral ecology: social organization in fission–fusion societies. Curr Biol 16:169–171. https://doi.org/10.1016/j.cub.2006.02.042
Couzin ID, Krause J (2003) Self-organization and collective behavior in vertebrates. Adv Study Behav 32:1–75. https://doi.org/10.1016/S0065-3454(03)01001-5
Couzin ID, Krause J, James R, Ruxton GD, Franks NR (2002) Collective memory and spatial sorting in animal groups. J Theor Biol 218:1–11. https://doi.org/10.1006/jtbi.2002.3065
Croft DP, Arrowsmith BJ, Bielby J, Skinner K, White E, Couzin ID, Magurran AE, Ramnarine I, Krause J (2003) Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata. Oikos 100:429–438
Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton. https://doi.org/10.1515/9781400837762
Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507. https://doi.org/10.1016/j.tree.2011.05.012
Croft DP, Edenbrow M, Darden SK (2015) Assortment in social networks and the evolution of cooperation. In: Krause J, James AJ, Franks D, Croft DP (eds) Animal social networks. Oxford University Press, Oxford, pp 13–23. https://doi.org/10.1093/acprof:oso/9780199679041.003.0003
Croll DA, Dewar H, Dulvy NK, Fernando D, Francis MP, Galván-Magaña F, Hall M, Heinrichs S, Marshall A, Mccauley D, Newton KM, Notarbartolo-di-Sciara G, O'Malley M, O'Sullivan J, Poortvliet M, Roman M, Stevens G, Tershy BR, White WT (2016) Vulnerabilities and fisheries impacts: the uncertain future of manta and devil rays. Aquat Conserv Mar Freshwat Ecosyst 26:562–575. https://doi.org/10.1002/aqc.2591
Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9
Deakos MH (2010) Ecology and social behavior of a resident manta ray (Manta alfredi) population off Maui, Hawai'i. PhD thesis, University of Hawai’i at Mānoa, http://www.hamerinhawaii.org/wp-content/uploads/DeakosDissertation2010.pdf
Deakos MH (2012) The reproductive ecology of resident manta rays (Manta alfredi) off Maui, Hawaii, with an emphasis on body size. Environ Biol Fish 94:443–456. https://doi.org/10.1007/s10641-011-9953-5
Deakos MH, Baker JD, Bejder L (2011) Characteristics of a manta ray Manta alfredi population off Maui, Hawaii, and implications for management. Mar Ecol Prog Ser 429:245–260. https://doi.org/10.3354/meps09085
Dekker D, Krackhardt D, Snijders TA (2007) Sensitivity of MRQAP tests to collinearity and autocorrelation conditions. Psychometrika 72:563–581. https://doi.org/10.1007/s11336-007-9016-1
Dewar H, Mous P, Domeier M, Muljadi A, Pet J, Whitty J (2008) Movements and site fidelity of the giant manta ray, Manta birostris, in the Komodo Marine Park, Indonesia. Mar Biol 155:121–133. https://doi.org/10.1007/s00227-008-0988-x
Duinkerken DI (2010) Movements and site fidelity of the reef manta ray, Manta alfredi, along the coast of southern Mozambique. MSc thesis, Utrecht University, The Netherlands
Dulvy NK, Pardo SA, Simpfendorfer CA, Carlson JK (2014) Diagnosing the dangerous demography of manta rays using life history theory. PeerJ 2:e400. https://doi.org/10.7717/peerj.400
Ellis S, Franks DW, Nattrass S, Cant MA, Weiss MN, Giles D, Balcomb KC, Croft DP (2017) Mortality risk and social network position in resident killer whales: sex differences and the importance of resource abundance. Proc R Soc B 284:20171313. https://doi.org/10.1098/rspb.2017.1313
Farine DR (2017a) asnipe: animal social network inference and permutations for ecologists. R package version 1.1.4, https://CRAN.R-project.org/package=asnipe
Farine DR (2017b) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320. https://doi.org/10.1111/2041-210X.12772
Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163. https://doi.org/10.1111/1365-2656.12418
Finger JS, Dhellemmes F, Guttridge TL, Kurvers RH, Gruber SH, Krause J (2016) Rate of movement of juvenile lemon sharks in a novel open field, are we measuring activity or reaction to novelty? Anim Behav 116:75–82. https://doi.org/10.1016/j.anbehav.2016.03.032
