Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Teleconnections reveal that drivers of inter-annual growth can vary from local to ocean basin scales in tropical snappers

Abstract

Individual growth rate is one of the key traits that determine the productivity of populations. Chronological approaches that relate time series of growth and climate information present the opportunity to identify important climatic drivers of demography and thereby understand the likely impact of climate change. We constructed otolith chronologies (a proxy for somatic growth) to examine synchrony of growth patterns within and between two mesopredatory fishes (Lutjanus bohar and L. gibbus) in the remote Chagos Archipelago, Indian Ocean. We then used mixed-model and pathway analysis to relate growth responses to a suite of climatic and environmental factors to determine the extent to which variation in inter-annual growth could be predicted at individual and population levels. Our models explained up to half the variance associated with annual growth at the level of populations. Significant environmental drivers of growth differed between species, as did the spatial scale of these drivers: L. gibbus exhibited a strong relationship with regional ocean temperature, whereas growth of L. bohar was correlated with the Pacific Decadal Oscillation, suggesting influential teleconnections between ocean basins as an underlying predictor of productivity of fish populations. Our results demonstrate that (1) synchronous growth stemming from relationships with climate factors may be suppressed at very low latitudes; (2) closely related species may respond to very different environmental stimuli; and (3) within the same environment, the scale of influential drivers may be local in nature or reflect oceanographic processes stretching across entire ocean basins. We demonstrate that biochronological approaches are effective tools for reconstructing relationships between climate variability and fish growth even in tropical regions where seasonality is low, and these methods can be valuable for forecasting population-level responses to projected climate change.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alheit J, Bakun A (2010) Population synchronies within and between ocean basins: Apparent teleconnections and implications as to physical-biological linkage mechanisms. J Marine Syst 79:267–285

  2. Almany GR (2004) Does increased habitat complexity reduce predation and competition in coral reef assemblages? Oikos 106:275–284

  3. Barneche DR, Allen AP (2018) The energetics of fish growth and how it constrains food-web trophic structure. Ecol Lett 21:836–844. https://doi.org/10.1111/ele.12947

  4. Bartoń K (2018) Multi-model inference. R package version 1.42.1. Available at https://cran.r-project.org/web/packages/MuMIn/index.html

  5. Beamish RJ, Nevile C, Sweeting R, Lange K (2012) The synchronous failure of juvenile Pacific salmon and herring production in the Strait of Georgia in 2007 and the poor return of Sockeye salmon to the Fraser River in 2009. Mar Coast Fish 4:403–414

  6. Beukers JS, Jones GP (1998) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59

  7. Black BA, Boehlert GW, Yoklavich MM (2005) Using tree-ring crossdating techniques to validate annual growth increments in long-lived fishes. Can J Fish Aquat Sci 62:2277–2284

  8. Black BA, van der Sleen P, Di Lorenzo E, Griffin D, Sydeman WJ, Dunham JB, Rykaczewski RR, García-Reyes M, Safeeq M, Arismendi I, Bograd SJ (2018) Rising synchrony controls western North American ecosystems. Glob Change Biol 24:2305–2314

  9. Bœuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Phys C 130:411–423

  10. Bunn AG (2008) A dendrochronology program library in R (dpIR). Dendrochronologia 26:115–124

  11. Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at Risk Revisited. World Resource Institute, Washington, DC

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

  13. Campana SE (1990) How reliable are growth back-calculations based on otoliths? Can J Fish Aquat Sci 47:2219–2227

  14. Chambers D, Tapley B, Stewart R (1999) Anomalous warming in the Indian Ocean coincident with El Niño. J Geophys Res 104:3035–3047

  15. Cheung WWL, Sarmiento JL, Dunne J, Frölicher TL, Lam VWY, Palomares MLD, Watson R, Pauly D (2013) Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat Clim Change 3:254

  16. Clarke A (2017) Principles of Thermal Ecology: Temperature, Energy and Life. Oxford University Press, New York

  17. Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23:79–92

  18. Coker DJ, Pratchett MS, Munday PL (2009) Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav Ecol 20:1204–1210

  19. Cook ER (1985) A time series analysis approach to tree ring standardization. Ph.D. thesis, University of Arizona, p 164

  20. Feary DA, McCormick MI, Jones GP (2009) Growth of reef fishes in response to live coral cover. J Exp Mar Biol Ecol 373:45–49

  21. Feng M, Waite A, Thompson P (2009) Climate variability and ocean production in the Leeuwin Current system off the west coast of West Australia. Journal of the Royal Society of Western Australia 92:67–81

  22. Forchhammer MC, Post E (2004) Using large-scale climate indices in climate change ecology studies. Popul Ecol 46:1–12

  23. Grace JB, Scheiner SM, Schoolmaster DR (2015) Structural equation modeling: building and evaluating causal models. In: Fox GA, Negrete-Yanlelevich S, Sosa VJ (eds) Ecological Statistics: From Principles to Applications. Oxford University Press, New York, NY, pp 168–199

