Advertisement

Aquaculture International

, Volume 26, Issue 6, pp 1311–1326 | Cite as

Bait-subsidized diets and their effects on ovigerous North American lobsters (Homarus americanus)

  • Jason S. Goldstein
  • Jeffrey D. Shields
Article

Abstract

Ovigerous American lobsters (Homarus americanus) display a protracted period of ovary maturation and maternal care when incubating their eggs, potentially influencing offspring fitness. Lobsters consume a wide range of food items; however, trap bait may comprise a larger proportion of their diet in some fished areas compared to non-fished areas, and the long-term consequences of a bait-based diet remain largely unexplored in lobsters. We tested the hypothesis that disproportionate amounts of bait in the diets of pre-ovigerous females affect the quality of their ovaries and eggs. We held pre-ovigerous lobsters (n = 29) over a period of ~ 300 days (range = 270–378) and fed them diets of herring bait, natural prey items (crab, mussel, urchin, macroalgae), or a combination of both diet types. Nutritional status, measured as biweekly blood indices and total glucose levels, suggest differences between lobsters fed a natural or combination diet and lobsters fed a bait-based diet (ANOVA; P < 0.05). We found that bait diets contained more protein (58.5%) and lipids (31.6%) compared to natural diets (34.5 and 13.2%, respectively) and lipid levels in ovaries and eggs significantly correlated with each other for all treatments (r = 0.76, n = 15, P = 0.028). Histopathological analysis indicates that ovaries contained more variable maturation in starved lobsters or those fed with bait, with some animals showing delayed gonad maturation. Results suggest that a varied diet promotes the overall fitness of ovigerous lobsters and the associated reserves that are used for ovarian development and subsequent oocyte formation.

Keywords

Maternal effects Ovigerous lobsters Egg lipids Atlantic herring 

Notes

Acknowledgments

We thank Nancy Whitehouse (UNH, Dairy Research Center) who helped with the nutritional analyses as well as provided laboratory equipment for processing samples, and the encouragement and support from Prof. Win Watson. Thanks to several lobstermen from New Hampshire for their help in collecting live lobsters for this study. We appreciate the help from Tracy Pugh, Kate Masury, and Audra Chaput who all assisted in weekly feedings, sampling, and general maintenance throughout the study. Nathan Rennels and Noel Carlson of the UNH Coastal Marine Laboratory helped coordinate logistics and space.

Funding

This research was supported from grants awarded to JSG from the UNH Marine Program and a Lerner-Gray Fund for Marine Research (American Museum of Natural History).

Compliance with ethical standards

All lobsters were collected and held in accordance with NHFG permits MFD0920 and MFD1016 issued to the University of New Hampshire.

Conflict of interest

The authors declare no conflict of interest.