Finger JS, Dhellemmes F, Guttridge TL (2017) Personality in elasmobranchs with a focus on sharks: early evidence, challenges, and future directions. In: Vonk J, Weiss A, Kuczaj SA (eds) Personality in nonhuman animals. Springer, Cham, pp 129–152. https://doi.org/10.1007/978-3-319-59300-5_7
Foster EA, Franks DW, Morrell LJ, Balcomb KC, Parsons KM, Van Ginneken A, Croft DP (2012) Social network correlates of food availability in an endangered population of killer whales (Orcinus orca). Anim Behav 83:731–736. https://doi.org/10.1016/j.anbehav.2011.12.021
Franks DW, Ruxton GD, James R (2010) Sampling animal association networks with the gambit of the group. Behav Ecol Sociobiol 64:493–503. https://doi.org/10.1007/s00265-009-0865-8
Frère CH, Krützen M, Mann J, Connor RC, Bejder L, Sherwin WB (2010) Social and genetic interactions drive fitness variation in a free-living dolphin population. Proc Natl Acad Sci U S A 107:19949–19954. https://doi.org/10.1073/pnas.1007997107
Frostman P, Sherman PT (2004) Behavioral response to familiar and unfamiliar neighbors in a territorial cichlid, Neolamprologus pulcher. Ichthyol Res 51:283–285. https://doi.org/10.1007/s10228-004-0223-9
Gadig OBF, Neto DG (2014) Notes on the feeding behaviour and swimming pattern of Manta alfredi (Chondrichthyes, Mobulidae) in the Red Sea. Acta Ethol 17:119–122. https://doi.org/10.1007/s10211-013-0165-1
Germanov ES, Marshall AD (2014) Running the gauntlet: regional movement patterns of Manta alfredi through a complex of parks and fisheries. PLoS One 9:e110071. https://doi.org/10.1371/journal.pone.0110071
Gero S, Bejder L, Whitehead H, Mann J, Connor RC (2005) Behaviourally specific preferred associations in bottlenose dolphins, Tursiops spp. Can J Zool 83:1566–1573. https://doi.org/10.1139/z05-155
Godde S, Humbert L, Côté SD, Réale D, Whitehead H (2013) Correcting for the impact of gregariousness in social network analyses. Anim Behav 85:553–558. https://doi.org/10.1016/j.anbehav.2012.12.010
Griffiths SW, Magurran AE (1997) Familiarity in schooling fish: how long does it take to acquire? Anim Behav 53:945–949. https://doi.org/10.1006/anbe.1996.0315
Griffiths SW, Ward A (2011) Social recognition of conspecifics. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Ames, pp 186–216. https://doi.org/10.1002/9781444342536.ch9
Griffiths SW, Brockmark S, Höjesjö J, Johnsson JI (2004) Coping with divided attention: the advantage of familiarity. Proc R Soc Lond B 271:695–699. https://doi.org/10.1098/rspb.2003.2648
Guttridge TL, Gruber SH, DiBattista JD, Feldheim KA, Croft DP, Krause S, Krause J (2011) Assortative interactions and leadership in a free-ranging population of juvenile lemon shark Negaprion brevirostris. Mar Ecol Prog Ser 423:235–245. https://doi.org/10.3354/meps08929
Guttridge TL, van Dijk S, Stamhuis EJ, Krause J, Gruber SH, Brown C (2013) Social learning in juvenile lemon sharks, Negaprion brevirostris. Anim Cogn 16:55–64. https://doi.org/10.1007/s10071-012-0550-6
Hamede RK, Bashford J, McCallum H, Jones M (2009) Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease. Ecol Lett 12:1147–1157. https://doi.org/10.1111/j.1461-0248.2009.01370.x
Heupel MR, Simpfendorfer CA (2005) Quantitative analysis of aggregation behavior in juvenile blacktip sharks. Mar Biol 147:1239–1249. https://doi.org/10.1007/s00227-005-0004-7
Heyman WD, Graham RT, Kjerfve B, Johannes RE (2001) Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Mar Ecol Prog Ser 215:275–282. https://doi.org/10.3354/meps215275
Hinde RA (1976) Interactions, Relationships and Social Structure. Man 1-17. https://doi.org/10.2307/2800384
Hoppitt WJ, Farine DR (2018) Association indices for quantifying social relationships: how to deal with missing observations of individuals or groups. Anim Behav 136:227–238. https://doi.org/10.1016/j.anbehav.2017.08.029
