in

Climate change threatens unique evolutionary diversity in Australian kelp refugia

  • Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. 113(48), 13785–13790. https://doi.org/10.1073/pnas.1606102113 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wernberg, T. et al. Biology and ecology of the globally significant kelp Ecklonia radiata. Oceanogr. Mar. Biol. https://doi.org/10.1201/9780429026379-6 (2019).

    Article 

    Google Scholar 

  • Bennett, S. et al. The ‘Great Southern Reef’: Social, ecological and economic value of Australia’s neglected kelp forests. Mar. Freshw. Res. 67(1), 47–56. https://doi.org/10.1071/MF15232 (2015).

    Article 

    Google Scholar 

  • Eger, A. et al. The economic value of fisheries, blue carbon, and nutrient cycling in global marine forests. EcoEvoRxiv. https://doi.org/10.32942/osf.io/n7kjs (2021).

    Article 

    Google Scholar 

  • Smith, K. E. et al. Socioeconomic impacts of marine heatwaves: Global issues and opportunities. Science 374, 6566. https://doi.org/10.1126/science.abj3593 (2021).

    Article 
    CAS 

    Google Scholar 

  • Coleman, M. et al. Loss of a globally unique kelp forest and genetic diversity from the northern hemisphere. Sci. Rep. 12, 5020. https://doi.org/10.1038/s41598-022-08264-3 (2022).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Vergés, A. et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl. Acad. Sci. 113(48), 13791–13796. https://doi.org/10.1073/pnas.1610725113 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353(6295), 169–172. https://doi.org/10.1126/science.aad8745 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wood, G. et al. Genomic vulnerability of a dominant seaweed points to future-proofing pathways for Australia’s underwater forests. Glob. Change Biol. 27(10), 2200–2212. https://doi.org/10.1111/gcb.15534 (2021).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Vranken, S. et al. Genotype-environment mismatch of kelp forests under climate change. Mol. Ecol. 30(15), 3730. https://doi.org/10.1111/mec.15993 (2021).

    Article 

    Google Scholar 

  • Assis, J. et al. Deep reefs are climatic refugia for genetic diversity of marine forests. J. Biogeogr. 43(4), 833–844. https://doi.org/10.1111/jbi.12677 (2016).

    Article 

    Google Scholar 

  • Lourenço, C. R. et al. Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. J. Biogeogr. 43(8), 1595–1607. https://doi.org/10.1111/jbi.12744 (2016).

    Article 

    Google Scholar 

  • Graham, M. H., Kinlan, B. P., Druehl, L. D., Garske, L. E. & Banks, S. Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc. Natl. Acad. Sci. 104(42), 16576–16580. https://doi.org/10.1073/pnas.0704778104 (2007).

    Article 
    ADS 

    Google Scholar 

  • Marzinelli, E. M. et al. Large-scale geographic variation in distribution and abundance of Australian deep-water kelp forests. PLoS ONE 10, e0118390. https://doi.org/10.1371/journal.pone.0118390 (2015).

    Article 
    CAS 

    Google Scholar 

  • Coleman, M. A. et al. Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. J. Ecol. 99(4), 1026–1032. https://doi.org/10.1111/j.1365-2745.2011.01822.x (2011).

    Article 

    Google Scholar 

  • Hampe, A. & Petit, R. J. Conserving biodiversity under climate change: The rear edge matters. Ecol. Lett. 8(5), 461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x (2005).

    Article 

    Google Scholar 

  • Maggs, C. A. et al. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89(sp11), S108–S122. https://doi.org/10.1890/08-0257.1 (2008).

    Article 

    Google Scholar 

  • Grant, W. S., Lydon, A. & Bringloe, T. T. Phylogeography of split kelp Hedophyllum nigripes: Northern ice-age refugia and trans-Arctic dispersal. Polar Biol. 43, 1829–1841. https://doi.org/10.1007/s00300-020-02748-6 (2020).

    Article 

    Google Scholar 

  • Hoarau, G., Coyer, J. A., Veldsink, J. H., Stam, W. T. & Olsen, J. L. Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol. Ecol. 16(17), 3606–3616. https://doi.org/10.1111/j.1365-294X.2007.03408.x (2007).

    Article 
    CAS 

    Google Scholar 

  • Fraser, C. I., Nikula, R., Spencer, H. G. & Waters, J. M. Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc. Natl. Acad. Sci. 106(9), 3249–3253. https://doi.org/10.1073/pnas.0810635106 (2009).

    Article 
    ADS 

    Google Scholar 

  • Assis, J. et al. Past climate changes and strong oceanographic barriers structured low-latitude genetic relics for the golden kelp Laminaria ochroleuca. J. Biogeogr. 45(10), 2326–2336. https://doi.org/10.1111/jbi.13425 (2018).

    Article 

    Google Scholar 

  • Gersonde, R., Crosta, X., Abelmann, A. & Armand, L. Sea-surface temperature and sea ice distribution of the Southern Ocean at the EPILOG last glacial maximum—A circum-Antarctic view based on siliceous microfossil records. Quat. Sci. Rev. 24(7–9), 869–896. https://doi.org/10.1016/j.quascirev.2004.07.015 (2005).