  24. Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree-Ring Res 57:205–221

  25. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. P Natl Acad Sci USA 103:14288–14293

  26. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018) Global warming transforms coral reef assemblages. Nature 556:492–496

  27. Jones GP (1986) Food availability affects growth in a coral reef fish. Oecologia 70:136–139

  28. Kilduff DP, Di Lorenzo E, Botsford LW, Teo SLH (2015) Changing central Pacific El Niños reduce stability of North American salmon survival rates. P Natl Acad Sci USA 112:10962–10966

  29. Kingsford M, Welch D, O’Callaghan M (2019) Latitudinal and cross-shelf patterns of size, age, growth, and mortality of a tropical damselfish Acanthochromis polyacanthus on the Great Barrier Reef. Diversity 11:67

  30. Kokita T, Nakazono A (2001) Rapid response of an obligately corallivorous filefish Oxymonacanthus longirostris (Monocanthidae) to a mass coral bleaching event. Coral Reefs 20:155–158

  31. Lefcheck JS (2016) PiecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579

  32. Liu Z, Alexander M (2007) Atmospheric bridge, oceanic tunnel, and global climatic teleconnections. Rev Geophys 45:34 pp

  33. Lorenzen K, Enberg K (2002) Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. P Roy Soc B-Biol Sci 269:49–54

  34. Marriott RJ, Mapstone BD, Begg GA (2007) Age-specific demographic parameters, and their implications for management of the red bass, Lutjanus bohar (Forsskål, 1775): a large tropical reef fish. Fish Res 83:204–215

  35. Martino JC, Fowler AJ, Doubleday ZA, Grammer GL, Gillanders BM (2019) Using otolith chronologies to understand long-term trends and extrinsic drivers of growth in fisheries. Ecosphere 10:e02553

  36. Moore BR (2019) Age-based life history of humpback red snapper, Lutjanus gibbus, in New Caledonia. J Fish Biol 95:1374–1384

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

  38. Munch SB, Salinas S (2009) Latitudinal variation in lifespan within species is explained by the metabolic theory of ecology. P Natl Acad Sci USA 106:13860–13864

  39. Munday PL, Jones GP, Pratchett MS, Williams AJ (2008) Climate change and the future for coral reef fishes. Fish Fish 9:261–285

  40. Nanami A, Kurihara T, Kurita Y, Aonuma Y, Suzuki N, Yamada H (2010) Age, growth and reproduction of the humpback red snapper Lutjanus gibbus off Ishigaki Island, Okinawa. Ichthyol Res 57:240–244

  41. Newman M, Alexander MA, Ault TR, Cobb KM, Deser C, Di Lorenzo E, Mantua NJ, Miller AJ, Minobe S, Nakamura H, Schneider N, Vimont DJ, Phillips AS, Scott JD, Smith CA (2016) The Pacific Decadal Oscillation, revisited. J Climate 29:4399–4427

  42. Nilsson GE, Crawley N, Lunde IG, Munday PL (2009) Elevated temperature reduces the respiratory scope of coral reef fishes. Glob Change Biol 15:1405–1412

  43. Ong JJL, Rountrey AN, Marriott RJ, Newman SJ, Meeuwig JJ, Meekan MG (2017) Cross-continent comparisons reveal differing environmental drivers of growth of the coral reef fish, Lutjanus bohar. Coral Reefs 36:195–206

  44. Ong JJL, Rountrey AN, Black BA, Nguyen HM, Coulson PG, Newman SJ, Wakefield CB, Meeuwig JJ, Meekan MG (2018) A boundary current drives synchronous growth of marine fishes across tropical and temperate latitudes. Glob Change Biol 24:1894–1903

  45. Pauly D, Cheung WWL (2018) Sound physiological knowledge and principles in modelling shrinking of fishing under climate change. Glob Change Biol 24:e15–e26

  46. Pratchett MS, Wilson SK, Berumen ML, McCormick MI (2004) Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23:352–356

  47. Pratchett MS, Munday PL, Graham NAJ, Kronen M, Pinca S, Friedman K, Brewer TD, Bell JD, Wilson SK, Cinner JE, Kinch JP, Lawton RJ, Williams AJ, Chapman L, Magron F, Webb A (2011) Vulnerability of coastal fisheries in the tropical Pacific to climate change. In: Bell JD, Johnson JE, Hobday AJ (eds) Vulnerability of Tropical Pacific Fisheries and Aquaculture to Climate Change. Secretariat of the Pacific Community, Noumea, New Caledonia, pp 493–576

  48. Rountrey AN (2009) Life histories of juvenile woolly mammoths from Siberia: stable isotope and elemental analyses of tooth dentin. Ph.D. thesis, The University of Michigan