Jacoby DM, Busawon DS, Sims DW (2010) Sex and social networking: the influence of male presence on social structure of female shark groups. Behav Ecol 21:808–818. https://doi.org/10.1093/beheco/arq061
Jacoby DM, Croft DP, Sims DW (2012) Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish Fish 13:399–417. https://doi.org/10.1111/j.1467-2979.2011.00436.x
Jacoby DM, Fear LN, Sims DW, Croft DP (2014) Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behav Ecol Sociobiol 68:1995–2003. https://doi.org/10.1007/s00265-014-1805-9
Jacoby DM, Papastamatiou YP, Freeman R (2016) Inferring animal social networks and leadership: applications for passive monitoring arrays. J R Soc Interface 13:20160676. https://doi.org/10.1098/rsif.2016.0676
Jaine FRA, Couturier LI, Weeks SJ, Townsend KA, Bennett MB, Fiora K, Richardson AJ (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. https://doi.org/10.1371/journal.pone.0046170
Jaine FRA, Rohner CA, Weeks SJ, Couturier LI, Bennett MB, Townsend KA, Richardson AJ (2014) Movements and habitat use of reef manta rays off eastern Australia: offshore excursions, deep diving and eddy affinity revealed by satellite telemetry. Mar Ecol Prog Ser 510:73–86. https://doi.org/10.3354/meps10910
Kalbitzer U, Bergstrom ML, Carnegie SD, Wikberg EC, Kawamura S, Campos FA & Fedigan, LM (2017). Female sociality and sexual conflict shape offspring survival in a Neotropical primate. Proc Nat Acad Sci, 114(8), 1892-1897. https://doi.org/10.1073/pnas.1608625114
Karczmarski L, Würsig B, Gailey G, Larson KW, Vanderlip C (2005) Spinner dolphins in a remote Hawaiian atoll: social grouping and population structure. Behav Ecol 16:675–685. https://doi.org/10.1093/beheco/ari028
Kashiwagi T, Marshall AD, Bennett MB, Ovenden JR (2011) Habitat segregation and mosaic sympatry of the two species of manta ray in the Indian and Pacific oceans: Manta alfredi and M. birostris. Mar Biodivers Rec 4:e53. https://doi.org/10.1017/S1755267211000479
King SL, Janik VM (2015) Come dine with me: food-associated social signalling in wild bottlenose dolphins (Tursiops truncatus). Anim Cogn 18:969–974. https://doi.org/10.1007/s10071-015-0851-7
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford
Krause J, James R, Franks DW, Croft DP (eds) (2014) Animal social networks. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199679041.001.0001
Kurvers RH, Krause J, Croft DP, Wilson AD, Wolf M (2014) The evolutionary and ecological consequences of animal social networks: emerging issues. Trends Ecol Evol 29:326–335. https://doi.org/10.1016/j.tree.2014.04.002
Lachlan RF, Crooks L, Laland KN (1998) Who follows whom? Shoaling preferences and social learning of foraging information in guppies. Anim Behav 56:181–190. https://doi.org/10.1006/anbe.1998.0760
Lawson JM, Fordham SV, O’Malley MP, Davidson LN, Walls RH, Heupel MR, Ender I (2017) Sympathy for the devil: a conservation strategy for devil and manta rays. PeerJ 5:e3027. https://doi.org/10.7717/peerj.3027
Lewis SA, Setiasih N, Fahmi F, Dharmadi D, O’Malley MP, Campbell SJ, Yusuf M, Sianipar AB (2015) Assessing Indonesian manta and devil ray populations through historical landings and fishing community interviews. PeerJ PrePrints 3:e1642
Lisney TJ, Yopak KE, Montgomery JC, Collin SP (2008) Variation in brain organization and cerebellar foliation in chondrichthyans: batoids. Brain Behav Evol 72:262–282. https://doi.org/10.1159/000171489
Lusseau D, Schneider K, Boisseau OJ, Haase P, Slooten E, Dawson SM (2003) The bottlenose dolphin community of Doubtful Sound features a large proportion of long-lasting associations. Behav Ecol Sociobiol 54:396–405. https://doi.org/10.1007/s00265-003-0651-y
Lusseau D, Wilson BEN, Hammond PS, Grellier K, Durban JW, Parsons KM, Thompson PM (2006) Quantifying the influence of sociality on population structure in bottlenose dolphins. J Anim Ecol 75:14–24. https://doi.org/10.1111/j.1365-2656.2005.01013.x
