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Same-sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid)

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Abstract

Dosidicus gigas (the Humboldt squid) is a widely distributed and ecologically important predator in the eastern Pacific Ocean, but its mating behaviour is poorly understood. Individuals of this species have undergone a drastic change in size at maturity in the last years. We investigated mating activity of Humboldt squid in the Gulf of California in 2013, 2014, and 2015 by quantifying spermatangia deposited in the tissue of the buccal area. In 2015, we encountered the smallest mean mantle length of mature specimens recorded to date in the Gulf of California. In all years, numerous males were encountered that had been mated by other males. Spermatangia in males were deposited on the tissue in similar numbers and in the same location as normally occurs in females (the buccal area), suggesting that male-to-male mating behaviour is similar to male-to-female. This behaviour is referred to as same-sex sexual behaviour and has been described for various taxa, including other cephalopods. Overall similarity in mating frequency between males and females and in body size of mated individuals (in 2015) suggests non-discriminative and brief encounters with body size being a cue for mating. This mating strategy may be beneficial for males, as Humboldt squid live in groups where competition for mates is likely high. The energetic costs of male-to-male mating events may be counterbalanced by the fitness profits of indiscriminate mating behaviour.

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References

  • Arkhipkin A, Argüelles J, Shcherbich Z, Yamashiro C (2015) Ambient temperature influences adult size and life span in jumbo squid (Dosidicus gigas). Can J Fish Aquat Sci 743:400–409

    Article  Google Scholar 

  • Bailey NW, Zuk M (2009) Same-sex sexual behavior and evolution. Trends Ecol Evol 24(8):439–446

    Article  Google Scholar 

  • Boal JG (2006) Social recognition: a top down view of cephalopod behaviour. Vie et Milieu 56(2):69–80

    Google Scholar 

  • Boyle PR, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Science Ltd, Oxford

    Book  Google Scholar 

  • DeMartini DG, Ghoshal A, Pandolfi E, Weaver AT, Baum M, Morse DE (2013) Dynamic biophotonics: female squid exhibit sexually dimorphic tunable leucophores and iridocytes. J Exp Biol 216:3733–3741

    Article  CAS  Google Scholar 

  • Drew GA (1919) Sexual activities of the squid Loligo pealii (Les.) II. The spermatophore; its structure, ejaculation and formation. J Morphol 32:379–435

    Article  Google Scholar 

  • Fernández-Álvarez FÁ, Villanueva R, Hoving HJT, Gilly WF (2018) The journey of squid sperm. Rev Fish Biol Fish 28:191–199

    Article  Google Scholar 

  • Fiorito G, Affuso A, Basil J, Cole A, De Girolamo P, D’Angelo L, Dickel L, Gestal C, Grasso F, Kuba M, Mark F, Melillo D, Osorio D, Perkins K, Ponte G, Shashar N, Smith D, Smith J, Andrews PL (2015) Guidelines for the care and welfare of cephalopods in research: a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab Anim 49:1–90

    Article  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion

  • Franklin AM, Stuart-Fox D (2017) Single and multiple mating reduces longevity of female dumpling squid (Euprymna tasmanica). J Evol Biol 30:977–984

    Article  CAS  Google Scholar 

  • Franklin AM, Squires ZE, Stuart-Fox D (2012) The energetic cost of mating in a promiscuous cephalopod. Biol Lett 8:754–756

    Article  Google Scholar 

  • Gilly WF, Elliger CA, Salinas-Zavala CA, Camarillo-Coop S, Bazzino G, Beman M (2006) Spawning by jumbo squid Dosidicus gigas in the San Pedro Mártir Basin, Gulf of California, Mexico. Mar Ecol Prog Ser 313:125–133

    Article  Google Scholar 

  • Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545

    Article  Google Scholar 

  • Hanlon RT, Forsythe JW (2008) Sexual cannibalism by Octopus cyanea on a Pacific coral reef. Mar Freshw Behav Physiol 41:19–28

    Article  Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod Behavior. Cambridge University Press