  49. Rountrey AN, Coulson PG, Meeuwig JJ, Meekan M (2014) Water temperature and fish growth: otoliths predict growth patterns of a marine fish in a changing climate. Glob Change Biol 20:2450–2458

  50. Rowland EL, Davison JE, Graumlich LJ (2011) Approaches to evaluating climate change impacts on species: a guide to initiating the adaptation planning process. Environ Manage 47:322–337

  51. Roxy MK, Modi A, Murtugudde R, Valsala V, Panickal S, Kumar SP, Ravichandran M, Vichi M, Lévy M (2016) A reduction in marine primary productivity driven by rapid warming over the tropical Indian Ocean. Geophys Res Lett 43:826–833

  52. Rummer JL, Couturier CS, Stecyk JAW, Gardiner NM, Kinch JP, Nilsson GE, Munday PL (2014) Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob Change Biol 20:1055–1066

  53. Saji NH, Goswami BN, Vinayachandran PN, Yamagata T (1999) A dipole mode in the tropical Indian Ocean. Nature 401:360–363

  54. Seebacher F, White CR, Franklin CE (2015) Physiological plasticity increases resilience of ectothermic animals to climate change. Nat Clim Change 5:61–66

  55. Sheppard C, Sheppard A, Mogg A, Bayley D, Dempsey AC, Roche R, Turner J, Purkis S (2017) Coral bleaching and mortality in the Chagos Archipelago. Atoll Research Bulletin 613:26

  56. Shestakova TA, Gutiérrez E, Kirdyanov AV, Camarero JJ, Génova M, Knorre AA, Linares JC, de Dios VR, Sánchez-Salguero R, Voltas J (2016) Forests synchronize their growth in contrasting Eurasian regions in response to climate warming. P Natl Acad Sci USA 113:662–667

  57. Shipley B (2009) Confirmatory pathway analysis in a generalized multilevel context. Ecology 90:363–368

  58. Taylor BM, Oyafuso ZS, Pardee CB, Ochavillo D, Newman SJ (2018a) Comparative demography of commercially-harvested snappers and an emperor from American Samoa. PeerJ 6:e5069

  59. Taylor BM, Brandl SJ, Kapur M, Robbins WD, Johnson G, Huveneers C, Renaud P, Choat JH (2018b) Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99:642–651

  60. Taylor BM, Choat JH, DeMartini EE, Hoey AS, Marshell A, Priest MA, Rhodes KL, Meekan MG (2019) Demographic plasticity facilitates ecological and economic resilience in a commercially important reef fish. J Anim Ecol 88:1888–1900. https://doi.org/10.1111/1365-2656.13095

  61. Taylor BM, Benkwitt CE, Choat JH, Clements KD, Graham NAJ, Meekan MG (2020) Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching. Glob Change Biol. https://doi.org/10.1111/gcb.14909

  62. Tommasi D, Stock CA, Hobday AJ, Methot R, Kaplan IC, Eveson JP, Holsman K, Miller TJ, Gaichas S, Gehlen M, Pershing A, Vecchi GA, Msadek R, Delworth T, Eakin CM, Haltuch MA, Séférian R, Spillman CM, Hartog JR, Siedlecki S, Samhouri JF, Muhling B, Asch RG, Pinsky ML, Saba VS, Kapnick SB, Gaitan CF, Rykaczewski RR, Alexander MA, Xue Y, Pegion KV, Lynch P, Payne MR, Kristiansen T, Lehodey P, Werner FE (2017) Managing living marine resources in a dynamic environment: The role of seasonal to decadal climate forecasts. Prog Oceanogr 152:15–49

  63. Trenberth KE (1990) Recent observed interdecadal climate changes in the Northern Hemisphere. B Am Meteorol Soc 71:988–993

Download references

Acknowledgements

We thank S. Arklie and P. McDowell for assistance with logistics; C. Sheppard for providing access to historical rainfall data; and N. Graham, S. Brandl, J. Ong, and A. Rountrey for helpful discussions. We would like to thank the United Kingdom Foreign and Commonwealth Office and the British Indian Ocean Territory Administration for granting us permission to undertake the research. Funding for this project was provided by the Bertarelli Foundation (Grant No. BPMS 2017-7) and contributed to the Bertarelli Programme in Marine Science. We thank two anonymous reviewers for their constructive feedback on this manuscript.

Author information

Correspondence to Brett M. Taylor.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic editor Michael Lee Berumen

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1527 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Taylor, B.M., Chinkin, M. & Meekan, M.G. Teleconnections reveal that drivers of inter-annual growth can vary from local to ocean basin scales in tropical snappers. Coral Reefs (2020). https://doi.org/10.1007/s00338-020-01903-z

Download citation

Keywords

  • Biochronology
  • Climate variability
  • Teleconnection
  • Growth
  • Otolith
  • Chagos Archipelago