Marine Biology

, 166:146 | Cite as

Role of gamete limitation in the occurrence of ‘abnormal early clutches’ on female American lobster, Homarus americanus, in eastern Canada

  • Feng TangEmail author
  • Bernard Sainte-Marie
  • Julien Gaudette
  • Rémy Rochette
Original Paper


A large-scale survey in 2011–2014 found that ovigerous female American lobsters, Homarus americanus, carrying “abnormal” early clutches (< 50% of abdomen covered by eggs) were ubiquitous in eastern Canada. This could be caused by reduced production of oocytes, or insufficient sperm to fertilize all oocytes produced. To address the oocyte limitation hypothesis, ovarian fecundity was assessed in 343 pre-spawn females and clutch fecundity in 169 post-spawn females sampled from ten sites across eastern Canada in May and June 2014. All females produced and spawned enough oocytes to form a full clutch, thus invalidating the oocyte limitation hypothesis. To address the sperm limitation hypothesis, the prevalence of different “types” of sperm plug in the seminal receptacle of 1735 wild-mated, pre-spawn or ovigerous females was surveyed in July–August 2014 and 2015, and the effect of sperm plug type on fecundity/fertility was examined in 60 wild-mated, laboratory-spawning females beginning in July 2014. Among the pre-spawn wild-mated females, 88.3% had a hard plug, 5.9% a soft plug and 5.8% no plug. These sperm plug types corresponded to sharply decreasing amounts of stored semen/sperm in post-spawn females. In the laboratory, 11 of 20 females with no plug produced a full clutch that became “abnormal” through egg loss or was completely dropped within 2 weeks of spawning. Thus, sperm limitation is one likely cause of abnormal early clutches on female American lobster, which may be occasioned by fishery-induced reductions in male reproductive potential and/or density-dependent processes occurring at currently high population levels.



The authors are grateful to the lobster harvesters from numerous industry associations who raised concern over the production of abnormal clutches by female American lobsters on their fishing grounds and enabled the extensive collection of samples throughout eastern Canada that made this project possible. We would also like to thank the students and staff in the Rochette laboratory for assisting in the field and in the laboratory. Comments from Marthe Haarr, Heather Hunt, Jeff Houlahan and the three anonymous reviewers greatly improved this manuscript. This project was funded by grants to R. Rochette from the Lobster Node of the NSERC Canadian Fisheries Research Network. F. Tang was funded by a NSERC CGS M (Grant no. CGSM-444848-2013).

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Ethical standards

All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study were followed and all necessary approvals were obtained.

Supplementary material

227_2019_3585_MOESM1_ESM.pdf (259 kb)
Supplementary material 1 (PDF 259 kb)


