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Marine Biology

, 163:71 | Cite as

Reconstructing climate–growth relations from the teeth of a marine mammal

  • Talia A. Wittmann
  • Christopher Izzo
  • Zoë A. Doubleday
  • Jane McKenzie
  • Steven Delean
  • Bronwyn M. Gillanders
Original paper

Abstract

Sclerochronological analysis of growth increment patterns (growth layer groups; GLG) in marine mammal teeth offers a unique opportunity to reconstruct climate–growth relations of marine mammal populations over long time series. We developed sclerochronologies from GLG width measures in the cementum of male and female New Zealand fur seal (Arctocephalus forsteri) post-canine teeth collected from southern Australia. Tooth growth chronologies spanned 15 years and encompassed the period from 1987 to 2001. We also developed a rigorous analytical framework for assessing species suitability for sclerochronological analyses. Suitability assessments indicated that GLG clarity and relative width measures were variable among regions within individual teeth, and therefore, measurements were standardised to a consistent tissue type. Deposition of cementum in post-canine teeth was also correlated with body size, suggesting tooth growth measures were a suitable proxy of somatic growth. Inter-annual patterns of tooth growth were negatively correlated with mean annual sea surface temperature and the Southern Oscillation Index (both lagged by 1 year), but the strength of the relationships differed between the sexes. These results suggest both local- and regional-scale physical processes influence variations in growth and provide the first evidence of an environmental effect on cementum growth in a marine mammal. This study demonstrates the underutilised potential of marine mammal teeth to provide extended time series of growth, critical information which facilitates predictions of future ecological response to environmental change.

Keywords

Marine Mammal Southern Oscillation Index Southern Annular Mode Climate Predictor Indian Ocean Subtropical Dipole 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank the many field assistants and National Parks staff who helped with the original field study and the collection of teeth from live animals. Collection of teeth was approved by the Animal Ethics Committees at La Trobe University and the South Australian Department for Environment and Heritage (Permit Number Z24347) and funded by the Sea World Research and Rescue Foundation, Holsworth Wildlife Research Fund and South Australian National Parks and Wildlife Council Wildlife Conservation Fund. We also thank Gretchen Grammer, Chris Woodrow, the Playford Memorial Trust Inc. (Honours Scholarship to TW), the University of Adelaide (The David Murray Scholarship in Science to TW) and the Australian Research Council (FT100100767, DP110100716, LP120100228 to BMG).

Supplementary material

227_2016_2846_MOESM1_ESM.pdf (956 kb)
Supplementary material 1 (PDF 956 kb)