  • Hanlon RT, Smale MJ, Sauer WHH (2002) The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bull Mar Sci 71:331–345

    Google Scholar 

  • Hoving HJT, Laptikhovsky VV (2007) Getting under the skin: autonomous implantation of squid spermatophores. Biol Bull 212:177–179

    Article  CAS  Google Scholar 

  • Hoving HJT, Robison BH (2016) Deep-sea in situ observations of gonatid squid and their prey reveal high occurrence of cannibalism. Deep Sea Res Part I Oceanogr Res Pap 116:94–98

    Article  Google Scholar 

  • Hoving HJT, Roeleveld MAC, Lipinski MR, Melo Y (2004) Reproductive system of the giant squid Architeuthis in South African waters. J Zool 264:153–169

    Article  Google Scholar 

  • Hoving HJT, Bush SL, Robison BH (2012) A shot in the dark: same-sex sexual behaviour in a deep-sea squid. Biol Lett 8:287–290

    Article  Google Scholar 

  • Hoving HJT, Gilly WF, Markaida U, Benoit-Bird KJ, West-Brown Z, Daniel P, Field J, Paressenti L, Liu B, Campos B (2013) Extreme plasticity in life history strategy allows a migratory predator (jumbo squid) to cope with a changing climate. Glob Change Biol 19(7):2089–2103

    Article  Google Scholar 

  • Hoving HJT, Laptikhovsky VV, Robison BH (2015) Vampire squid’s reproductive strategy is unique among coleoid cephalopods. Biology 25(8):322–323

    Google Scholar 

  • Lipinski MR, Underhill LG (1995) Sexual maturation in squid: quantum or continuum? S Afr J Mar Sci 15:207–223

    Article  Google Scholar 

  • Lordan C, Casey J (1997) The first record of ‘accidental’ copulation between male squid of the genus Illex. J Molluscan Stud 63:556–558

    Article  Google Scholar 

  • Lutz RA, Voight JR (1994) Close encounter in the deep. Nature 371:563

    Article  CAS  Google Scholar 

  • Marian JEAR (2015) Evolution of spermatophore transfer mechanisms in cephalopods. J Nat Hist 49:1423–1455

    Article  Google Scholar 

  • Markaida U, Gilly WF (2016) Cephalopods of Pacific Latin America. Fish Res 173:113–121

    Article  Google Scholar 

  • Markaida U, Sosa-Nishizaki O (2003) Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. J Mar Biol Assoc UK 83:507–522

    Article  Google Scholar 

  • Moltschaniwskyj NA, Hall K, Lipinski MR, Marian JEAR, Nishiguchi M, Sakai M, Shulman DJ, Sinclair B, Sinn DL, Staudinger M, Van Gelderen R, Villanueva R, Warnke K (2007) Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 17(2–3):455–476

    Article  Google Scholar 

  • Morse P, Huffard CL, Meekan MG, McCormick MI, Zenger KR (2018) Mating behaviour and postcopulatory fertilization patterns in the southern blue-ringed octopus, Hapalochlaena maculosa. Anim Behav 136:41–51

    Article  Google Scholar 

  • Nesis KN, Nigmatullin ChM, Nikitina IV (1998) Spent females of deepwater squid Galiteuthis glacialis under the ice at the surface of the Weddell Sea (Antarctic). J Zool Lond 244:185–200

    Article  Google Scholar 

  • Nigmatullin ChM, Arkhipkin AI, Sabirov RM (1995) Age, growth and reproductive biology of diamond-shaped squid Thysanoteuthis rhombus (Oegopsida: Thysanoteuthidae). Mar Ecol Prog Ser 124:73–87

    Article  Google Scholar 

  • Nigmatullin CM, Nesis KN, Arkhipkin AI (2001) A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fish Res 54:9–19

    Article  Google Scholar 

  • Robinson CJ, Gomez-Gutierrez J, Markaida U, Gilly WF (2016) Prolonged decline of jumbo squid (Dosidicus gigas) landings in the Gulf of California is associated with chronically low wind stress and decreased chlorophyll a after El Nino 2009–2010. Fish Res 173:128–138