  1. Aiken DE, Waddy SL (1982) Cement gland development, ovary maturation and reproductive cycles in the American Lobster Homarus americanus. J Crustac Biol 2:315–327. CrossRefGoogle Scholar
  2. Aiken DE, Waddy SL, Mercer SM (2004) Confirmation of external fertilization in the American lobster, Homarus americanus. J Crustac Biol 24:474–480CrossRefGoogle Scholar
  3. ASMFC (2009) American lobster stock assessment report for peer review. ASMFC Stock Assessment Report No. 09-01 (Supplement). Atlantic States Marine Fisheries Commission, Washington, DCGoogle Scholar
  4. Attard J, Hudon C (1987) Embryonic development and energetic investment in egg production in relation to size of female lobster (Homarus americanus). Can J Fish Aquat Sci 44:1157–1164. CrossRefGoogle Scholar
  5. Belgrad BA, Griffen BD (2016) The influence of diet composition on fitness of the blue crab, Callinectes sapidus. PLoS One 11:e0145481. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Botsford LW (1991) Crustacean egg production and fisheries management. In: Wenner AM, Kuris A, Balkema AA (eds) Crustacean egg production. CRC Press, Rotterdam, pp 379–394Google Scholar
  7. Bray A, Ismay C, Baumer B, Cetinkaya-Rundel M (2019) Infer: tidy statistical inference. R package version Accessed 10 May 2019
  8. Butler MJ, MacDiarmid A, Gnanalingam G (2015) The effect of parental size on spermatophore production, egg quality, fertilization success, and larval characteristics in the Caribbean Spiny lobster, Panulirus argus. ICES J Mar Sci 72:i115–i123. CrossRefGoogle Scholar
  9. Campbell A (1980) A review of mortality estimates of lobster populations in the Canadian Maritimes. Can Tech Rep Fish Aquat Sci 932:28–35Google Scholar
  10. Campbell A, Brattey J (1986) Egg loss from the American lobster, Homarus americanus, in relation to nemertean, Pseudocarcinonemertes homari, infestation. Can J Fish Aquat Sci 43:772–780CrossRefGoogle Scholar
  11. Carloni JT, Wahle R, Geoghegan P, Bjorkstedt E (2018) Bridging the spawner-recruit disconnect: trends in American lobster recruitment linked to the pelagic food web. Bull Mar Sci 94:719–735CrossRefGoogle Scholar
  12. Cobb JS, Wang D (2012) Fisheries biology of lobsters and crayfishes. In: Provenzano AJ (ed) Economic aspects: fisheries and culture. Academic Press, Orlando, pp 167–230Google Scholar
  13. Comeau M, Benhalima K (2018) Functional anatomy of the female reproductive system of the American lobster (Homarus americanus). J Morphol 279:1603–1614PubMedCrossRefGoogle Scholar
  14. Currie JJ, Schneider DC (2011) Spatial scaling from latitudinal gradients: size specific fecundity in the American lobster Homarus americanus. Mar Ecol Prog Ser 439:193–201CrossRefGoogle Scholar
  15. Dehn PF, Aiken DE, Waddy SL (1983) Aspects of vitellogenesis in the lobster Homarus americanus. Can Tech Rep Fish Aquat Sci 1161:1–28Google Scholar
  16. DFO (2016) 2015 lobster stock assessment in the Magdalen Islands (LFA 22), Quebec area. DFO Can Sci Advis Sec, Sci Advis Rep 2016/045Google Scholar
  17. DFO (2018) 2016 value of Atlantic coast commercial landings, by region (thousand dollars). Accessed 1 Oct 2018
  18. DFO (2019) Commercial fisheries for Rock crab, Toad crab and Jonah crab. Accessed 10 May 2019
  19. Easton MDL (1976) Lobster population modelling. Ann Rep Fish Mar Serv, Biol Sta. St. John’s, NewfoundlandGoogle Scholar
  20. Ennis GP, Collins PW (1983) Computer program to assess egg production per recruit in a lobster (Homarus americanus) population. Can Tech Rep Fish Aquat Sci 1198:1–15Google Scholar
  21. Erkan M, Tunali Y, Sancar-Bas S (2009) Male reproductive system morphology and spermatophore formation in Astacus leptodactylus (Eschscholtz, 1823) (Decapoda: Astacidae). J Crustac Biol 29:42–50CrossRefGoogle Scholar
  22. Fogarty MJ (1995) Populations, fisheries, and management. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press, San Diego, pp 111–137CrossRefGoogle Scholar
  23. FRCC (2007) Sustainability framework for Atlantic lobster. Fisheries Resource Conservation Council, Report to the Minister of Fisheries and Oceans. July 2007. Minister of Supply and Services Canada, Cat. No. Fs158-2/2Google Scholar
  24. Gaudette J, Tremblay MJ, Silva AM, Denton CSPD (2014) Reproductive status of the American lobster in southwest Nova Scotia and the Bay of Fundy (Lobster Fishing Areas 34-38). DFO Can Sci Advis Sec Res Doc 2014/045Google Scholar
  25. Gendron L, Fradette P, Godbout G (2001) The importance of rock crab (Cancer irroratus) for growth, condition and ovary development of adult American lobster (Homarus americanus). J Exp Mar Biol Ecol 262:221–241PubMedCrossRefGoogle Scholar
  26. Goldstein JS, Shields JD (2018) Bait-subsidized diets and their effects on ovigerous North American lobsters (Homarus americanus). Aquacult Int 26:1311–1326. CrossRefGoogle Scholar