References

  1. Amsler MO, George RY (1984) Seasonal variation in the biochemical composition of the embryos of Callinectes sapidus. Rathbun. J Crustacean Biol 4:546–553CrossRefGoogle Scholar
  2. ASMFC (2015) American Lobster Benchmark Stock Assessment and Peer Review ReportGoogle Scholar
  3. Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105CrossRefGoogle Scholar
  4. Bertram DF, Strathmann RR (1998) Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79:315–327CrossRefGoogle Scholar
  5. Bethoney ND, Stokesbury KD, Stevens BG, Altabet MA (2011) Bait and the susceptibility of American lobsters Homarus americanus to epizootic shell disease. Dis Aquat Org 95:1–8CrossRefGoogle Scholar
  6. Boghen AD, Castell JD, Conklin DE (1982) In search of a reference protein to replace “vitamin-free casein” in lobster nutrition studies. Can J Zool 60:2033–2038CrossRefGoogle Scholar
  7. Bordner CE, D’Abramo LR, Conklin DE (1983) Assimilation of nutrients by cultured hybrid lobsters (Homarus sp.) fed experimental diets. J World Maricult Soc 14:11–24CrossRefGoogle Scholar
  8. Boudreau SA, Worm B (2010) Top-down control of lobster in the Gulf of Maine: insights from local ecological knowledge and research surveys. Mar Ecol Prog Ser 403:181–191CrossRefGoogle Scholar
  9. Boudreau SA, Anderson SC, Worm B (2015) Top-down and bottom-up forces interact at thermal range extremes on American lobster. J Anim Ecol 84:840–850CrossRefGoogle Scholar
  10. Brander K (2010) Impacts of climate change on fisheries. J Marine Syst 79:389–402CrossRefGoogle Scholar
  11. Bumpus HC (1891) The embryology of the American lobster. J Morphol 5:215–262CrossRefGoogle Scholar
  12. Campbell A (1986) Migratory movements of ovigerous lobster, Homarus americanus, tagged off grand Manan, eastern Canada. Can J Fish Aquat Sci 43:2197–2205CrossRefGoogle Scholar
  13. Campbell A, Stasko AB (1985) Movements of lobsters (Homarus americanus) tagged in the Bay of Fundy. Canada Mar Biol 92:393–404CrossRefGoogle Scholar
  14. Castell JD, Covey JF (1976) Dietary lipid requirements of adult lobsters, Homarus americanus. J Nutr 106:1159–1165CrossRefGoogle Scholar
  15. Carrasco SA, Phillips NE, Sewell MA (2016) Maternal lipid provisioning mirrors evolution of reproductive strategies in direct-developing whelks. Biol Bull 230:188–196CrossRefGoogle Scholar
  16. Castell JD, Kean JC (1986) Evaluation of the role of nutrition in lobster recruitment. Can J Fish Aquat Sci 43:2320–2327CrossRefGoogle Scholar
  17. Clark AS, Jury SH, Goldstein JS, Langley TG, Watson WH III (2015) A comparison of American lobster size structure and abundance using standard and ventless traps. Fish Res 167:243–251CrossRefGoogle Scholar
  18. Cooper R, Uzmann J (1980) Ecology of juvenile and adult Homarus. In: Cobb JS, Phillips BF (eds) The biology and management of lobsters. Academic Press, New York, pp 97–142CrossRefGoogle Scholar
  19. Conklin DE (1995) Digestive physiology and nutrition. In: Biology of the lobster Homarus americanus. In: Factor JR (ed) Academic Press, San Diego, pp 153–175Google Scholar
  20. Cowan DF, Watson WHIII, Solow AR, Mountcastle AM (2007) Thermal histories of brooding lobsters, Homarus americanus, in the Gulf of Maine. J Mar Biol 179:70–78Google Scholar
  21. Dall W, Smith DM, Moore LE (1995) Carotenoids in the tiger prawn Penaeus esculentus during ovarian maturation. Mar Biol 123:435–441CrossRefGoogle Scholar
  22. Drinkwater KF, Harding GC, Mann KH, Tanner N (1996) Temperature as a possible factor in the increased abundance of American lobster, Homarus americanus, during the 1980s and early 1990s. Fish Oceanogr 5:176–193CrossRefGoogle Scholar
  23. Elner RW, Campbell A (1987) Natural diets of lobster Homarus americanus from barren ground and macroalgal habitats off southwestern Nova Scotia, Canada. Mar Ecol Prog Ser 37:131–140CrossRefGoogle Scholar
  24. Fox CW (2000) Natural selection on seed-beetle egg size in nature and the laboratory: variation among environments. Ecology 81:3029–3035CrossRefGoogle Scholar
  25. Gallagher ML, Bayer RC, Rittenburg JH, Leavitt DF (1983) Studies on the mineral requirements of the adult American lobster. Prog Fish Cult 44:210–212CrossRefGoogle Scholar