    Article  Google Scholar 

  • Rosen H, Gilly WF, Bell L, Abernathy K, Marshall G (2015) Chromogenic behaviors of the Humboldt squid (Dosidicus gigas) studied in situ with an animal-borne video package. J Exp Biol 218:265–275

    Article  Google Scholar 

  • Sato N, Kasugai T, Ikeda Y, Munehara H (2010) Structure of the seminal receptacle and sperm storage in the Japanese pygmy squid. J Zool 282(3):151–156

    Article  Google Scholar 

  • Sato N, Kasugai T, Munehara H (2014) Spermatangium formation and sperm discharge in the Japanese pygmy squid Idiosepius paradoxus. Zoology 117:192–199

    Article  Google Scholar 

  • Sato N, Yoshida M, Kasugai T (2017) Impact of cryptic female choice on insemination success: larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia. Evolution 71(1):111–120

    Article  Google Scholar 

  • Scharf I, Martin OY (2013) Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences. Behav Ecol Sociobiol 67:1719

    Article  Google Scholar 

  • Squires ZE, Wong BBM, Norman MD, Stuart-Fox D (2014) Multiple paternity but no evidence of biased sperm use in female dumpling squid Euprymna tasmanica. Mar Ecol Prog Ser 511:93–103

    Article  Google Scholar 

  • Squires ZE, Wong BBM, Norman MD, Stuart-Fox D (2015) Last male sperm precedence in a polygamous squid. Biol J Lin Soc 116:277–287

    Article  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Van Voorhies WA (1992) Production of sperm reduces nematode lifespan. Nature 360:456

    Article  Google Scholar 

  • Wada T, Takegaki T, Mori T, Natsukari Y (2005) Sperm displacement behaviour of the cuttlefish Sepia esculenta (Cephalopoda: Sepiidae). J Ethol 23:85–92

    Article  Google Scholar 

  • Wormuth JH (1976) The biogeography and numerical taxonomy of the oegopsid squid family Ommastrephidae in the Pacific Ocean. Bull Scripps Inst Oceanogr 23:1–90

    Google Scholar 

  • Ylitalo et al (2018) Who’s your daddy? A behavioral and genetic study of multiple paternity in a polygamous marine invertebrate, Octopus oliveri. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.27309v1

    Article  Google Scholar 

Download references

Acknowledgements

HJTH was funded by a Grant (CP1218) of the Cluster of Excellence 80 “The Future Ocean.” “The Future Ocean” is funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments. FAFA was supported by Grants (BES-2013-063551 and EEBB-I- 15-09631) from the Spanish Ministry of Economy and Competitiveness (MINECO). WG acknowledges support from Stanford University and by Grants from the US National Science Foundation (IOS-1557754, OCE-1338973 RAPID, IOS-142093 EAGER, OCE 0850839), the National Geographic Committee for Research and Exploration (7578-04 and 9366-13), and Lindblad Expeditions-National Geographic Fund (LXII-15). EP was supported in part by the National Science Foundation Graduate Research Fellowship Program under Grant no. DGE-114747. We thank Karmina Arroyo-Ramírez, Diana Li, Carlos Zayas Santiago, and Patrick Daniel for support in the field and the SURMAR program of the Ocean Foundation for use of laboratory facilities in Santa Rosalía.

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Correspondence to Henk-Jan T. Hoving.

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The datasets generated and/or analysed during the current study are available as electronic supplemental material (ESM) and will be available in the Pangaea repository.

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In 2013 and 2014, we obtained dead squid from fishermen. The specimens that were captured by our own jigging efforts in 2015 were killed using methods that are in line with current international standards for cephalopod care and welfare reviewed by Fiorito et al. (2015).

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Hoving, HJ.T., Fernández-Álvarez, F.Á., Portner, E.J. et al. Same-sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid). Mar Biol 166, 33 (2019). https://doi.org/10.1007/s00227-019-3476-6

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