References

  1. Baker JD (1991) Trends in female northern fur seal, Callorhinus ursinus, feeding cycles indicated by nursing lines in juvenile male teeth. M.Sc. thesis, University of Washington, SeattleGoogle Scholar
  2. Baker JD, Fowler CW (1990) Tooth weights of juvenile male Northern fur seals, Callorhinus ursinus. Mar Mamm Sci 6:32–47CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-8, http://CRAN.R-project.org/package=lme4
  4. Baylis AMM, Page B, Goldsworthy SD (2008) Effect of seasonal changes in upwelling activity on the foraging locations of a wide-ranging central-place forager, the New Zealand fur seal. Can J Zool 86:774–789. doi: 10.1139/z08-055 CrossRefGoogle Scholar
  5. Blackwell GL, Basse SM, Dickman CR (2006) Measurement error associated with external measurements commonly used in small-mammal studies. J Mammal 87:216–223. doi: 10.1644/05-Mamm-a-215r1.1 CrossRefGoogle Scholar
  6. Boyd IL, Roberts JP (1993) Tooth growth in male Antarctic fur seals (Arctocephalus gazella) from South Georgia: an indicator of long-term growth history. J Zool 229:177–190CrossRefGoogle Scholar
  7. Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:R602–R614. doi: 10.1016/j.cub.2009.05.046 CrossRefGoogle Scholar
  8. Bureau of Meteorology (2012) Record-breaking La Niña events: an analysis of the La Niña life cycle and the impacts and significance of the 2010–11 and 2011–12 La Niña events in Australia. In: Bureau of Meteorology (ed). Bureau of Meteorology, Melbourne, VICGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  10. Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242CrossRefGoogle Scholar
  11. Core Team R (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  12. Croxall JP, Callaghan T, Cervellati R, Walton DWH (1992) Southern ocean environmental changes: effects on seabird, seal and whale populations. Philos Trans R Soc Lond B 338:319–328. doi: 10.1098/rstb.1992.0152 CrossRefGoogle Scholar
  13. Dellabianca NA, Hohn AA, Goodall RNP, Pousa JL, Macleod CD, Lima M (2012) Influence of climate oscillations on dentinal deposition in teeth of Commerson’s dolphin. Glob Change Biol 18:2477–2486. doi: 10.1111/j.1365-2486.2012.02707.x CrossRefGoogle Scholar
  14. Evans K, Kemper C, McKenzie J, McIntosh RR (2011) Age determination of marine mammals using tooth structure. The South Australian Museum, AdelaideGoogle Scholar
  15. Forcada J, Trathan PN, Reid K, Murphy EJ (2005) The effects of global climate variability in pup production of Antarctic fur seals. Ecology 86:2408–2417. doi: 10.1890/04-1153 CrossRefGoogle Scholar
  16. Gibbens J, Arnould YPJ (2009) Age-specific growth, survival, and population dynamics of female Australian fur seals. Can J Zool 87:902–911. doi: 10.1139/Z09-080 CrossRefGoogle Scholar
  17. Gillanders BM, Black BA, Meekan MG, Morrison MA (2012) Climatic effects on the growth of a temperate reef fish from the Southern Hemisphere: a biochronological approach. Mar Biol 159:1327–1333. doi: 10.1007/s00227-012-1913-x CrossRefGoogle Scholar
  18. Goldsworthy SD, Page B (2007) A risk-assessment approach to evaluating the significance of seal bycatch in two Australian fisheries. Biol Conserv 139:269–285CrossRefGoogle Scholar
  19. Hamilton V, Evans K, Raymond B, Hindell MA (2013) Environmental influences on tooth growth in sperm whales from southern Australia. J Exp Mar Biol Ecol 446:236–244CrossRefGoogle Scholar
  20. Hanson NN, Wurster CM, Bird MI, Reid K, Boyd IL (2009) Intrinsic and extrinsic forcing in life histories: patterns of growth and stable isotopes in male Antarctic fur seal teeth. Mar Ecol Prog Ser 388:263–272. doi: 10.3354/Meps08158 CrossRefGoogle Scholar
  21. Harcourt RG (2001) Advances in New Zealand mammalogy 1990–2000: Pinnipeds. J R Soc N Z 31:135–160CrossRefGoogle Scholar
  22. Harwood J (2001) Marine mammals and their environment in the twenty-first century. J Mammal 82:630–640. doi: 10.1644/1545-1542(2001)082<0630:MMATEI>2.0.CO;2 CrossRefGoogle Scholar
  23. Harwood J, Prime JH (1978) Some factors affecting the size of British grey seal populations. J Appl Ecol 15:401–411CrossRefGoogle Scholar
  24. Helama S, Schoene BR, Black BA, Dunca E (2006) Constructing long-term proxy series for aquatic environments with absolute dating control using a sclerochronological approach: introduction and advanced applications. Mar Freshw Res 57:591–599. doi: 10.1071/mf05176 CrossRefGoogle Scholar