Lusseau D, Whitehead H, Gero S (2008) Incorporating uncertainty into the study of animal social networks. Anim Behav 75:1809–1815. https://doi.org/10.1016/j.anbehav.2007.10.029
Marshall AD (2008) Biology and population ecology of Manta birostris in southern Mozambique. PhD thesis, The University of Queensland
Marshall AD, Bennett MB (2010) Reproductive ecology of the reef manta ray Manta alfredi in southern Mozambique. J Fish Biol 77:169–190. https://doi.org/10.1111/j.1095-8649.2010.02669.x
Marshall AD, Holmberg J (2019) MantaMatcher photo-identification library. Accessed January 21, 2019, from https://www.mantamatcher.org/
Marshall AD, Dudgeon CL, Bennett MB (2011) Size and structure of a photographically identified population of manta rays Manta alfredi in southern Mozambique. Mar Biol 158:1111–1124. https://doi.org/10.1007/s00227-011-1634-6
Marshall AD, Kashiwagi T, Bennett MB, Deakos M, Stevens G, McGregor F, Clark T, Ishihara H, Sato K (2018a) Mobula alfredi (amended version of 2011 assessment). The IUCN Red List of Threatened Species 2018:e.T195459A126665723, https://doi.org/10.2305/IUCN.UK.2011-2.RLTS.T195459A126665723.en
Marshall AD, Bennett MB, Kodja G, Hinojosa-Alvarez S, Galvan-Magana F, Harding M, Stevens G, Kashiwagi T (2018b) Mobula birostris (amended version of 2011 assessment). The IUCN Red List of Threatened Species 2018:e.T198921A126669349, http://www.iucnredlist.orq/details/198921/0
Martin RA (2007) A review of shark agonistic displays: comparison of display features and implications for shark–human interactions. Mar Freshw Behav Physiol 40:3–34. https://doi.org/10.1080/10236240601154872
Matich P, Heithaus MR (2015) Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia 178:347–359. https://doi.org/10.1007/s00442-015-3253-2
Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Anim Behav 83:389–401. https://doi.org/10.1016/j.anbehav.2011.11.008
Mourier J, Brown C, Planes S (2017) Learning and robustness to catch-and-release fishing in a shark social network. Biol Lett 13:20160824. https://doi.org/10.1098/rsbl.2016.0824
Newman MEJ (2006) Modularity and community structure in networks. Proc Nat Acad Sci 103 (23):8577-8582. https://doi.org/10.1073/pnas.0601602103
O’Malley MP, Lee-Brooks K, Medd HB (2013) The global economic impact of manta ray watching tourism. PLoS One 8:e65051. https://doi.org/10.1371/journal.pone.0065051
Opsahl T, Agneessens F, Skvoretz J (2010) Node centrality in weighted networks: generalizing degree and shortest paths. Soc Networks 32:245–251. https://doi.org/10.1016/j.socnet.2010.03.006
Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Phil Trans R Soc B, 361(1466), 235-259. https://doi.org/10.1098/rstb.2005.1785
Pierce SJ, Holmberg J, Kock AA, Marshall AD (2018) Photographic identification of sharks. In: Carrier JC, Heithaus MR, Simpfendorfer CA (eds) Shark research: emerging technologies and applications for the field and laboratory. CRC Press, Boca Raton, pp 219–234. https://doi.org/10.1201/b21842
Rohner CA, Flam AL, Pierce SJ, Marshall AD (2017) Steep declines in sightings of manta rays and devilrays (Mobulidae) in southern Mozambique (no. e3051v1). PeerJ Preprints 5:e3051v1. https://doi.org/10.7287/peerj.preprints.3051v1
Setyawan E, Sianipar AB, Erdmann MV, Fischer AM, Haddy JA, Beale CS, Lewis SA, Mambrasar R (2018) Site fidelity and movement patterns of reef manta rays (Mobula alfredi): Mobulidae using passive acoustic telemetry in northern Raja Ampat, Indonesia. Nat Conserv Res 3:1–15. https://doi.org/10.24189/ncr.2018.043
Shizuka D, Farine DR (2016) Measuring the robustness of network community structure using assortativity. Anim Behav 112:237–246. https://doi.org/10.1016/j.anbehav.2015.12.007
Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088. https://doi.org/10.1016/j.anbehav.2013.02.017