  26. 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 262:221–241CrossRefGoogle Scholar
  27. Geraldi NR, Wahle RA, Dunnington M (2009) Habitat effects on American lobster (Homarus americanus) movement and density: insights from georeferenced trap arrays, seabed mapping, and tagging. Can J Fish Aquat Sci 66:460–470CrossRefGoogle Scholar
  28. Goldstein JS, Pugh TL, Dubofsky EA, Lavalli KL, Clancy M, Watson WH (2014) A non-invasive method for in-situ determination of mating success in female American lobsters (Homarus americanus). JOVE- J Vis Exp 84:e50498.  https://doi.org/10.3791/5049 CrossRefGoogle Scholar
  29. Goldstein JS, Watson WH III (2015a) Seasonal movements of American lobsters in southern Gulf of Maine coastal waters: patterns, environmental triggers, and implications for larval release. Mar Ecol Prog Ser 524:197–211.  https://doi.org/10.3354/meps11192 CrossRefGoogle Scholar
  30. Goldstein JS, Watson WH III (2015b) Quantifying the influence of natural inshore and offshore thermal regimes on egg development in the north American lobster, Homarus americanus. Biol Bull 228:1–12CrossRefGoogle Scholar
  31. 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 Fresh 43:185–193CrossRefGoogle Scholar
  32. Grabowski JH, Clesceri EJ, Gaudette J, Baukus A, Weber M, Yund PO (2010) Use of herring bait to farm lobsters in the Gulf of Maine. PLoS One 5:e10188CrossRefGoogle Scholar
  33. Gutzler BC, Butler MJ IV (2017) Comparison of methods for determining nutritional condition in spiny lobsters. J Shell Res 36:175–179CrossRefGoogle Scholar
  34. Hanson JM (2009) Predator–prey interactions of American lobster (Homarus americanus) in the southern Gulf of St. Lawrence, Canada. New Zeal J Mar Fresh 43:69–88CrossRefGoogle Scholar
  35. Harnish L, Martin Willison JH (2009) Efficiency of bait usage in the Nova Scotia lobster fishery: a first look. J Clean Prod 17:345–347CrossRefGoogle Scholar
  36. Herrick FH (1895) The American lobster: a study of its habits and development. Bull. U.S. fish Comm 15: 1–252 + 254 platesGoogle Scholar
  37. Herrick FH (1909) Natural history of the American lobster. Bulletin US Bureau of Fisheries 29:147Google Scholar
  38. Hirtle RWM, Mann KH (1978) Distance chemoreception and vision in the selection of prey by American lobster (Homarus americanus). J Fish Res Board Can 35:1006–1008CrossRefGoogle Scholar
  39. Holland D (1978) Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In: Malins DC (ed) Biochemical and biophysical perspectives in marine biology. Academic Press, Seattle, pp 85–123Google Scholar
  40. Johnson KJ, Goldstein JS, Watson WH III (2011) Two methods for determining the fertility status of early-stage American lobster, Homarus americanus, eggs. J Crustacean Biol 31:693–700CrossRefGoogle Scholar
  41. Jones PL, Shulman MJ (2008) Subtidal-tidal trophic links: American lobsters [(Homarus americanus (Milne-Edwards)] forage in the intertidal zone on nocturnal high tides. J Exp Mar Biol Ecol 361:98–103Google Scholar
  42. Jury SH, Howell H, O’Grady DF, Watson WHIII (2001) Lobster trap video: in situ video surveillance of the behavior of Homarus americanus in and around traps. New Zeal J Mar Fresh 52:1125–1132CrossRefGoogle Scholar
  43. Karnofsky EB, Price HJ (1989) Behavioural response of the lobster Homarus americanus to traps. Can J Fish Aquat Sci 46:1625–1632CrossRefGoogle Scholar
  44. Kean JC, Castell JD, Boghen AG, D’Abramo LR, Conklin DE (1985) A reevaluation of the lecithin and cholesterol requirements of juvenile lobsters (Homarus americanus) using crab protein based diets. Aquaculture 47:143–149CrossRefGoogle Scholar
  45. Leavitt DF, Bayer RC (1977) A refractometric method of determining serum protein concentration in the American lobster. Aquaculture 12:169–171CrossRefGoogle Scholar
  46. Lewis AR, Choat JH (1993) Spawning mode and reproductive output of the tropical cephalopod Idiosepius pygmaeus. Can J Fish Aquat Sci 50:20–28CrossRefGoogle Scholar
  47. Linan-Cabello MA, Paniagua-Michel J, Hopkins PM (2002) Bioactive roles of carotenoids and retinoids in crustaceans. Aquac Nutr 8:299–309CrossRefGoogle Scholar