  25. Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F, Hill KL, Holbrook NJ, Hosie GW, Last PR, Ling SD, Melbourne-Thomas J, Miller K, Pecl GT, Richardson AJ, Ridgway KR, Rintoul SR, Ritz DA, Ross DJ, Sanderson JC, Shepherd SA, Slotwinski A, Swadling KM, Taw N (2011) Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Biol Ecol 400:17–32. doi: 10.1016/j.jembe.2011.02.032 CrossRefGoogle Scholar
  26. Kampf J, Doubell M, Griffin D, Matthews RL, Ward TM (2004) Evidence of a large scale seasonal coastal upwelling system along the southern shelf of Australia. Geophys Res Lett 31:1–4CrossRefGoogle Scholar
  27. Kirkwood R, Goldsworthy SD (2013) Fur seals and sea lions. CSIRO Publishing, CollingwoodGoogle Scholar
  28. Klevezal’ GA (1980) Layers in the hard tissues of mammals as a record of growth rhythms of individuals. Rep Int Whal Comm Spec Issue 3:89–94Google Scholar
  29. Klevezal’ GA, Stewart BS (1994) Patterns and calibration of layering in tooth cementum of female Northern elephant seals, Mirounga angustirostris. J Mammal 75:483–487CrossRefGoogle Scholar
  30. Knox TC, Stuart-Williams H, Warneke RM, Hoskins AJ, Arnould JPY (2014) Analysis of growth and stable isotopes in teeth of male Australian fur seals reveals interannual variability in prey resources. Mar Mamm Sci 30:763–781CrossRefGoogle Scholar
  31. Learmonth JA, Macleod CD, Santos MB, Pierce GJ, Crick HQP, Robinson RA (2006) Potential effects of climate change on marine mammals. Oceanogr Mar Biol 44:431–464Google Scholar
  32. Li J, Xie SP, Cook ER, Huang G, D’Arrigo R, Liu F, Ma J, Zheng X-T (2011) Interdecadal modulation of El Niño amplitude during the past millennium. Nat Clim Change 1:114–118CrossRefGoogle Scholar
  33. Lieberman DE (1994) The biological basis for seasonal increments in dental cementum and their application to archaeological research. J Archaeol Sci 21:525–539. doi: 10.1006/jasc.1994.1052 CrossRefGoogle Scholar
  34. Lieberman DE, Meadow RH (1992) The biology of cementum increments (with an archaeological application). Mamm Rev 22:57–77. doi: 10.1111/j.1365-2907.1992.tb00120.x CrossRefGoogle Scholar
  35. Lough J, Gupta A, Hobday AJ (2012) Temperature. In: Poloczanska ES, Hobday A, Richardson AJ (eds) A marine climate change impacts and adaptation report card for Australia 2012. http://www.oceanclimatechange.org.au/. ISBN: 978-0-643-10928-5
  36. Manzanilla S (1989) The 1982–1983 El Niño event recorded in dentinal growth layers in teeth of Peruvian dusky dolphins (Lagenorhynchus obscurus). Can J Zool 67:2120–2125CrossRefGoogle Scholar
  37. Marshall GJ (2003) Trends in the Southern Annular Mode from observations and reanalyses. J Clim 16:4134–4143CrossRefGoogle Scholar
  38. Matta ME, Black BA, Wilderbuer TK (2010) Climate-driven synchrony in otolith growth-increment chronologies for three Bering Sea flatfish species. Mar Ecol Prog Ser 413:137–145. doi: 10.3354/meps08689 CrossRefGoogle Scholar
  39. McIntosh RR, Arthure AD, Dennis TE, Berris M, Goldsworthy SD, Shaughnessy PD, Teixeira CEP (2013) Survival estimates for the Australian sea lion: negative correlation of sea surface temperature with cohort survival to weaning. Mar Mamm Sci 29:84–108. doi: 10.1111/j.1748-7692.2011.00558.x CrossRefGoogle Scholar
  40. McKenzie J, Parry LJ, Page B, Goldsworthy SD (2005) Estimation of pregnancy rates and reproductive failure in New Zealand fur seals (Arctocephalus forsteri). J Mammal 86:1237–1246CrossRefGoogle Scholar
  41. McKenzie J, Page B, Goldsworthy SD, Hindell MA (2007a) Growth strategies of New Zealand fur seals in southern Australia. J Zool 272:377–389. doi: 10.1111/j.1469-7998.2006.00278.x CrossRefGoogle Scholar
  42. McKenzie J, Page B, Shaughnessy PD, Hindell MA (2007b) Age and reproductive maturity of New Zealand fur seals (Arctocephalus forsteri) in southern Australia. J Mammal 88:639–648. doi: 10.1644/06-Mamm-a-150r1.1 CrossRefGoogle Scholar
  43. McLeod DJ, Hobday AJ, Lyle JM, Welsford DC (2012) A prey-related shift in the abundance of small pelagic fish in eastern Tasmania? ICES J Mar Sci 69:953–960. doi: 10.1093/icesjms/fss069 CrossRefGoogle Scholar
  44. Medill S, Derocher AE, Stirling I, Lunn N, Moses RA (2009) Estimating cementum annuli width in polar bears: identifying sources of variation and error. J Mammal 90:1256–1264. doi: 10.1644/08-Mamm-a-186.1 CrossRefGoogle Scholar