Sih A, Hanser SF, McHugh KA (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988. https://doi.org/10.1007/s00265-009-0725-6
Simcox H, Colegrave N, Heenan A, Howard C, Braithwaite VA (2005) Context-dependent male mating preferences for unfamiliar females. Anim Behav 70:1429–1437. https://doi.org/10.1016/j.anbehav.2005.04.003
Snijders L, Blumstein DT, Stanley CR, Franks DW (2017) Animal social network theory can help wildlife conservation. Trends Ecol Evol 32:567–577. https://doi.org/10.1016/j.tree.2017.05.005
Sperone E, Micarelli P, Andreotti S, Brandmayr P, Bernabò I, Brunelli E, Tripepi S (2012) Surface behaviour of bait-attracted white sharks at Dyer Island (South Africa). Mar Biol Res 8:982–991. https://doi.org/10.1080/17451000.2012.708043
Stevens G (2016) Conservation and population ecology of manta rays in the Maldives. PhD thesis, University of York
Stevens G, Hawkins JP, Roberts CM (2018) Courtship and mating behaviour of manta rays Mobula alfredi and M. birostris in the Maldives. J Fish Biol 93:344–359. https://doi.org/10.1111/jfb.13768
Stewart JD, Beale CS, Fernando D, Sianipar AB, Burton RS, Semmens BX, Aburto-Oropeza O (2016a) Spatial ecology and conservation of Manta birostris in the Indo-Pacific. Biol Conserv 200:178–183. https://doi.org/10.1016/j.biocon.2016.05.016
Stewart JD, Stevens GM, Marshall GJ, Abernathy K (2016b) Are mantas self aware or simply social? A response to Ari and D’Agostino 2016. J Ethol 35:145–147. https://doi.org/10.1007/s10164-016-0491-7
Stewart JD, Jaine FR, Armstrong AJ et al (2018) Research priorities to support effective manta and devil ray conservation. Front Mar Sci 5:314. https://doi.org/10.3389/fmars.2018.00314
Sumpter DJ (2006) The principles of collective animal behaviour. Philos Trans R Soc B 361:5–22. https://doi.org/10.1098/rstb.2005.1733
Sutherland WJ (1998) The importance of behavioural studies in conservation biology. Anim Behav 56:801–809. https://doi.org/10.1006/anbe.1998.0896
Swaney W, Kendal J, Capon H, Brown C, Laland KN (2001) Familiarity facilitates learning of foraging behaviour in the guppy. Anim Behav 62:591–598. https://doi.org/10.1006/anbe.2001.1788
Team RC (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Thonhauser KE, Gutnick T, Byrne RA, Kral K, Burghardt GM, Kuba MJ (2013) Social learning in cartilaginous fish (stingrays Potamotrygon falkneri). Anim Cogn 16:927–932. https://doi.org/10.1007/s10071-013-0625-z
Trivers RL (1971) The Evolution of Reciprocal Altruism. Quart Rev Biol 46 (1):35-57. https://doi.org/10.1086/406755
Venables S, McGregor F, Brain L, van Keulen M (2016a) Manta ray tourism management, precautionary strategies for a growing industry: a case study from the Ningaloo Marine Park, Western Australia. Pac Conserv Biol 22:295–300. https://doi.org/10.1071/PC16003
Venables S, Winstanley G, Bowles L, Marshall AD (2016b) A giant opportunity: the economic impact of manta rays on the Mozambican tourism industry - an incentive for increased management and protection. Tour Mar Environ 12:51–68. https://doi.org/10.3727/154427316X693225
Ward AJ, Herbert-Read JE, Sumpter DJ, Krause J (2011) Fast and accurate decisions through collective vigilance in fish shoals. Proc Natl Acad Sci U S A 108:2312–2315. https://doi.org/10.1073/pnas.1007102108
Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Adv Mar Biol 54:107–170
Wearmouth VJ, Southall EJ, Morritt D, Thompson RC, Cuthill IC, Partridge JC, Sims DW (2012) Year-round sexual harassment as a behavioral mediator of vertebrate population dynamics. Ecol Monogr 82:351–366. https://doi.org/10.1890/11-2052.1
Wetherbee BM, Cortés E, Bizzarro JJ (2004) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 225–246
Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208. https://doi.org/10.1093/beheco/6.2.199
Whitehead H (2007) Selection of models of lagged identification rates and lagged association rates using AIC and QAIC. Commun Stat Simulat 36:1233–1246. https://doi.org/10.1080/03610910701569531
