Skip to main content
SpringerLink
Log in

The journey of squid sperm

  • Research Paper
  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

Abstract

Sperm storage is common in internally fertilizing animals, but is also present in several external fertilizers, such as many cephalopods. Cephalopod males attach sperm packets (spermatangia) to female conspecifics during mating. Females of eight externally fertilizing families comprising 25% of cephalopod biodiversity have sperm-storage organs (seminal receptacles) in their buccal area, which are not in direct physical contact with the deposited spermatangia. The mechanism of sperm transmission between the implantation site and the storage organ has remained a major mystery in cephalopod reproductive biology. Here, jumbo squid females covering almost the entire life cycle, from immature to a laboratory spawned female, were used to describe the internal structure of the seminal receptacles and the process of sperm storage. Seminal fluid was present between the spermatangia and seminal receptacles, but absent in regions devoid of seminal receptacles. The sperm cellular component was formed by spermatozoa and round cells. Although spermatozoa were tracked over the buccal membrane of the females to the inner chambers of the seminal receptacles, round cells were not found inside the seminal receptacles, suggesting that spermatozoa are not sucked up by the muscular action of the seminal receptacles. This finding supports the hypothesis that spermatozoa are able to actively migrate over the female skin. Although further experimental support is needed to fully confirm this hypothesis, our findings shed light on the elusive process of sperm storage in many cephalopods, a process that is fundamental for understanding sexual selection in the sea.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aiken DE, Waddy SL, Mercer SM (2004) Confirmation of external fertilization in the American lobster, Homarus americanus. J Crustacean Biol 24(3):474–480. doi:10.1651/C-2454

    Article  Google Scholar 

  • Beninger PG, Valdizan A, Le Pennec G (2016) The seminal receptacle and implications for reproductive processes inthe invasive gastropod Crepidula fornicata. Zool 119:4–10. doi:10.1016/j.zool.2015.09.001

    Article  Google Scholar 

  • Birk MA, Paight C, Seibel BA (2016) Observations of multiple pelagic egg masses from small-sized jumbo squid (Dosidicus gigas) in the Gulf of California. J Nat Hist. doi:10.1080/00222933.2016.1209248

    Google Scholar 

  • Bush SL, Hoving HJT, Huffard CL, Robison BH, Zeidberg LD (2012) Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). J Mar Biol Assoc UK 92:1629–1636. doi:10.1017/S0025315411002165

    Article  Google Scholar 

  • Fernández-Álvarez FA, Li DH, Portner E, Villanueva R, Gilly WE (2017) Morphological description of egg masses and hatchlings of Lolliguncula diomedeae (Cephalopoda: Loliginidae). J Molluscan Stud 83:194–199. doi:10.1093/mollus/eyx008

    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. doi:10.1177/0023677215580006

    Article  PubMed  Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, New York

    Google Scholar 

  • Hirohashi N et al (2013) Sperm from sneaker male squids exhibit chemotactic swarming to CO2. Curr Biol 23:775–781. doi:10.1016/j.cub.2013.03.040

    Article  CAS  PubMed  Google Scholar 

  • Hirohashi N, Iida T, Sato N, Warwick SHH, Iwata Y (2016) Complex adaptive traits between mating behavior and post-copulatory sperm behaviour in squids. Rev Fish Biol Fish 26:601–607. doi:10.1007/s11160-016-9434-1

    Article  Google Scholar 

  • Hoving H-JT et al. (2014) In: Erica AGV (ed) Advances in marine biology, vol 67. Academic Press, Cambridge, pp 235–359. doi:10.1016/B978-0-12-800287-2.00003-2

  • Jereb P, Roper CFE (2010) Cephalopods of the world. An annotated and illustrated catalogue of species known to date, vol 2. Myopsid and Oegopsid Squids. FAO species catalogue for fishery purposes, no. 4, vol 2. FAO, Rome

  • Johanisson E, Campana A, Luthi R, de Agostini A (2000) Evaluation of ‘round cells’ in semen analysis: a comparative study. Hum Reprod Update 6:404–412

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Marian JEAR (2015) Evolution of spermatophore transfer mechanisms in cephalopods. J Nat Hist 49:1423–1455. doi:10.1080/00222933.2013.825026

    Article  Google Scholar 

  • Markaida U, Gilly WF (2016) Cephalopods of Pacific Latin America. Fish Res 173:113–121. doi:10.1016/j.fishres.2015.09.014

    Article  Google Scholar 

  • Moltschaniwskyj NA et al (2007) Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 17:455–476. doi:10.1007/s11160-007-9056-8

    Article  Google Scholar 

  • Naud MJ, Havenhand JN (2006) Sperm motility and longevity in the giant cuttlefish, Sepia apama (Mollusca: Cephalopoda). Mar Biol 148:559–566. doi:10.1007/s00227-005-0109-z

    Article  Google Scholar 

  • Naud MJ, Shaw PW, Hanlon RT, Havenhand JN (2005) Evidence for biased use of sperm sources in wild female giant cuttlefish (Sepia apama). Proc R Soc Lond B Biol Sci 272:1047–1051. doi:10.1098/rspb.2004.3031

