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Global biogeography of marine dispersal potential

Abstract

The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed. Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydrodynamics also covary with latitude—these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale. Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance. We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations. Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.

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Fig. 1: Factors affecting maximum dispersal distance across latitudes.
Fig. 2: Planktonic duration across egg sizes and temperatures.
Fig. 3: Planktonic duration across latitudes.
Fig. 4: Potential dispersal distance across latitudes.

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Data availability

Compiled data are available as Supplementary Information.

Code availability

All code is available at Github (https://github.com/MarianaAlvarezNoriega/Marine_invertebrate_dispersal).

References

  1. Benton, T. G. & Bowler, D. E. in Dispersal Ecology and Evolution (ed. Clobert, J.) 251–265 (Oxford Univ. Press, 2012).

  2. Gundersen, G., Johannesen, E., Andreassen, H. P. & Ims, R. A. Source–sink dynamics: how sinks affect demography of sources. Ecol. Lett. 4, 14–21 (2001).

    Google Scholar 

  3. Amarasekare, P. The role of density-dependent dispersal in source–sink dynamics. J. Theor. Biol. 226, 159–168 (2004).

    PubMed  Google Scholar 

  4. Brown, J. H. & Kodric-Brown, A. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58, 445–449 (1977).

    Google Scholar 

  5. Tilman, D. Competition and biodiversity in spatially structured habitats. Ecology 75, 2–16 (1994).

    Google Scholar 

  6. Levin, S., Muller-Landau, H., Ran, N. & Chave, J. The ecology and evolution of seed dispersal: a theoretical perspective. Annu. Rev. Ecol. Evol. Syst. 34, 575–604 (2003).

    Google Scholar 

  7. Palumbi, S. R. Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Syst. 25, 547–572 (1994).

    Google Scholar 

  8. Jeffery, C. H. & Emlet, R. B. Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the Tertiary of southern Australia. Evolution (N Y) 57, 1031–1048 (2003).

    Google Scholar 

  9. Bohonak, A. J. Dispersal, gene flow, and population structure. Q. Rev. Biol. 74, 21–45 (1999).

    CAS  PubMed  Google Scholar 

  10. Botsford, Hastings & Gaines Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecol. Lett. 4, 144–150 (2001).

    Google Scholar 

  11. Gaines, S. D., White, C., Carr, M. H. & Palumbi, S. R. Designing marine reserve networks for both conservation and fisheries management. Proc. Natl Acad. Sci. USA 107, 18286–18293 (2010).

    CAS  PubMed  Google Scholar 

  12. Haag, C. R., Saastamoinen, M., Marden, J. H. & Hanski, I. A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc. Biol. Sci. 272, 2449–2456 (2005).

    PubMed  PubMed Central  Google Scholar 

  13. Muller‐Landau, H. C., Wright, S. J., Calderón, O., Condit, R. & Hubbell, S. P. Interspecific variation in primary seed dispersal in a tropical forest. J. Ecol. 96, 653–667 (2008).

    Google Scholar 

  14. Uriarte, M. et al. Disentangling the drivers of reduced long‐distance seed dispersal by birds in an experimentally fragmented landscape. Ecology 92, 924–937 (2011).

    PubMed  Google Scholar 

  15. Janzen, D. H. Why mountain passes are higher in the tropics. Am. Naturalist. 101, 233–249 (1967).

    Google Scholar 

  16. Mittelbach, G. G. et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10, 315–331 (2007).

    PubMed  Google Scholar 

  17. Ghalambor, C. K., Huey, R. B., Martin, P. R., Tewksbury, J. J. & Wang, G. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr. Comp. Biol. 46, 5–17 (2006).

    PubMed  Google Scholar 

  18. Polato, N. R. et al. Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains. Proc. Natl Acad. Sci. USA 115, 12471 (2018).

    CAS  PubMed  Google Scholar 

  19. Brown, J. H. Why are there so many species in the tropics? J. Biogeogr. 41, 8–22 (2014).

    PubMed  Google Scholar 

  20. Brown, J. H. Why marine islands are farther apart in the Tropics. Am. Nat. 183, 842–846 (2014).

    PubMed  Google Scholar 

  21. O’Connor, M. I. et al. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc. Natl Acad. Sci. USA 104, 1266–1271 (2007).