Whitehead H (2008a) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago. https://doi.org/10.7208/chicago/9780226895246.001.0001
Whitehead H (2008b) Precision and power in the analysis of social structure using associations. Anim Behav 75:1093–1099. https://doi.org/10.1016/j.anbehav.2007.08.022
Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778. https://doi.org/10.1007/s00265-008-0697-y
Whitehead H, Dufault S (1999) Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. Adv Study Behav 28:33–74. https://doi.org/10.1016/S0065-3454(08)60215-6
Whitehead H, James R (2015) Generalized affiliation indices extract affiliations from social network data. Methods Ecol Evol 6:836–844. https://doi.org/10.1111/2041-210X.12383
Whitehead H, Rendell L (2004) Movements, habitat use and feeding success of cultural clans of South Pacific sperm whales. J Anim Ecol 73:190–196. https://doi.org/10.1111/j.1365-2656.2004.00798.x
Williams R, Lusseau D (2006) A killer whale social network is vulnerable to targeted removals. Biol Lett 2:497–500. https://doi.org/10.1098/rsbl.2006.0510
Wilson AD, Brownscombe JW, Krause J, Krause S, Gutowsky LF, Brooks EJ, Cooke SJ (2015) Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior. Behav Ecol 26:1577–1586. https://doi.org/10.1093/beheco/arv115
Wolf JB, Mawdsley D, Trillmich F, James R (2007) Social structure in a colonial mammal: unravelling hidden structural layers and their foundations by network analysis. Anim Behav 74:1293–1302. https://doi.org/10.1016/j.anbehav.2007.02.024
Yano K, Sato F & Takahashi T (1999) Observations of mating behavior of the manta ray, Manta birostris, at the Ogasawara Islands, Japan. Ich Res, 46(3), 289-296. https://doi.org/10.1007/BF02678515
Zanardo N, Parra GJ, Diaz-Aguirre F, Pratt EA, Möller LM (2018) Social cohesion and intra-population community structure in southern Australian bottlenose dolphins (Tursiops sp.). Behav Ecol Sociobiol 72:156. https://doi.org/10.1007/s00265-018-2557-8
Acknowledgments
We would like to thank Papua Explorers Dive Resort, Raja Ampat SEA Centre, University of Papua, Barefoot Conservation, and KemenRisTek-Dikti for their invaluable support in enabling our fieldwork in Raja Ampat. We are grateful to all citizen scientists, recreational divers, and photographers who have submitted photographs and videos to MantaMatcher.org. Thanks to E. Germanov, E. Sinderson, G. Winstanley, and J. Holmberg for support with MantaUtil and MantaMatcher and E. Germanov for help with illustrations. We would also like to thank D. Jacoby and one anonymous reviewer for their helpful comments.
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No external funding was received for this research. Research was funded by the authors with some funds sourced via donations to Marine Megafauna Foundation and through RJYP student research budget at Macquarie University (during 2017–2018).
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RJYP was the primary author of the manuscript. RJYP and DWF conceived the central idea of the manuscript. RJYP, SKV, ADM, and RFT collected and input data. RJYP conducted all statistical analyses with input from DWF and CB, ADM, and SKV contributed to editing and manuscript revisions.
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All applicable international, national, and institutional guidelines for conducting research on animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the corresponding author is based.
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Perryman, R.J.Y., Venables, S.K., Tapilatu, R.F. et al. Social preferences and network structure in a population of reef manta rays. Behav Ecol Sociobiol 73, 114 (2019). https://doi.org/10.1007/s00265-019-2720-x
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DOI: https://doi.org/10.1007/s00265-019-2720-x