    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 

  • Orr TJ, Brennan PLR (2015) Sperm storage: distinguishing selective processes and evaluating criteria. Trends Ecol Evol 30:261–272. doi:10.1016/j.tree.2015.03.006

    Article  PubMed  Google Scholar 

  • Pantin CFA (1968) Técnicas microscópicas para zoólogos. Editorial Academia León, León

    Google Scholar 

  • Pascini TV, Martins GF (2017) The insect spermatheca: an overview. Zool 121:56–71. doi:10.1016/j.zool.2016.12.001

    Article  Google Scholar 

  • Reeve MR, Walter MA (1972) Observations and experiments on methods of fertilization in the chaetognath Sagitta hispida. Biol Bull 143:207–214

    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 282:151–156. doi:10.1111/j.1469-7998.2010.00733.x

    Article  Google Scholar 

  • Sato N, Kasugai T, Munehara H (2013) Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid. Mar Biol 160:553–561. doi:10.1007/s00227-012-2112-5

    Article  Google Scholar 

  • Sato N, Yoshida MA, 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 71:111–120. doi:10.1111/evo.13149

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Staaf DJ, Camarillo-Coop S, Haddock SHD, Nyack AC, Payne J, Salinas-Zavala CA, Seibel BA, Trueblood L, Widmer C, Gilly WF (2008) Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae. J Mar Biol Assoc UK 88:759–770. doi:10.1017/S0025315408001422

    Article  Google Scholar 

  • Tinbergen L (1939) Zur Fortpflanzungsethologie von Sepia officinalis L. Archs Neerl Zool 3:323–364

    Article  Google Scholar 

  • van Oordt GJ (1938) The spermatheca of Loligo vulgaris. I. Structure of the spermatheca and function of its unicellular glands. Q J Microsc Sci 80:593–599

    Google Scholar 

  • Villanueva R et al (2012) A laboratory guide to in vitro fertilization of oceanic squids. Aquaculture 342–343:125–133. doi:10.1016/j.aquaculture.2012.02.025

    Article  Google Scholar 

  • Waddy SL, Aiken DE (1986) Multiple fertilization and consecutive spawning in large American lobsters, Homarus americanus. Can J Fish Aquat Sci 43:2291–2294

    Article  Google Scholar 

  • Wegener BJ, Stuart-Fox D, Norman MD, Wong BBM (2013) Spermatophore consumption in a cephalopod. Biol Lett 9:20130192. doi:10.1098/rsbl.2013.0192

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Diana H. Li, Hannah Rosen, Elan Portner, Patrick C. Daniel and Timothy H. Frawley for their valuable help in the collection of jumbo squids. Thanks to Mr. J. M. Fortuño (Electron Microscopy Service, ICM) for his dedication and kindness during the SEM sessions and Mr. J. M. Anguita (ICM) for the elaboration of Fig. 2a. We thank the editor and two anonymous reviewers for their helpful comments. This study was funded by the research project CALOCEAN-2 (AGL2012-39077) from the Ministry of Economy and Competitiveness (MINECO) of Spain. FAFA was supported by two Grants (BES-2013-063551 and EEBB-I-15-09631) from MINECO. HJTH was financed by a Grant (CP1218) of the Cluster of Excellence 80 “The Future Ocean”, funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments. Support from Grants OCE-1338973 RAPID, IOS-142093 EAGER, OCE 0850839 and IOS-1557754 (US National Science Foundation), and N000140911054 (US Office of Naval Research) is also acknowledged.

Author contributions

FAFA, RV, HJTH and WFG conceived the study. FAFA and WFG performed the samplings. FAFA performed the histology and SEM observations. All authors contributed to the interpretation of the material, the writing of the manuscript, and its revision, and approved its final version. All the authors agree to be accountable for the content.

Author information

Authors and Affiliations

  1. Institut de Ciències del Mar (CSIC), Passeig Maritim 37-49, 08003, Barcelona, Spain

    Fernando Á. Fernández-Álvarez & Roger Villanueva

  2. Hopkins Marine Station, Department of Biological Sciences, Stanford University, Pacific Grove, CA, 93950, USA

    Fernando Á. Fernández-Álvarez & William F. Gilly

  3. GEOMAR, Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Henk-Jan T. Hoving

Authors
  1. Fernando Á. Fernández-Álvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roger Villanueva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henk-Jan T. Hoving
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William F. Gilly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando Á. Fernández-Álvarez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

Laboratory protocols and experimental conditions were in line with current international standards for cephalopod care and welfare reviewed by Fiorito et al. (2015).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernández-Álvarez, F.Á., Villanueva, R., Hoving, HJ.T. et al. The journey of squid sperm. Rev Fish Biol Fisheries 28, 191–199 (2018). https://doi.org/10.1007/s11160-017-9498-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11160-017-9498-6

Keywords

Search

Navigation