    Google Scholar 

  22. Kelly, R. P. & Eernisse, D. J. Southern hospitality: a latitudinal gradient in gene flow in the marine environment. Evolution (N Y) 61, 700–707 (2007).

    CAS  Google Scholar 

  23. Marshall, D. J. & Álvarez-Noriega, M. Projecting marine developmental diversity and connectivity in future oceans. Phil. Trans. R. Soc. B (in the press).

  24. Powell, M. G. The latitudinal diversity gradient of brachiopods over the past 530 million years. J. Geol. 117, 585–594 (2009).

    Google Scholar 

  25. Mannion, P. D., Upchurch, P., Benson, R. B. J. & Goswami, A. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol. 29, 42–50 (2014).

    PubMed  Google Scholar 

  26. Yasuhara, M. et al. Cenozoic dynamics of shallow‐marine biodiversity in the Western Pacific. J. Biogeogr. 44, 567–578 (2017).

    Google Scholar 

  27. Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73 (2002).

    Google Scholar 

  28. Shanks, A. L., Grantham, B. A. & Carr, M. H. Propagule dispersal distance and the size and spacing of marine reserves. Ecol. Appl. 13, S159–S169 (2003).

    Google Scholar 

  29. Shanks, A. L. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216, 373–385 (2009).

    PubMed  Google Scholar 

  30. Kinlan, B. P. & Gaines, S. D. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84, 2007–2020 (2003).

    Google Scholar 

  31. Thorson, G. Rerproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 25, 1–45 (1950).

    CAS  PubMed  Google Scholar 

  32. Pearse, J. in Reproduction, Larval Biology and Recruitment of the Deep-Sea Benthos (eds Young, C. & Eckelbarger, K.) 26–44 (Columbia Univ. Press, 1994).

  33. Marshall, D. J., Krug, P. J., Kupriyanova, E. K., Byrne, M. & Emlet, R. B. The biogeography of marine invertebrate life histories. Annu. Rev. Ecol. Evol. Syst. 43, 97–114 (2012).

    Google Scholar 

  34. Ewers-Saucedo, C. & Pappalardo, P. Testing adaptive hypotheses on the evolution of larval life history in acorn and stalked barnacles. Ecol. Evol. 9, 11434–11447 (2019).

  35. Marshall, D. J. & Keough, M. J. The evolutionary ecology of offspring size in marine invertebrates. Adv. Mar. Biol. 53, 1–60 (2008).

    Google Scholar 

  36. Barneche, D. R., Burgess, S. C. & Marshall, D. J. Global environmental drivers of marine fish egg size. Glob. Ecol. Biogeogr. 27, 890–898 (2018).

    Google Scholar 

  37. Marshall, D. J. & Keough, M. J. Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size. Mar. Ecol. Prog. Ser. 255, 145–153 (2003).

    Google Scholar 

  38. Kohn, A. J. & Perron, F. E. Life History and Biogeography: Patterns in Conus (AbeBooks, 1994).

  39. Levitan, R. M. Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids. Am. Nat. 156, 175–192 (2000).

    PubMed  Google Scholar 

  40. Vance, R. R. On reproductive strategies in marine benthic invertebrates. Am. Nat. 107, 339–352 (1973).

    Google Scholar 

  41. Byers, J. E. & Pringle, J. M. Going against the flow: retention, range limits and invasions in advective environments. Mar. Ecol. Prog. Ser. 313, 27–41 (2006).

    Google Scholar 

  42. Pappalardo, P., Pringle, J. M., Wares, J. P. & Byers, J. E. The location, strength, and mechanisms behind marine biogeographic boundaries of the east coast of North America. Ecography (Cop.) 38, 722–731 (2015).

    Google Scholar 

  43. Halanych, K. M. & Mahon, A. R. Challenging dogma concerning biogeographic patterns of Antarctica and the Southern Ocean. Annu. Rev. Ecol. Evol. Syst. 49, 355–378 (2018).