  27. Goldstein JS, Pugh TL, Dubofsky EA, Lavalli KL, Clancy M, Watson WH (2014) A noninvasive method for in situ determination of mating success in female American lobsters (Homarus americanus). J Vis Exp. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gosselin T, Sainte-Marie B, Bernatchez L (2003) Patterns of sexual cohabitation and female ejaculate storage in the American lobster (Homarus americanus). Behav Ecol Sociobiol 55:151–160. CrossRefGoogle Scholar
  29. Gosselin T, Sainte-Marie B, Bernatchez L (2005) Geographic variation of multiple paternity in the American lobster, Homarus americanus. Mol Ecol 14:1517–1525. CrossRefPubMedGoogle Scholar
  30. Grabowski JH, Gaudette J, Clesceri EJ, Yund PO (2009) The role of food limitation in lobster population dynamics in coastal Maine, United States, and New Brunswick, Canada. New Zeal J Mar Freshw Res 43:185–193CrossRefGoogle Scholar
  31. Griffen BD (2014) Linking individual diet variation and fecundity in an omnivorous marine consumer. Oecologia 174:121–130PubMedCrossRefGoogle Scholar
  32. Haarr ML, Sainte-Marie B, Comeau M, Tremblay MJ, Rochette R (2018) Female American lobster (Homarus americanus) size-at-maturity declined in Canada during the 20th and early 21st centuries. Can J Fish Aquat Sci 75:908–924. CrossRefGoogle Scholar
  33. Harrison KE (1990) The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: a review. J Shellfish Res 9:1–28Google Scholar
  34. Hedgecock D, Moffett WL, Borgeson W, Nelson K (1978) Progress and problems in lobster broodstock development. Proc World Maric Soc 9:497–506CrossRefGoogle Scholar
  35. Hines AH, Jivoff PR, Bushmann PJ, Van Montfrans J, Reed SA, Wolcott DL, Wolcott TG (2003) Evidence for sperm limitation in the blue crab, Callinectes sapidus. Bull Mar Sci 72:287–310Google Scholar
  36. Jury SH, Pugh TL, Henninger H, Carloni JT, Watson WH (2019) Patterns and possible causes of skewed sex ratios in American lobster (Homarus americanus) populations. Invert Reprod Dev 63:189–199. CrossRefGoogle Scholar
  37. Kelly CD, Jennions MD (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol Rev 86:863–884PubMedCrossRefPubMedCentralGoogle Scholar
  38. Kooda-Cisco MJ, Talbot P (1982) A structural analysis of the freshly extruded spermatophore from the lobster, Homarus americanus. J Morphol 172:193–207PubMedCrossRefPubMedCentralGoogle Scholar
  39. Koopman HN, Westgate AJ, Siders ZA (2014) Declining fecundity and factors affecting embryo quality in the American lobster (Homarus americanus) from the Bay of Fundy. Can J Fish Aquat Sci 72:352–363CrossRefGoogle Scholar
  40. Kuris AM, Wickham DE (1987) Effect of nemertean egg predators on crustaceans. Bull Mar Sci 41:151–164Google Scholar
  41. Lambert Y (2008) Why should we closely monitor fecundity in marine fish populations. J Northwest Atl Fish Sci 41:93–106CrossRefGoogle Scholar
  42. Lowerre-Barbieri SK, Brown-Peterson NJ, Murua H (2011) Emerging issues and methodological advances in fisheries reproductive biology. Mar Coast Fish 3:32–51CrossRefGoogle Scholar
  43. MacDiarmid AB, Butler MJ (1999) Sperm economy and limitation in spiny lobsters. Behav Ecol Sociobiol 46:14–24CrossRefGoogle Scholar
  44. MacDiarmid AB, Sainte-Marie B (2006) Reproduction. In: Phillips BF (ed) Lobsters: biology, management, aquaculture and fisheries. Blackwell, Oxford, pp 45–77CrossRefGoogle Scholar
  45. Marshall CT (2016) Implementing information on stock reproductive potential in fisheries management: the motivation, challenges and opportunities. In: Jakobsen TT, Fogarty M, Megrey BA, Moksness E (eds) Fish reproductive biology: implications for assessment and management. Wiley-Blackwell, Oxford, pp 438–464CrossRefGoogle Scholar
  46. Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60Google Scholar
  47. Miller RJ (1995) Fishery regulations and methods. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press, San Diego, pp 89–109CrossRefGoogle Scholar
  48. NOAA (2017) NOAA Fisheries Landings Accessed 22 Apr 2019
  49. Ouellet P, Plante F (2004) An investigation of the sources of variability in American lobster (Homarus americanus) eggs and larvae: female size and reproductive status, and interannual and interpopulation comparisons. J Crustac Biol 24:481–495CrossRefGoogle Scholar
  50. Pardo LM, Riveros MP, Fuentes JP, Pinochet R, Cardenas C, Sainte-Marie B (2017) High fishing intensity reduces females’ sperm reserve and brood fecundity in a eubrachyuran crab subject to sex- and size-biased harvest. ICES J Mar Sci 74:2459–2469CrossRefGoogle Scholar
  51. Powell GC, James KE, Hurd CL (1974) Ability of male king crab, Paralithodes camtschatica to mate repeatedly, Kodiak, Alaska, 1973. Fish Bull 72:171–179Google Scholar
