Skip to main content
Log in

The reproductive ecology of resident manta rays (Manta alfredi) off Maui, Hawaii, with an emphasis on body size

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

In resident manta rays (Manta alfredi) off Maui, sexual maturity appears delayed until growth exceeds 90% of maximum size, an indicator that large body size provides a reproductive advantage at the expense of a shorter reproductive time period. In this study, 286 surveys were conducted between 2005 and 2010 using photo-identification and photogrammetry to study the reproductive ecology of a resident population of manta rays off Maui, Hawaii, and investigate the reproductive benefits of large body size in each sex. Although reproductive activities occurred year-round, mating trains and late-term pregnant females were significantly more likely to be observed during the winter months. Some females were pursued by males during both winter and summer of the same year, suggesting multiple ovulations may be possible in a single year. Males likely detect a female’s reproductive state by positioning directly behind her, or passing through her bodily excretions. The mean pregnancy rate was estimated at 0.56 pregnancies/adult female/year with larger females pregnant more often, and more likely in consecutive years. The operational sex ratio was heavily skewed with 2.68 adult males per reproductively available female. Although males appear to compete with one another for females within a mating train, no direct physical competition was ever observed between males. Evidence of highly dynamic mating trains lasting more than one day suggests endurance rivalry may be the primary mating strategy among males, during which larger males may benefit from greater energy reserves. The study area appears to be an important staging area for mating individuals in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andersson M (1994) Sexual Selection. Princeton University Press, Princeton

    Google Scholar 

  • Andersson M, Iwasa Y (1996) Sexual selection. Trends Ecol Evol 11(2):53–58

    Article  PubMed  CAS  Google Scholar 

  • Ari C, Correia J (2008) Role of sensory cues on food searching behavior of a captive Manta birostris (Chondrichtyes, Mobulidae). Zoo Biol 27(4)

  • Baker C, Herman L (1984) Aggressive behavior between humpback whales (Megaptera novaeangliae) wintering in Hawaiian waters. Can J Zool 62(10):1922–1937

    Article  Google Scholar 

  • Bercovitch F (1989) Body size, sperm competition, and determinants of reproductive success in male savanna baboons. Evolution 43(7):1507–1521

    Article  Google Scholar 

  • Berglund A (1994) The operational sex ratio influences choosiness in a pipefish. Behav Ecol 5(3):254

    Article  Google Scholar 

  • Bigelow H, Schroeder WC (1953) Fishes of the western North Atlantic. Sawfishes, guitarfishes, skates, rays, and chimaeroids. Mem Sears Found Mar Res 1:500–514

    Google Scholar 

  • Birkhead T, Briskie J, Miller A (1993) Male sperm reserves and copulation frequency in birds. Behav Ecol Sociobiol 32(2):85–93

    Article  Google Scholar 

  • Braccini JM, Gillanders BM, Walker TI (2006) Determining reproductive parameters for population assessments of chondrichthyan species with asynchronous ovulation and parturition: piked spurdog (Squalus megalops) as a case study. Mar Freshw Res 57(1):105–119

    Article  Google Scholar 

  • Brownell RL, Balls K (1986) Potential for sperm competition in baleen whales. Report for the International Whaling Commmission 8 (Special issue):97 – 112

  • Carrier J, Pratt Jr H, Martin L (1994) Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum. Copeia:646–656

  • Clark TB (2001) Population Structure of Manta birostris (Chondrichthyes: mobulidae) from the Pacific and Atlantic Oceans. MS thesis, Texas A&M University, Galveston, Texas

  • Clutton-Brock T, Guinness F, Albon S (1982) Behaviour and ecology of two sexes. Edinburgh University Press, Edinburgh

    Google Scholar 

  • Clutton-Brock T, Vincent A (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351(6321):58–60

    Article  PubMed  CAS  Google Scholar 

  • Compagno L, Last P (1999) Mobulidae. In: Carpenter KE, Niem VH (eds) FAO species identification guide for fishery purposes. The living marine resources of the western Central Pacific., vol 3. Batoid Fishes, Chimaeras and Bony Fishes. Part 1 (Elopidae to Linophyrnidae). FAO, Rome,

  • Coté I (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol 38:311–355

    Google Scholar 

  • Cox C, Le Boeuf B (1977) Female incitation of male competition: a mechanism in sexual selection. Am Nat 111(978):317–335