    Google Scholar 

  44. Mercier, A., Sewell, M. A. & Hamel, J.-F. Pelagic propagule duration and developmental mode: reassessment of a fading link. Glob. Ecol. Biogeogr. 22, 517–530 (2013).

    Google Scholar 

  45. Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192–211 (2004).

    PubMed  Google Scholar 

  46. Albouy, C. et al. The marine fish food web is globally connected. Nat. Ecol. Evol. 3, 1153–1161 (2019).

    PubMed  Google Scholar 

  47. Chaudhary, C., Saeedi, H. & Costello, M. J. Bimodality of latitudinal gradients in marine species richness. Trends Ecol. Evol. 31, 670–676 (2016).

    PubMed  Google Scholar 

  48. Saeedi, H., Dennis, T. E. & Costello, M. J. Bimodal latitudinal species richness and high endemicity of razor clams (Mollusca). J. Biogeogr. 44, 592–604 (2017).

    Google Scholar 

  49. Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392–395 (2018).

    CAS  PubMed  Google Scholar 

  50. Chiu, W.-T. R. et al. Marine latitudinal diversity gradients, niche conservatism and out of the tropics and Arctic: climatic sensitivity of small organisms. J. Biogeogr. 47, 817–828 (2020).

    Google Scholar 

  51. Burgess, S. C., Baskett, M. L., Grosberg, R. K., Morgan, S. G. & Strathmann, R. R. When is dispersal for dispersal? Unifying marine and terrestrial perspectives. Biol. Rev. 91, 867–882 (2016).

    PubMed  Google Scholar 

  52. Pechenik, J. A. On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar. Ecol. Prog. Ser. 177, 269–297 (1999).

    Google Scholar 

  53. Pringle, J. M., Byers, J. E., Pappalardo, P., Wares, J. P. & Marshall, D. Circulation constrains the evolution of larval development modes and life histories in the coastal ocean. Ecology 95, 1022–1032 (2014).

    PubMed  Google Scholar 

  54. Houde, E. D. Fish early life dynamics and recruitment variability. Am. Fish. Soc. Symp. 2, 17–29 (1987).

    Google Scholar 

  55. Gillooly, J. F. & Dodson, S. I. The relationship of neonate mass and incubation temperature to embryonic development time in a range of animal taxa. J. Zool. 251, 369–375 (2000).

    Google Scholar 

  56. Bradbury, I. R., Laurel, B., Snelgrove, P. V. R., Bentzen, P. & Campana, S. E. Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc. Biol. Sci. 275, 1803–1809 (2008).

    PubMed Central  Google Scholar 

  57. Stobutzki, I. C. & Bellwood, D. R. Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar. Ecol. Prog. Ser. 149, 35–41 (1997).

    Google Scholar 

  58. Nanninga, G. B. & Manica, A. Larval swimming capacities affect genetic differentiation and range size in demersal marine fishes. Mar. Ecol. Prog. Ser. 589, 1–12 (2018).

    Google Scholar 

  59. Burgess, S. C. et al. Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected‐area design. Ecol. Appl. 24, 257–270 (2014).

    PubMed  Google Scholar 

  60. Hastings, A. & Botsford, L. W. Persistence of spatial populations depends on returning home. Proc. Natl Acad. Sci. USA 103, 6067–6072 (2006).

    CAS  PubMed  Google Scholar 

  61. Marshall, D. J. & Bolton, T. F. Effects of egg size on the development time of non-feeding larvae. Biol. Bull. 212, 6–11 (2007).

    PubMed  Google Scholar 

  62. Berrill, N. J. Studies in tunicate development. Part III. Differential retardation and acceleration. Phil. Trans. R. Soc. B 225, 255–326 (1935).

    Google Scholar 

  63. Queiroga, H. & Blanton, J. Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae. Adv. Mar. Biol. 47, 107–214 (2004).

    Google Scholar 

  64. Kingsford, M. J. Linear oceanographic features: a focus for research on recruitment processes. Aust. J. Ecol. 15, 391–401 (1990).

    Google Scholar 

  65. Largier, J. L. Considerations in estimating larval dispersal distances from oceanographic data. Ecol. Appl. 13, 71–89 (2003).