  52. Pugh TL, Goldstein JS, Lavalli KL, Clancy M, Watson WH (2013) At-sea determination of female American lobster (Homarus americanus) mating activity: patterns vs. expectations. Fish Res 147:327–337. CrossRefGoogle Scholar
  53. Pugh TL, Comeau M, Benhalima K, Watson WH (2015) Variation in the size and composition of ejaculates produced by male American lobsters, Homarus americanus Milne Edwards, 1837 (Decapoda: Nephropidae). J Crustac Biol 35:593–604CrossRefGoogle Scholar
  54. Ripley B, Venables W, Ripley MB (2016) Package ‘nnet’. R package version 7:3–12Google Scholar
  55. Robertson DN, Butler MJ (2013) Mate choice and sperm limitation in the spotted spiny lobster, Panulirus guttatus. Mar Biol Res 9:69–76CrossRefGoogle Scholar
  56. Rochette R, Sainte-Marie B, Allain M, Baker J, Bernatchez L, Boudreau V, Comeau M, Côté J, Miron G, Ramsay L, Squires K, Tremblay MJ (2017) The Lobster Node of the CFRN: co-constructed and collaborative research on productivity, stock structure and connectivity in the American lobster Homarus americanus. Can J Fish Aquat Sci 75:813–824. CrossRefGoogle Scholar
  57. Rubolini D, Galeotti P, Ferrari G, Spairani M, Bernini F, Fasola M (2006) Sperm allocation in relation to male traits, female size, and copulation behaviour in freshwater crayfish species. Behav Ecol Sociobiol 60:212–219CrossRefGoogle Scholar
  58. Sainte-Marie B, Chabot D (2002) Ontogenetic shifts in natural diet during benthic stages of American lobster (Homarus americanus), off the Magdalen Islands. Fish Bull 100:106–116Google Scholar
  59. Sainte-Marie B, Gosselin T, Sévigny JM, Urbani N (2008) The snow crab mating system: opportunity for natural and unnatural selection in a changing environment. Bull Mar Sci 83:131–161Google Scholar
  60. Sato T, Ashidate M, Jinbo T, Goshima S (2007) Does male-only fishing influence reproductive success of the female spiny king crab, Paralithodes brevipes? Can J Fish Aquat Sci 64:735–742CrossRefGoogle Scholar
  61. Sibert V, Ouellet P, Brêthes J-C (2004) Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle. Mar Biol 144:1075–1086CrossRefGoogle Scholar
  62. Smith EM (1977) Some aspects of catch/effort, biology, and the economics of the Long Island Sound lobster fishery during 1976. NOAA, NMFS, Comm Fish Res Dev Act Final Rep, Proj No 3-253-R-1, pp 1–97Google Scholar
  63. Sørdalen TK, Halvorsen KT, Harrison HB, Ellis CD, Vøllestad LA, Knutsen H, Moland E, Olsen EM (2018) Harvesting changes mating behaviour in European lobster. Evol Appl 11:963–977. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Subramoniam T (1991) Chemical composition of spermatophores in decapod crustaceans. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 308–321CrossRefGoogle Scholar
  65. Talbot P, Helluy S (1995) Reproduction and embryonic development. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press, San Diego, pp 177–216CrossRefGoogle Scholar
  66. Tang F, Haarr ML, Sainte-Marie B, Comeau M, Tremblay MJ, Gaudette J, Rochette R (2018) Spatio-temporal patterns and reproductive costs of abnormal clutches of female American lobster, Homarus americanus, in eastern Canada. ICES J Mar Sci 75:2045–2059. CrossRefGoogle Scholar
  67. Templeman W (1936) Further contributions to lobster mating. J Biol Board Canada 2:223–226CrossRefGoogle Scholar
  68. Templeman W (1940) Embryonic developmental rates and egg-laying of Canadian lobsters. J Fish Board Canada 5:71–83CrossRefGoogle Scholar
  69. Tully O, Roantree V, Robinson M (2001) Maturity, fecundity and reproductive potential of the European lobster (Homarus gammarus) in Ireland. J Mar Biol Assoc UK 81:61–68CrossRefGoogle Scholar
  70. Waddy SL, Aiken DE (1990) Intermolt insemination, an alternative mating strategy for the American lobster (Homarus americanus). Can J Fish Aquat Sci 47:2402–2406CrossRefGoogle Scholar
  71. Waddy SL, Aiken DE (1991) Egg production in the American lobster, Homarus americanus. In: Wenner AM, Kuris A, Balkema AA (eds) Crustacean egg production. CRC Press, Delft, pp 267–288Google Scholar
  72. Waddy SL, Aiken DE, De Klejin DPV (1995) Control of growth and reproduction. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press, San Diego, pp 217–266CrossRefGoogle Scholar
  73. Waddy SL, Feindel N, Hamilton-Gibson N, Aiken DE, Merritt V, Leavitt N (2017) Reproductive cycles and mating capacity in male American lobsters (Homarus americanus). Fish Res 186:358–366. CrossRefGoogle Scholar
  74. Wahle RA (2003) Revealing stock-recruitment relationships in lobsters and crabs: is experimental ecology the key? Fish Res 65:3–32. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New Brunswick Saint JohnSaint JohnCanada
  2. 2.Institut Maurice-Lamontagne, Pêches et Océans CanadaMont-JoliCanada
  3. 3.Department of Fisheries and OceansSaint Andrews Biological StationSaint AndrewsCanada

Personalised recommendations