  48. Maine Division of Marine Resources (DMR) (2017). https://www.maine.gov/dmr/commercial-fishing/landings/index.html. Accessed 10 Mar 1998
  49. Mann KH, Breen PA (1972) The relation between lobster abundance, sea urchins and kelp beds. J Fish Res Board Can 29:603–609CrossRefGoogle Scholar
  50. Marshall DJ, Keough MJ (2004) When the going gets rough: effect of maternal size manipulation on offspring quality. Mar Ecol Prog Ser 272:301–305CrossRefGoogle Scholar
  51. Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:3–50Google Scholar
  52. Melvin GD, Stephenson RL (2007) The dynamics of a recovering fish stock: Georges Bank herring. ICES J Mar Sci 64:69–82CrossRefGoogle Scholar
  53. Miller RJ (1995) Fishery regulations and methods. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press Inc., San Diego, CA, pp. 89–109CrossRefGoogle Scholar
  54. Mills KE, Pershing AJ, Brown CJ, Chen Y, Fu-Sung C, Holland DS, Sigrid L, Nye JA, Sun JC, Thomas AC, Wahle RA (2013) Fisheries management in a changing climate: lessons from the 2012 ocean heat wave in the Northwest Atlantic. Oceanography 26:191–195CrossRefGoogle Scholar
  55. Moland E, Moland Olsen E, Stenseth NC (2010) Maternal influence on offspring size variation and viability in wild European lobster Homarus gammarus. Mar Ecol Prog Ser 400:165–173CrossRefGoogle Scholar
  56. Myers A, Tlusty MF (2009) A long-term assessment of the physiological effects of herring (Clupea harengus) as a dietary component of the American lobster (Homarus americanus). New Zeal J Mar Fresh 43:173–183CrossRefGoogle Scholar
  57. Nye J (2010) State of the Gulf of Maine Report: climate change and its effects on ecosystems, habitats and biota. NOAA and the Gulf of Maine Council on the Marine Environment. Woods Hole, MA,18 ppGoogle Scholar
  58. Oliver MD, MacDiarmid AB (2001) Blood refractive index and ratio of weight to carapace length as indices of nutritional condition in juvenile rock lobsters (Jasus edwardsii). New Zeal J Mar Fresh 52:1395–1400CrossRefGoogle Scholar
  59. Ojeda PF, Dearborn JH (1991) Feeding ecology of benthic mobile predators: experimental analysis of their influence in rocky subtidal communities of the Gulf of Maine. J Exp Mar Biol Ecol 149:13–44CrossRefGoogle Scholar
  60. Oviatt CA (2004) The changing ecology of temperate coastal waters during a warming trend. Estuaries 27:895–904CrossRefGoogle Scholar
  61. Ozbay G, Riley JG (2002) An analysis of refractometry as a method of determining blood total protein concentration in the American lobster Homarus americanus (Milne Edwards). Aquac Res 33:557–562CrossRefGoogle Scholar
  62. Palma AT, Wahle RA, Steneck RS (1998) Different early post-settlement strategies between American lobsters Homarus americanus and rock crabs Cancer irroratus in the Gulf of Maine. Mar Ecol Prog Ser 162:215–225CrossRefGoogle Scholar
  63. Peters-Didier J, Sewell MA (2017) Maternal investment and nutrient utilization during early larval development of the sea cucumber Australostichopus mollis. Mar Biol 164:178CrossRefGoogle Scholar
  64. Pinsky ML, Fogarty M (2012) Lagged social–ecological responses to climate and range shifts in fisheries. Clim Chang 115:883–891CrossRefGoogle Scholar
  65. Prince D, Bayer B, Gallagher M, Subramanyam M (1995) Reduction of shell disease with an experimental diet in a Nova Scotian lobster pound. J Shellfish Res 14:205–207Google Scholar
  66. Pugh TP (2014) The potential for sperm limitation in American lobsters (Homarus americanus) as indicated by female mating activity and male reproductive capacity. PhD Dissertation. 213 p.Google Scholar
  67. Pugh TP, Goldstein JS, Lavalli, KL, Clancy M, Watson WH III (2013) At-sea determination of female American lobster (Homarus americanus) mating activity: Patterns vs. expectations. Fish Res 147:327–337CrossRefGoogle Scholar
  68. Qian PY, Chia FS (1991) Fecundity and egg size are mediated by food quality in the polycheate worm Capitella sp. J Exp Mar Biol Ecol 148:11–25CrossRefGoogle Scholar