    Google Scholar 

  66. Cowen, R. K., Sponaugle, S., Paris, C. B. & Olson, D. B. Connectivity of marine populations: open or closed? Science 287, 857–859 (2000).

    CAS  PubMed  Google Scholar 

  67. Mitarai, S., Watanabe, H., Nakajima, Y., Shchepetkin, A. F. & McWilliams, J. C. Quantifying dispersal from hydrothermal vent fields in the western Pacific Ocean. Proc. Natl Acad. Sci. USA 113, 2976–2981 (2016).

    CAS  PubMed  Google Scholar 

  68. Becker, B. J., Levin, L. A., Fodrie, F. J. & McMillan, P. A. Complex larval connectivity patterns among marine invertebrate populations. Proc. Natl Acad. Sci. USA 104, 3267–3272 (2007).

    CAS  PubMed  Google Scholar 

  69. Jones, G. P., Milicich, M. J., Emslie, M. J. & Lunow, C. Self-recruitment in a coral reef fish population. Nature 402, 802–804 (1999).

    CAS  Google Scholar 

  70. Almany, G. R., Berumen, M. L., Thorrold, S. R., Planes, S. & Jones, G. P. Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744 (2007).

    CAS  PubMed  Google Scholar 

  71. Edmands, S. Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Mol. Ecol. 10, 1743–1750 (2001).

    CAS  PubMed  Google Scholar 

  72. Burgess, S. C., Treml, E. A. & Marshall, D. J. How do dispersal costs and habitat selection influence realized population connectivity? Ecology 93, 1378–1387 (2012).

    PubMed  Google Scholar 

  73. Lellouche, J.-M. et al. Recent updates to the Copernicus Marine Service global ocean monitoring and forecasting real-time 1/12° high-resolution system. Ocean Sci. 14, 1093–1126 (2018).

    Google Scholar 

  74. Laurindo, L. C., Mariano, A. J. & Lumpkin, R. An improved near-surface velocity climatology for the global ocean from drifter observations. Deep Sea Res. Part I Oceanogr. Res. Pap. 124, 73–92 (2017).

    Google Scholar 

  75. Lopez, M. & Clarke, A. The wind-driven shelf and slope water-flow in terms of a local and a remote response. J. Phys. Oceanogr. 19, 1091–1101 (1989).

    Google Scholar 

  76. Csanady, G. T. The arrested topographic wave. J. Phys. Oceanogr. 8, 47–62 (1978).

    Google Scholar 

  77. Bürkner, P.-C. brms: an R package for Bayesian multilevel models using stan. J. Stat. Softw. 80, 1–28 (2017).

    Google Scholar 

  78. Hoffman, M. D. & Gelman, A. The No-U-Turn sampler: adaptively setting path lengths in Hamiltonian Monte Carlo. J. Mach. Learn. Res. 15, 1593–1623 (2014).

    Google Scholar 

  79. Michonneau, F., Brown, J. W., Winter, D. J. & Fitzjohn, R. rotl: an R package to interact with the Open Tree of Life data. Methods Ecol. Evol. 7, 1476–1481 (2016).

    Google Scholar 

  80. Grafen, A. The phylogenetic regression. Phil. Trans. R. Soc. B 326, 119–157 (1989).

    CAS  PubMed  Google Scholar 

  81. Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).

    CAS  Google Scholar 

  82. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Google Scholar 

  83. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

  84. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

  85. Gabry, J. & Goodrich, B. rstantools: Tools for Developing R Packages Interfacing with ‘Stan’. R package version 2.0.0 https://cran.r-project.org/web/packages/rstantools/index.html (2018).

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Acknowledgements

We thank the Australian Research Council for financial support. We thank C. Cook, H. Ritchie, J. Burgin, K. Davis and M. Thompson for compiling the data. This study has been conducted using EU Copernicus Marine Service Information.

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D.J.M., S.C.B., J.E.B., J.M.P., J.P.W. and M.Á.-N. conceived the study. M.Á.-N. analysed the data and wrote the first draft, with help from D.J.M. and J.M.P. D.J.M., S.C.B., J.E.B., J.M.P., J.P.W. and M.Á.-N. contributed to subsequent drafts.

