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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

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, Seattle

  2. Baker JD, Fowler CW (1990) Tooth weights of juvenile male Northern fur seals, Callorhinus ursinus. Mar Mamm Sci 6:32–47

    Article  Google 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

    Article  Google 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

    Article  Google 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 229:177–190

    Article  Google 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

    CAS  Article  Google 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, VIC

  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google 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 59:197–242

    Article  Google Scholar 

  11. Core Team R (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google 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

    Article  Google 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

    Article  Google Scholar 

  14. Evans K, Kemper C, McKenzie J, McIntosh RR (2011) Age determination of marine mammals using tooth structure. The South Australian Museum, Adelaide

    Google 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

    Article  Google 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

    Article  Google 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

    Article  Google Scholar 

  18. Goldsworthy SD, Page B (2007) A risk-assessment approach to evaluating the significance of seal bycatch in two Australian fisheries. Biol Conserv 139:269–285

    Article  Google 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 446:236–244

    Article  Google 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

    CAS  Article  Google Scholar 

  21. Harcourt RG (2001) Advances in New Zealand mammalogy 1990–2000: Pinnipeds. J R Soc N Z 31:135–160

    Article  Google 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

    Article  Google Scholar 

  23. Harwood J, Prime JH (1978) Some factors affecting the size of British grey seal populations. J Appl Ecol 15:401–411

    Article  Google 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

    Article  Google 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

    Article  Google 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 31:1–4

    Article  Google Scholar 

  27. Kirkwood R, Goldsworthy SD (2013) Fur seals and sea lions. CSIRO Publishing, Collingwood

    Google 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 3:89–94

    Google Scholar 

  29. Klevezal’ GA, Stewart BS (1994) Patterns and calibration of layering in tooth cementum of female Northern elephant seals, Mirounga angustirostris. J Mammal 75:483–487

    Article  Google 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 30:763–781

    CAS  Article  Google 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 44:431–464

    Google 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 1:114–118

    CAS  Article  Google 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

    Article  Google 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

    Article  Google 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 67:2120–2125

    Article  Google Scholar 

  37. Marshall GJ (2003) Trends in the Southern Annular Mode from observations and reanalyses. J Clim 16:4134–4143

    Article  Google 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

    Article  Google 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

    Article  Google 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 86:1237–1246

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google Scholar 

  47. Morrongiello JR, Thresher RE, Smith DC (2012) Aquatic biochronologies and climate change. Nat Clim Change 2:849–857. doi:10.1038/Nclimate1616

    Article  Google 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 4:133–142

    Article  Google 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 54:1548–1558

    Article  Google Scholar 

  50. Page B, McKenzie J, Goldsworthy SD (2005) Dietary resource partitioning among sympatric New Zealand and Australian fur seals. Mar Ecol Prog Ser 293:283–302

    Article  Google 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

    Article  Google 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 45:407

    Google 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 108:1–22

    Article  Google 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 3:51–63

    Google Scholar 

  55. Scheffer VB, Peterson RS (1967) Growth layers in teeth of suckling fur seals. Growth 31:35–38

    CAS  Google 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

    Article  Google 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, Australia

  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

    Article  Google 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 416:389–395

    CAS  Article  Google 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 15:191–207

    Article  Google 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

    Article  Google 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 368:9–21

    Article  Google 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

    Article  Google Scholar 

  64. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin

    Book  Google Scholar 

  65. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

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).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Bronwyn M. Gillanders.

Additional information

Reviewed by Undisclosed experts.

Responsible Editor: G. Pierce.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 956 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wittmann, T.A., Izzo, C., Doubleday, Z.A. et al. Reconstructing climate–growth relations from the teeth of a marine mammal. Mar Biol 163, 71 (2016). https://doi.org/10.1007/s00227-016-2846-6

Download citation

Keywords

  • Marine Mammal
  • Southern Oscillation Index
  • Southern Annular Mode
  • Climate Predictor
  • Indian Ocean Subtropical Dipole