Bomb radiocarbon dating of the endangered white abalone (Haliotis sorenseni): investigations of age, growth and lifespan
Allen H. Andrews A G , Robert T. Leaf B , Laura Rogers-Bennett C , Melissa Neuman D , Heather Hawk E and Gregor M. Cailliet F
+ Author Affiliations
- Author Affiliations
A NOAA Fisheries, Pacific Islands Fisheries Science Center, 99‐193 Aiea Heights Drive, #417, Aiea, HI 96701, USA.
B Department of Coastal Sciences, The University of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564, USA.
C Bodega Marine Laboratory – California Department of Fish and Wildlife, 2099 Westside Road, Bodega Bay, CA 94923, USA.
D NOAA Fisheries, Southwest Region, Office of Protected Resources, 501 West Ocean Boulevard, Suite 4200, Long Beach, CA 90802-4213, USA.
E Département de Biologie, Université Laval, 1045 Avenue de la Médecine, Québec, QC G1V 0A6, Canada.
F Moss Landing Marine Laboratories, California State University, 8272 Moss Landing Road, Moss Landing, CA 95039, USA.
G Corresponding author. Email: allen.andrews@noaa.gov
Marine and Freshwater Research 64(11) 1029-1039 https://doi.org/10.1071/MF13007
Submitted: 8 January 2013 Accepted: 27 April 2013 Published: 19 July 2013
Abstract
Understanding basic life-history characteristics of white abalone (Haliotis sorenseni), such as estimated lifespan, is critical to making informed decisions regarding the recovery of this endangered species. All predictive modelling tools used to forecast the status and health of populations following restoration activities depend on a validated estimate of adult lifespan. Of the seven Haliotis species in California, white abalone is considered to have the highest extinction risk and was the first marine invertebrate listed as an endangered species under the Federal Endangered Species Act (ESA). Lifespan was previously estimated from observations of early growth; however, no study has generated ages for the largest white abalone. To address questions of age and growth, bomb radiocarbon (Δ14C) dating was used on shells from large white abalone. Measured bomb Δ14C levels were compared to regional Δ14C reference records to provide estimates of age, growth and lifespan. Bomb radiocarbon dating indicated that growth was variable among individuals, with a maximum estimated age of 27 years. The findings presented here provide support for previous age and growth estimates and an estimated lifespan near 30 years. These age data support the perception of a critical need for restoring the remnant aging and potentially senescent population.
Additional keywords: age validation, carbon-14, Haliotidae, longevity, Mollusca, Southern California Bight.
References
Andrews, A. H., Kerr, L. A., Cailliet, G. M., Brown, T. A., Lundstrom, C. C., and Stanley, R. D. (2007). Age validation of canary rockfish (Sebastes pinniger) using two independent otolith techniques: lead–radium and bomb radiocarbon dating. Marine and Freshwater Research 58, 531–541.| Age validation of canary rockfish (Sebastes pinniger) using two independent otolith techniques: lead–radium and bomb radiocarbon dating.Crossref | GoogleScholarGoogle Scholar |
Beamish, R. J., and McFarlane, G. A. (1983). The forgotten requirement for age validation in fisheries biology. Transactions of the American Fisheries Society 112, 735–743.
| The forgotten requirement for age validation in fisheries biology.Crossref | GoogleScholarGoogle Scholar |
Bevelander, E. (1987). ‘Abalone: Gross and Fine Structure.’ 1st edn. (Boxwood Press: Pacific Grove, CA.)
Broecker, W. S., and Peng, T.-H. (1982). ‘Tracers in the Sea.’ (Lamont-Doherty Geological Observatory: Palisades, NY.)
Butler, J., Neuman, M., Pinkard, D., Kvitek, R., and Cochrane, G. (2006). The use of multibeam sonar mapping techniques to refine population estimates of the endangered white abalone (Haliotis sorenseni). Fishery Bulletin 104, 521–532.