    Article  Google Scholar 

  • Deakos M (2010) Paired-laser photogrammetry as a simple and accurate system for measuring the body size of free-ranging manta rays Manta alfredi. Aquat Biol 10(1):1–10. doi:10.3354/ab00258

    Article  Google Scholar 

  • Deakos M, Baker J, 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

    Article  Google Scholar 

  • 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(2):121–133

    Article  Google Scholar 

  • Emlen S (1976) Lek organization and mating strategies in the bullfrog. Behav Ecol Sociobiol 1(3):283–313

    Article  Google Scholar 

  • Emlen S, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197(4300):215–223

    Article  PubMed  CAS  Google Scholar 

  • Fisher R (1930) The genetical theory of natural selection. Clarendon, Oxford

    Google Scholar 

  • Gomendio M, Harcourt AH, Roldan ERS (1998) Sperm competition in mammals. In: Birkhead TH, Moller AP (eds) Sperm competition and sexual selection. pp 467–755

  • Gordon I (1993) Pre-copulatory behaviour of captive sandtiger sharks, Carcharias taurus. Environ Biol Fishes 38(1):159–164

    Article  Google Scholar 

  • Hamlett W, Koob T (1999) Female reproductive system. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. The John Hopkins University Press, Baltimore, pp 398–443

    Google Scholar 

  • Harvey P, Harcourt A (1984) Sperm competition, testes size, and breeding systems in primates. Sperm competition and the evolution of animal mating systems 18:589–600

    Google Scholar 

  • Herman E, Herman L, Pack A, Marshall G, Shepard M, Bakhtiari M (2007) When whales collide: crittercam offers insight into the competitive behavior of humpback whales on their hawaiian wintering grounds. Mar Technol Soc J 41(4):35–43

    Article  Google Scholar 

  • Hodgson E, Mathewson R (1978) Sensory biology of sharks, skates, and rays. Office of Naval Research, Dept. of the Navy: for sale by the Supt. of Docs., US Govt. Print. Off.,

  • Höglund J, Montgomerie R, Widemo F (1993) Costs and consequences of variation in the size of ruff leks. Behav Ecol Sociobiol 32(1):31–39

    Article  Google Scholar 

  • Homma K, Maruyama T, Itoh T, Ishihara H, Uchida S (1999) Biology of the manta ray, Manta birostris Walbaum, in the Indo-Pacific. In: Seret B, Sire JY (eds) Indo-Pacific fish biology: proceedings of the fifth international conference on Indo-Pacific fishes, Noumea, 1997, France, 1999. Ichthyological Society of France, pp 209–216

  • Johnson R, Nelson D (1978) Copulation and possible olfaction-mediated pair formation in two species of carcharhinid sharks. Copeia 1978(3):539–542

    Article  Google Scholar 

  • Kitchen-Wheeler A (2010) Visual identification of individual manta ray (Manta alfredi) in the Maldives Islands, Western Indian Ocean. Mar Biol Res 6(4):351–363

    Article  Google Scholar 

  • Kleerekoper H (1978) Chemoreception and its interaction with flow and light perception in the locomotion and orientation of some elasmobranchs. Sensory Biology of Sharks, Skates and Rays:269–329

  • Losey G Jr (1972) The ecological importance of cleaning symbiosis. Copeia 1972(4):820–833

    Article  Google Scholar 

  • Madsen T, Shine R (1993) Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes. Am Nat 141(1):167–171

    Article  PubMed  CAS  Google Scholar 

  • Marshall A, Bennett M (2010) Reproductive ecology of the reef manta ray Manta alfredi in southern Mozambique. J Fish Biol 77(1):169–190

    Article  PubMed  CAS  Google Scholar 

  • Marshall A, Compagno L, Bennett M (2009) Redescription of the genus Manta with resurrection of Manta alfredi (Krefft,1868) (Chondrichthyes; Myliobatoidei; Mobulidae). Zootaxa 2301:1–28

    Google Scholar 

  • Marshall AD (2009) Biology and population ecology of Manta birostris in southern Mozambique. PhD Thesis, University of Queensland,

  • Marshall AD, Pierce SJ, Bennett MB (2008) Morphological measurements of manta rays (Manta birostris) with a description of a foetus from the east coast of Southern Africa. Zootaxa 1717:24–30