  45. Medill S, Derocher AE, Stirling I, Lunn N (2010) Reconstructing the reproductive history of female polar bears using cementum patterns of premolar teeth. Polar Biol 33:115–124. doi: 10.1007/s00300-009-0689-z CrossRefGoogle Scholar
  46. Morrongiello JR, Crook DA, King AJ, Ramsey DSL, Brown P (2011) Impacts of drought and predicted effects of climate change on fish growth in temperate Australian lakes. Glob Change Biol 17:745–755. doi: 10.1111/j.1365-2486.2010.02259.x CrossRefGoogle Scholar
  47. Morrongiello JR, Thresher RE, Smith DC (2012) Aquatic biochronologies and climate change. Nat Clim Change 2:849–857. doi: 10.1038/Nclimate1616 CrossRefGoogle Scholar
  48. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  49. Nieblas A, Sloyan BM, Hobday AJ, Coleman R, Richardson AJ (2009) Variability of biological production in low wind-forced regional upwelling systems: a case study off southeastern Australia. Limnol Oceanogr 54:1548–1558CrossRefGoogle Scholar
  50. Page B, McKenzie J, Goldsworthy SD (2005) Dietary resource partitioning among sympatric New Zealand and Australian fur seals. Mar Ecol Prog Ser 293:283–302CrossRefGoogle Scholar
  51. Page B, McKenzie J, Sumner MD, Coyne M, Goldsworthy SD (2006) Spatial separation of foraging habitats among New Zealand fur seals. Mar Ecol Prog Ser 323:263–279. doi: 10.3354/meps323263 CrossRefGoogle Scholar
  52. Poloczanska E, Babcock R, Butler A, Hobday A, Hoegh-Guldberg O, Kunz T, Matear R, Milton D, Okey T, Richardson A (2007) Climate change and Australian marine life. Oceanogr Mar Biol 45:407Google Scholar
  53. Rayner NA, Parker DE, Horton EB, Folland CK, Alexander LV, Rowell DP, Kent EC, Kaplan A (2003) Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J Geophys Res 108:1–22CrossRefGoogle Scholar
  54. Scheffer VB, Myrick AC (1980) A review of studies to 1970 of growth layers in the teeth of marine mammals. Rep Int Whal Comm Spec Issue 3:51–63Google Scholar
  55. Scheffer VB, Peterson RS (1967) Growth layers in teeth of suckling fur seals. Growth 31:35–38Google Scholar
  56. Schumann N, Gales NJ, Harcourt RG, Arnould JPY (2013) Impacts of climate change on Australian marine mammals. Aust J Zool 61:146–159. doi: 10.1071/ZO12131 CrossRefGoogle Scholar
  57. Shaughnessy P, Dennis T (2001) Research on New Zealand fur seals and Australian sea lions in South Australia, 2000–2001. Report to National Parks and Wildlife South Australia, Department for Environment and Heritage. CSIRO, Canberra, AustraliaGoogle Scholar
  58. Von Biela VR, Testa JW, Gill VA, Burns JM (2008) Evaluating cementum to determine past reproduction in Northern Sea otters. J Wildl Manag 72:618–624. doi: 10.2193/2007-218 CrossRefGoogle Scholar
  59. Walther G, Post E, Convey P, Menzels A, Parmesan C, Beebee TJC, Fromentin J, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  60. Ward TM, McLeay LJ, Dimmlich WF, Rogers P, McClatchie S, Matthews R, Kampf J, Van Ruth PD (2006) Pelagic ecology of a northern boundary current system: effects of upwelling on the production and distribution of sardine (Sardinops sagax), anchovy (Engraulis australis) and southern bluefin tuna (Thunnus maccoyii) in the Great Australian Bight. Fish Oceanogr 15:191–207CrossRefGoogle Scholar
  61. Weisberg S, Spangler G, Richmond LS (2010) Mixed effects models for fish growth. Can J Fish Aquat Sci 67:269–277. doi: 10.1139/F09-181 CrossRefGoogle Scholar
  62. Wilson JA, Vigliola L, Meekan MG (2009) The back-calculation of size and growth from otoliths: validation and comparison of models at an individual level. J Exp Mar Biol Ecol 368:9–21CrossRefGoogle Scholar
  63. Young JW, Jordan AR, Bobbi C, Johannes RE, Haskard K, Pullen G (1993) Seasonal and interannual variability in krill (Nyctiphanes australis) stocks and their relationship to the fishery for jack mackerel (Trachurus declivis) off eastern Tasmania, Australia. Mar Biol 116:9–18. doi: 10.1007/BF00350726 CrossRefGoogle Scholar
  64. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, BerlinCrossRefGoogle Scholar
  65. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Southern Seas Ecology Laboratories, School of Biological SciencesThe University of AdelaideAdelaideAustralia
  2. 2.SemaphoreAustralia
  3. 3.School of Biological SciencesThe University of AdelaideAdelaideAustralia

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