Button, C. A., and Rogers-Bennett, L. (2011). Vital rates of pink abalone (Haliotis corrugata) estimated from mark–recapture data to inform recovery. Marine Ecology Progress Series 431, 151–161.
| Vital rates of pink abalone (Haliotis corrugata) estimated from mark–recapture data to inform recovery.Crossref | GoogleScholarGoogle Scholar |
Campana, S. E. (2001). Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology 59, 197–242.
| Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods.Crossref | GoogleScholarGoogle Scholar |
Daniels, R., and Floren, R. (1998). Poaching pressures on northern California’s abalone fishery. Journal of Shellfish Research 17, 859–862.
Davis, G. E., Haaker, P. L., and Richards, D. V. (1996). Status and trends of white abalone at the California Channel Islands. Transactions of the American Fisheries Society 125, 42–48.
| Status and trends of white abalone at the California Channel Islands.Crossref | GoogleScholarGoogle Scholar |
Druffel, E. R. M. (1981). Radiocarbon in annual coral rings from the eastern tropical Pacific Ocean. Geophysical Research Letters 8, 59–62.
| Radiocarbon in annual coral rings from the eastern tropical Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXoslGktA%3D%3D&md5=630ca9fb1c2edcd053a151b553afcb4bCAS |
Druffel, E. R. M. (1987). Bomb radiocarbon in the Pacific: annual and seasonal timescale variations. Journal of Marine Research 45, 667–698.
| Bomb radiocarbon in the Pacific: annual and seasonal timescale variations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXmt1arsbg%3D&md5=3c4bc9a65953a8ceebfa2fa8cf50f0d0CAS |
Druffel, E. R. M., and Linick, T. W. (1978). Radiocarbon in annual coral rings of Florida. Geophysical Research Letters 5, 913–916.
| Radiocarbon in annual coral rings of Florida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktFKgug%3D%3D&md5=02094ce1ba3c0c8d49bdd0c93f2f3803CAS |
Druffel, E. R. M., and Williams, P. M. (1991). Radiocarbon in seawater and organisms from the Pacific coast of Baja California. Radiocarbon 33, 291–296.
| 1:CAS:528:DyaK38XhtlGktr8%3D&md5=a89382701be99dc01f9da73c4f7210d1CAS |
Ebert, T. A., and Southon, J. R. (2003). Red sea urchins (Stronglyocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fishery Bulletin 101, 915–922.
Ewing, G. P., Lyle, J. M., Murphy, R. J., Kalish, J. M., and Ziegler, P. E. (2007). Validation of age and growth in a long-lived temperate reef fish using otolith structure, oxytetracycline and bomb radiocarbon methods. Marine and Freshwater Research 58, 944–955.
| Validation of age and growth in a long-lived temperate reef fish using otolith structure, oxytetracycline and bomb radiocarbon methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yit7jM&md5=579a7b5104bf682f407050aea420c64bCAS |
Fabens, A. J. (1965). Properties and fitting of the von Bertalanffy growth curve. Growth 29, 265–289.
| 1:STN:280:DyaF287gs1WmtA%3D%3D&md5=f67381e79b40face841bce80f4d07c1dCAS | 5865688PubMed |
Frantz, B. R., Kashgarian, M., Coale, K. H., and Foster, M. H. (2000). Growth rate and potential climate record from a rhodolith using 14C accelerator mass spectrometry. Limnology and Oceanography 45, 1773–1777.
| Growth rate and potential climate record from a rhodolith using 14C accelerator mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Frantz, B. R., Foster, M. S., and Riosmensa-Rodriguez, R. (2005). Clathromorphum nereostratum (Corralinales, Rhodophyta): the oldest alga? Journal of Phycology 41, 770–773.