    Google Scholar 

  • Marshall L, White W, Potter I (2007) Reproductive biology and diet of the southern fiddler ray, Trygonorrhina fasciata (Batoidea: Rhinobatidae), an important trawl bycatch species. Mar Freshw Res 58(1):104–115

    Article  Google Scholar 

  • Okinawa Churaumi Aquarium (2010). We have just recently had our 4th successful manta ray (Manta birostris) birth in captivity at Okinawa Churaumi Aquarium. News Release 6 July 2010. http://okichuraumi.jp/info/ennews/archives/1341. Accessed 31 August 2011

  • Pack A, Herman L, Spitz S, Hakala S, Deakos M, Herman E (2009) Male humpback whales in the Hawaiian breeding grounds preferentially associate with larger females. Anim Behav 77(3):653–662

    Article  Google Scholar 

  • Parker G (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Pratt H, Carrier J (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fishes 60(1):157–188

    Article  Google Scholar 

  • Ralls K, Mesnick S (2002) In: Perrin W, Würsig B, Thewissen J (eds) Sexual dimorphism. Encyclopedia of Marine Mammals Academic Press, San Diego, pp 1071–1078

    Google Scholar 

  • Rubin RD (2002) Manta Rays: not all black and white. Shark Focus 15:4–5

    Google Scholar 

  • Shine R (1988) The evolution of large body size in females: a critique of Darwin’s “fecundity advantage” model. Am Nat 131(1):124–131

    Article  Google Scholar 

  • Spitz S, Herman L, Pack A, Deakos M (2002) The relation of body size of male humpback whales to their social roles on the Hawaiian winter grounds. Can J Zool 80(11):1938–1947

    Article  Google Scholar 

  • SPSS, Inc. (2007) SPSS statistics base 17.0 user’s guide. SPSS Inc., Chicago

    Google Scholar 

  • Tricas T (1980) Courtship and mating-related behaviors in myliobatid rays. Copeia, 553–556.

  • Trivers R (1972) Parental investment and sexual selection. Sexual selection and the descent of man: the Darwinian pivot:136

  • Tyack P, Whitehead H (1982) Male competition in large groups of wintering humpback whales. Behaviour 83(1):132–154

    Article  Google Scholar 

  • Uchida S, Toda M, Matsumoto Y (2008) Captive Records of Manta Rays in Okinawa Churaumi Aquarium Paper presented at the 2008 Joint Meeting of Ichthyologists and Herpetologists. Montreal, Canada

    Google Scholar 

  • White WT, Giles J, Dharmadi PIC (2006) Data on the bycatch fishery and reproductive biology of mobulid rays (Myliobatiformes) in Indonesia. Fish Res 82(1–3):65–73

    Article  Google Scholar 

  • Whitney NM, Pratt Jr HL, Carrier JC (2004) Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Animal Behaviour 68(6): 1435-1442

    Google Scholar 

  • Wolff J (1998) Breeding strategies, mate choice, and reproductive success in American bison. Oikos 83(3):529–544

    Article  Google Scholar 

  • Yano K, Sato F, Takahashi T (1999) Observations of mating behavior of the manta ray, Manta birostris, at the Ogasawara Islands, Japan. Ichthyol Res 46(3):289–296

    Article  Google Scholar 

Download references

Acknowledgments

J. Whitney, A. Ligon, R. Deakos, and E. Lyman provided valuable support with ongoing data collection. I wish to thank R. Deakos, S. Spitz, and B. Brainstetter for their assistance with paired-laser photogrammetry calibrations. L. Herman, S. Yin, S. Spitz, A. Pack, J. Mobley, K. Minke, and P. Couvillon provided valuable feedback on earlier versions of this manuscript. My sincere gratitude goes to G.S. Mills for his guidance and support aboard the Oscar Elton Sette. For assistance with animal care permit issuance, I wish to thank J. Mobley. Research was conducted under the University of Hawaii Animal Care & Use Committee, Protocol No. 08-591-2, and Assurance number A3423-01.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark H. Deakos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Deakos, M.H. The reproductive ecology of resident manta rays (Manta alfredi) off Maui, Hawaii, with an emphasis on body size. Environ Biol Fish 94, 443–456 (2012). https://doi.org/10.1007/s10641-011-9953-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-011-9953-5

Keywords

Navigation