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Correspondence to Mariana Álvarez-Noriega.

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Extended data

Extended Data Fig. 1 Latitudinal gradients in egg size (predictions from the phylogenetically controlled model).

Panel a, Egg size (μm) of planktotrophic larvae across latitudes. Panel b, Egg size (μm) of lecithotrophic larvae across latitudes. The gradient from dark to light red shows large to small egg sizes. Note that the scale differs between panels. White circles show the distribution of studies from which data was obtained. Larger circles indicate a higher number of studies.

Extended Data Fig. 2 Probability that planktonic larvae are planktotrophic vs. lecithotrophic across latitudes (predictions from the phylogenetically controlled model).

The gradient from dark red to light red shows higher to lower probability that planktonic larvae are feeding. Grey circles (planktotrophic larvae) and triangles (lecithotrophic larvae) show the distribution of studies from which data was obtained. Larger shapes indicate a higher number of studies, which range from 1 to 26 for planktotrophic larvae and from 1 to 16 for lecithotrophic larvae.

Extended Data Fig. 3 Latitudinal gradients in planktonic duration (predictions from the phylogenetically controlled model).

Panel a, Planktonic duration (days) of planktotrophic larvae across latitudes. Panel b, Planktonic duration (days) of lecithotrophic larvae across latitudes. The gradient from dark to light red shows long to short planktonic durations. Note that the scale differs between panels. White circles show the distribution of studies from which data was obtained. Larger circles indicate a higher number of studies.

Extended Data Fig. 4 Predicted planktonic durations (days; log10-scale) across latitudes, weighted by the predicted proportion of each developmental mode and incorporating changes in egg size (predictions from phylogenetically controlled models).

The grey lines show predictions from 2000 random values from the models’ posterior distributions. The blue line shows median predictions and the blue ribbon shows the 95% credible interval.

Extended Data Fig. 5 Mean annual surface speed (ms−1).

Predictions obtained from the Mercator model73.

Extended Data Fig. 6 Mean annual surface speed (ms−1).

Data obtained from Laurindo et al.74

Extended Data Fig. 7

Proportional change in predicted dispersal distance with a 10% increase in the probability that a larva is planktotrophic (Panel a), a 10% increase in egg size (in log-scale) (Panel b), a 10% increase in the effect of temperature on planktonic duration (with absolute latitude as a proxy) (Panel c), and a 10% increase in mean annual surface speed (Panel d). White colour indicates areas where the proportional change in the predicted dispersal distance is equal to the proportional change in the dispersal driver of interest, blue colours show areas it is larger (that is a 10% increase in the driver of interest results in a > 10% increase in predicted dispersal distance), and red colours show areas where it is smaller (that is a 10% increase in the driver of interest results in a < 10% increase in predicted dispersal distance). Panel d used data from surface drifters74.

Extended Data Fig. 8 Ratio of the original predicted dispersal distance (with all dispersal drivers varying across latitudes) divided by the predicted dispersal distance for the case when one of the factors is kept constant across latitudes (at its mean value across latitudes 55°S to 55°N).

In panel a, the proportion of larvae being planktotrophic is kept constant; in panel b, the effect of egg size is kept constant; in panel c, the effect of planktonic duration is kept constant; and in panel d, mean annual current speed is kept at its mean across space. Blue colours show locations where dispersal would be underestimated if the dispersal driver of interest was assumed to stay constant across space (ratios > 1), red colours show locations where dispersal distance would be overestimated if the dispersal driver of interest was assumed to stay constant across space (ratios < 1). White areas show locations with ratios ≈1 (that is where the driver of interest occurs at its mean value). Panel d used data from surface drifters74.

Supplementary information

Supplementary Information

Sensitivity analysis. Results from phylogenetically uncontrolled models. Caveats. Temperature scaling on larval duration among species. Supplementary Figs. 1–9, Table 1, information and references.

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Supplementary Data

Compiled life-history data from Marshall et al.33.

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Álvarez-Noriega, M., Burgess, S.C., Byers, J.E. et al. Global biogeography of marine dispersal potential. Nat Ecol Evol 4, 1196–1203 (2020). https://doi.org/10.1038/s41559-020-1238-y

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