| Clathromorphum nereostratum (Corralinales, Rhodophyta): the oldest alga?Crossref | GoogleScholarGoogle Scholar |
Haltuch, M. A., Hamell, O. S., Piner, K. R., McDonald, P., Kastelle, C. R., and Field, J. C. (2013). A California current bomb radiocarbon reference chronology and petrale sole age validation. Canadian Journal of Fisheries and Aquatic Sciences 70, 22–31.
| A California current bomb radiocarbon reference chronology and petrale sole age validation.Crossref | GoogleScholarGoogle Scholar |
Hobday, A. J., and Tegner, M. J. (2000). Status review of white abalone (Haliotis sorenseni) throughout its range in California and Mexico. NOAA Technical Memorandum NMFS, NOAA-TM-NMFS-SWR-035. United States Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Southwest Region Office, Long Beach, CA.
Kalish, J. M. (1993). Pre- and post-bomb radiocarbon in fish otoliths. Earth and Planetary Science Letters 114, 549–554.
| Pre- and post-bomb radiocarbon in fish otoliths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFKqs7k%3D&md5=a013ef4ace34ecd9715d71bbaf97a405CAS |
Kalish, J. M. (2001). Use of the bomb radiocarbon chronometer to validate fish age. Final report FRDC Project 93/109. Fisheries Research and Development Corporation, Canberra.
Karpov, K. A., Haaker, P., Taniguchi, I., and Rogers-Bennett, L. (2000). Serial depletion and the collapse of the California abalone (Haliotis spp.) fishery. In ‘Workshop on Rebuilding Abalone Stocks in British Columbia.’ (Ed. A. Campbell.) Canadian Special Publication of Fisheries and Aquatic Sciences 130, 11–24.
Kerr, L. A., Andrews, A. H., Frantz, B. R., Coale, K. H., Brown, T. A., and Cailliet, G. M. (2004). Radiocarbon in otoliths of yelloweye rockfish (Sebastes ruberrimus): a reference time series for the coastal waters of southeast Alaska. Canadian Journal of Fisheries and Aquatic Sciences 61, 443–451.
| Radiocarbon in otoliths of yelloweye rockfish (Sebastes ruberrimus): a reference time series for the coastal waters of southeast Alaska.Crossref | GoogleScholarGoogle Scholar |
Kerr, L. A., Andrews, A. H., Munk, K., Cailliet, G. M., Coale, K. H., Frantz, B. R., Cailliet, G. M., and Brown, T. A. (2005). Age validation of quillback rockfish (Sebastes maliger) using bomb radiocarbon. Fishery Bulletin 103, 97–107.
Kilada, R., Campana, S. E., and Roddick, D. (2009). Growth and sexual maturity of the northern propellerclam (Crytodaria siliqua) in eastern Canada, with bomb radiocarbon validation. Marine Biology 156, 1029–1037.
| Growth and sexual maturity of the northern propellerclam (Crytodaria siliqua) in eastern Canada, with bomb radiocarbon validation.Crossref | GoogleScholarGoogle Scholar |
Leaf, R. T., Andrews, A. H., Cailliet, G. M., and Brown, T. A. (2008a). The feasibility of bomb radiocarbon analysis to support an age-at-length relationship for red abalone, Haliotis rufescens Swainson in northern California. Journal of Shellfish Research 27, 1177–1182.
| The feasibility of bomb radiocarbon analysis to support an age-at-length relationship for red abalone, Haliotis rufescens Swainson in northern California.Crossref | GoogleScholarGoogle Scholar |
Leaf, R. T., Rogers-Bennett, L., and Jiao, Y. (2008b). Exploring the use of a size-based egg-per-recruit model for the red abalone fishery in California. North American Journal of Fisheries Management 28, 1638–1647.
| Exploring the use of a size-based egg-per-recruit model for the red abalone fishery in California.Crossref | GoogleScholarGoogle Scholar |
Linick, T. W. (1978). La Jolla measurements of radiocarbon in the oceans. Radiocarbon 20, 333–359.
| 1:CAS:528:DyaE1MXkvFKgsbk%3D&md5=6ed6cd3570f32bdf230f75b4cc76ce00CAS |
Moore, J. D., Finley, C. A., Friedman, C. S., and Robbins, T. T. (2002). Withering syndrome and restoration of southern California abalone populations. California Cooperative Oceanic Fisheries Investigations Reports 43, 112–119.