  69. Saila SB, Nixon S, Oviatt C (2002) Does lobster trap bait influence the Maine inshore trap fishery? N Am J Fish Manage 22:602–605CrossRefGoogle Scholar
  70. Sainte-Marie B, Chabot D (2002) Ontogenetic shifts in natural diet during benthic stages of American lobster (Homarus americanus) off the Magdalene Islands. Fish Bull100:106–116Google Scholar
  71. Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster, Homarus americanus. Can J Fish Aquat Sci 43:2311–2319CrossRefGoogle Scholar
  72. Sato T, Suzuki N (2010) Female size as a determinant of larval size, weight, and survival period in the coconut crab, Birgus latro. J Crustacean Biol 30:624–628CrossRefGoogle Scholar
  73. Scarratt DJ (1980) The food of lobsters. Can Tech Rep Fish Aquat Sci 954:66–91Google Scholar
  74. Shields JD, Wheeler KN, Moss JA (2012) Histological assessment of the lobster (Homarus americanus) in the “100 lobsters project”. J Shellfish Res 31:439–447CrossRefGoogle Scholar
  75. Sibert V, Ouellet P, Brethes J-C (2004) Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated temperature cycle. Mar Biol 144:1075–1086CrossRefGoogle Scholar
  76. Sindermann CJ (1990) Principal diseases of marine fish and shellfish. Vol. 2. Academic Press Inc. San Diego, CA, 516 ppGoogle Scholar
  77. Steneck RS, Wilson CJ (2011) Large-scale and long-term, spatial and temporal patterns in demography and landings of the American lobster, Homarus americanus, in Maine. Mar Freshw Res 52:1303–1319CrossRefGoogle Scholar
  78. Talbot P, Helluy S (1995) Reproduction and embryonic development. In: Factor JR (ed) Biology of the lobster Homarus americanus. Academic Press Inc. San Diego, CA, pp 177–216CrossRefGoogle Scholar
  79. Thunberg EM (2007) Demographic and economic trends in the northeastern United States lobster (Homarus americanus) fishery, 1970–2005. US Dept of Commer, Northeast Fish Sci Cent Ref Doc 07-17, 64 ppGoogle Scholar
  80. Tlusty MF, Lightner D, Goldstein J, White B (2000) Potential synergistic stressors trigger a mortal infection in juvenile Homarus americanus. The Lobster Newsletter 13:6–8Google Scholar
  81. Tlusty MF, Goldstein JS, Fiore DR (2005a) Hatchery performance of early benthic juvenile American lobsters (Homarus americanus) fed enriched frozen adult Artemia diets. Aquac Nutr 11:191–198CrossRefGoogle Scholar
  82. Tlusty MF, Fiore DR, Goldstein JS (2005b) Use of formulated diets as replacements for Artemia in the rearing of juvenile American lobsters (Homarus americanus). Aquaculture 250:781–795CrossRefGoogle Scholar
  83. Tlusty MF, Myers A, Metzler A (2008) Short and long-term dietary effects on disease and mortality in American lobster, Homarus americanus. Dis Aquat Org 78:249–253CrossRefGoogle Scholar
  84. Waddy SL, Aiken DE (1992) Environmental intervention in the reproductive process of the American lobster, Homarus americanus. Inver Rep Devt 22:245–252CrossRefGoogle Scholar
  85. Wahle RA, Brown C, Hovel K (2013) The geography and body-size dependence of top-down forcing in New England’s lobster–groundfish interaction. Bull Mar Sci 89:189–212CrossRefGoogle Scholar
  86. Wang G, Mcgaw IJ (2014) Use of serum protein concentration as an indicator of quality and physiological condition in the lobster Homarus americanus (Milne-Edwards, 1837). J Shell Res 33:805–813CrossRefGoogle Scholar
  87. Watson WH III, Golet W, Scopel D, Jury S (2009) Use of ultrasonic telemetry to determine the area of bait influence and trapping area of American lobster, Homarus americanus, traps. New Zeal J Mar Fresh Res 43:411–418CrossRefGoogle Scholar
  88. Wells RJD, Steneck RS, Palma AT (2010) Three-dimensional resource partitioning between American lobster (Homarus americanus) and rock crab (Cancer irroratus) in a subtidal kelp forest. J Exp Mar Biol Ecol 384:1–6CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Wells National Estuarine Research ReserveThe Maine Coastal Ecology CenterWellsUSA
  2. 2.Department of Biological Sciences and School of Marine Sciences and Ocean EngineeringUniversity of New HampshireDurhamUSA
  3. 3.Department of Aquatic Health Sciences, Virginia Institute of Marine ScienceThe College of William and MaryGloucester PointUSA

Personalised recommendations