National Marine Fisheries Service (2008). ‘White Abalone Recovery Plan (Haliotis sorenseni).’ (United States Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service: Southwest Regional Office, Long Beach, CA.)
Neilson, J. D., and Campana, S. E. (2008). A validated description of age and growth of western Atlantic bluefin tuna (Thunnus thynnus). Canadian Journal of Fisheries and Aquatic Sciences 65, 1523–1527.
| A validated description of age and growth of western Atlantic bluefin tuna (Thunnus thynnus).Crossref | GoogleScholarGoogle Scholar |
Nydal, R. (2000). Radiocarbon in the ocean. Radiocarbon 42, 81–98.
| 1:CAS:528:DC%2BD3cXksl2gt78%3D&md5=020303c29adfe6b716dd05f0feac02f8CAS |
Piner, K. R., and Wischniowski, S. G. (2004). Pacific halibut chronology of bomb radiocarbon in otoliths from 1941 to 1981 and a validation of ageing methods. Journal of Fish Biology 64, 1060–1071.
| Pacific halibut chronology of bomb radiocarbon in otoliths from 1941 to 1981 and a validation of ageing methods.Crossref | GoogleScholarGoogle Scholar |
Piner, K. R., Hamel, O. S., Henkel, J. L., Wallace, J. R., and Hutchinson, C. E. (2005). Age validation of canary rockfish (Sebastes pinniger) from off the Oregon coast (USA) using the bomb radiocarbon method. Canadian Journal of Fisheries and Aquatic Sciences 62, 1060–1066.
| Age validation of canary rockfish (Sebastes pinniger) from off the Oregon coast (USA) using the bomb radiocarbon method.Crossref | GoogleScholarGoogle Scholar |
Rau, G. H., Ralston, S., Southon, J. R., and Chavez, F. P. (2001). Upwelling and the condition and diet of juvenile rockfish: a study using 14C, 13C, and 15N natural abundances. Limnology and Oceanography 46, 1565–1570.
| Upwelling and the condition and diet of juvenile rockfish: a study using 14C, 13C, and 15N natural abundances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsVSkurg%3D&md5=44ace072ed082345791d50d87afa1f59CAS |
Richardson, C. A. (2000). Molluscs as archives of environmental change. Oceanography and Marine Biology - an Annual Review 39, 103–164.
Roark, E. B., Guilderson, T. P., Dunbar, R. B., and Ingram, B. L. (2006). Radiocarbon based ages and growth rates: Hawaiian deep sea corals. Marine Ecology Progress Series 327, 1–14.
| Radiocarbon based ages and growth rates: Hawaiian deep sea corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjt1Sgtbc%3D&md5=f9e4ad4ed2d64e9e72bbe067024c9b60CAS |
Robinson, S. W. (1981). Natural and man-made radiocarbon as a tracer for coastal upwelling process. In ‘Coastal Upwelling.’ (Ed. F. A. Richards.) pp. 298–302. (American Geophysical Union: Washington, DC.)
Rogers-Bennett, L., and Leaf, R. T. (2006). Elasticity analyses of size-based red and white abalone matrix models: management and conservation. Ecological Applications 16, 213–224.
| Elasticity analyses of size-based red and white abalone matrix models: management and conservation.Crossref | GoogleScholarGoogle Scholar | 16705974PubMed |
Rogers-Bennett, L., Haaker, P. A., Huff, T. O., and Dayton, P. K. (2002). Estimating baseline abundances of abalone in California for restoration. California Cooperative Oceanic Fisheries Investigations Reports 43, 97–111.
Rogers-Bennett, L., Rogers, D. W., and Schultz, S. A. (2007). Modeling growth and mortality of red abalone (Haliotis rufescens) in northern California. Journal of Shellfish Research 26, 719–727.
| Modeling growth and mortality of red abalone (Haliotis rufescens) in northern California.Crossref | GoogleScholarGoogle Scholar |
Sainsbury, K. J. (1980). Effect of individual variability on the von Bertalanffy growth equation. Canadian Journal of Fisheries and Aquatic Sciences 37, 241–247.
| Effect of individual variability on the von Bertalanffy growth equation.Crossref | GoogleScholarGoogle Scholar |
Shepherd, S. A., and Avalos-Borja, M. (1997). The shell microstructure and chronology of the abalone Haliotis corrugata. Molluscan Research 18, 197–207.
Stewart, R. E. A., Campana, S. E., Jones, C. M., and Stewart, B. E. (2006). Bomb radiocarbon dating calculated beluga (Delphinapterus leucas) age estimates. Canadian Journal of Zoology 84, 1840–1852.
| Bomb radiocarbon dating calculated beluga (Delphinapterus leucas) age estimates.Crossref | GoogleScholarGoogle Scholar |
Stierhoff, K. L., Neuman, M., and Butler, J. L. (2012). On the road to extinction? Population declines of the endangered white abalone, Haliotis sorenseni. Biological Conservation 152, 46–52.
| On the road to extinction? Population declines of the endangered white abalone, Haliotis sorenseni.Crossref | GoogleScholarGoogle Scholar |
Stuiver, M., and Polach, H. A. (1977). Discussion: reporting of 14C data. Radiocarbon 19, 355–363.
Suarez, A. V., and Tsutsui, N. D. (2004). The value of museum collections for research and society. Bioscience 54, 66–74.
| The value of museum collections for research and society.Crossref | GoogleScholarGoogle Scholar |
Tegner, M. J., Breen, P. A., and Lennert, C. E. (1989). Population biology of red abalones, Haliotis rufescens, in southern California and management of the red and pink, H. corrugata, abalone fisheries. Fish Bulletin 87, 313–339.
Tutschulte, T. C., and Connell, J. H. (1988). Growth of three species of abalone (Haliotis) in southern California. The Veliger 31, 204–213.
Tutschulte, T. C. (1976). The comparative ecology of three sympatric abalones. Ph.D. Dissertation, University of California, San Diego, CA.
Watson, J. (2000). The effects of sea otters (Enhydra lutris) on abalone (Haliotis spp.) populations. In ‘Workshop on rebuilding abalone stocks in British Columbia.’ (Ed. A. Campbell.) Canadian Special Publication of Fisheries and Aquatic Sciences 130, 123–132.
Weidman, C. R., and Jones, G. A. (1993). A shell-derived time history of bomb 14C on Georges Bank and its Labrador Sea implications. Journal of Geophysical Research 98, 14 577–14 588.
| A shell-derived time history of bomb 14C on Georges Bank and its Labrador Sea implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXit1artrs%3D&md5=b937a7f1b6afacf25296fe0b5f9bfa3bCAS |
Williams, P. M., Roberstson, K. J., Soutar, A., Griffin, S. M., and Druffel, E. R. M. (1992). Isotopic signatures (14C, 13C, 15N) as tracers of sources and cycling of soluble and particulate organic matter in the Santa Monica Basin, California. Progress in Oceanography 30, 253–290.
| Isotopic signatures (14C, 13C, 15N) as tracers of sources and cycling of soluble and particulate organic matter in the Santa Monica Basin, California.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi, G. (1975). Estimating growth parameters from growth rate data: problems with marine sedentary invertebrates. Oecologia 20, 321–332.
| Estimating growth parameters from growth rate data: problems with marine sedentary invertebrates.Crossref | GoogleScholarGoogle Scholar |