    Article 
    ADS 

    Google Scholar 

  • Bostock, H. C., Opdyke, B. N., Gagan, M. K., Kiss, A. E. & Fifield, L. K. Glacial/interglacial changes in the East Australian current. Clim. Dyn. 26, 645–659. https://doi.org/10.1007/s00382-005-0103-7 (2006).

    Article 

    Google Scholar 

  • Brooke, B. P., Nichol, S. L., Huang, Z. & Beaman, R. J. Palaeoshorelines on the Australian continental shelf: Morphology, sea-level relationship and applications to environmental management and archaeology. Cont. Shelf Res. 134, 26–38. https://doi.org/10.1016/j.csr.2016.12.012 (2017).

    Article 
    ADS 

    Google Scholar 

  • Williams, A. N., Ulm, S., Sapienza, T., Lewis, S. & Turney, C. S. M. Sea-level change and demography during the last glacial termination and early Holocene across the Australian continent. Quat. Sci. Rev. 182, 144–154. https://doi.org/10.1016/j.quascirev.2017.11.030 (2018).

    Article 
    ADS 

    Google Scholar 

  • Durrant, H. M. S., Barrett, N. S., Edgar, G. J., Coleman, M. A. & Burridge, C. P. Shallow phylogeographic histories of key species in a biodiversity hotspot. Phycologia 54(6), 556–565. https://doi.org/10.2216/15-24.1 (2015).

    Article 

    Google Scholar 

  • O’Hara, T. D. & Poore, G. C. B. Patterns of distribution for southern Australian marine echinoderms and decapods. J. Biogeogr. 27(6), 1321–1335. https://doi.org/10.1046/j.1365-2699.2000.00499.x (2000).

    Article 

    Google Scholar 

  • Waters, J. M. Marine biogeographical disjunction in temperate Australia: Historical landbridge, contemporary currents, or both? Divers. Distrib. 14(4), 692–700. https://doi.org/10.1111/j.1472-4642.2008.00481.x (2008).

    Article 

    Google Scholar 

  • Davis, T. R., Champion, C. & Coleman, M. A. Climate refugia for kelp within an ocean warming hotspot revealed by stacked species distribution modelling. Mar. Environ. Res. 166, 105267. https://doi.org/10.1016/j.marenvres.2021.105267 (2021).

    Article 
    CAS 

    Google Scholar 

  • Barrows, T. T. & Juggins, S. Sea-surface temperatures around the Australian margin and Indian Ocean during the last glacial maximum. Quat. Sci. Rev. 24(7–9), 1017–1047. https://doi.org/10.1016/j.quascirev.2004.07.020 (2005).

    Article 
    ADS 

    Google Scholar 

  • Richmond, S. & Stevens, T. Classifying benthic biotopes on sub-tropical continental shelf reefs: How useful are abiotic surrogates? Estuar. Coast. Shelf Sci. 138, 79–89. https://doi.org/10.1016/j.ecss.2013.12.012 (2014).

    Article 
    ADS 

    Google Scholar 

  • Jordan, A. et al. Seabed Habitat Mapping of the Continental Shelf of NSW (New South Wales Department of Environment, Climate Change and Water, 2010).

    Google Scholar 

  • Lewis, S. E., Sloss, C. R., Murray-Wallace, C. V., Woodroffe, C. D. & Smithers, S. G. Post-glacial sea-level changes around the Australian margin: A review. Quat. Sci. Rev. 74, 115–138. https://doi.org/10.1016/j.quascirev.2012.09.006 (2013).

    Article 
    ADS 

    Google Scholar 

  • Millar, A. J. K. Marine benthic algae of Norfolk island, South Pacific. Aust. Syst. Bot. 12(4), 479–547. https://doi.org/10.1071/SB98004 (1999).

    Article 

    Google Scholar 

  • Ridgway, K. R. & Dunn, J. R. Mesoscale structure of the mean East Australian current system and its relationship with topography. Prog. Oceanogr. 56, 189–222. https://doi.org/10.1016/S0079-6611(03)00004-1 (2003).

    Article 
    ADS 

    Google Scholar 

  • Lough, J. M. & Hobday, A. J. Observed climate change in Australian marine and freshwater environments. Mar. Freshw. Res. 62(9), 984–999. https://doi.org/10.1071/MF10272 (2011).

    Article 

    Google Scholar 

  • Sunday, J. M. et al. Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot. Ecol. Lett. 18(9), 944–953. https://doi.org/10.1111/ele.12474 (2015).

    Article 

    Google Scholar 

  • Coleman, M. A. et al. Variation in the strength of continental boundary currents determines patterns of large-scale connectivity in kelp. J. Ecol. 99, 1026–1032 (2011).

    Article 

    Google Scholar 

  • Maeda, T., Kawai, T., Nakaoka, M. & Yotsukura, N. Effective DNA extraction method for fragment analysis using capillary sequencer of the kelp, Saccharina. J. Appl. Phycol. 25, 337–347. https://doi.org/10.1007/s10811-012-9868-3 (2013).

    Article 
    CAS 

    Google Scholar 

  • Lane, C. E., Lindstrom, S. C. & Saunders, G. W. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenet. Evol. 44(2), 634–648. https://doi.org/10.1016/j.ympev.2007.03.016 (2007).

    Article 
    CAS 

    Google Scholar 

  • Saunders, G. W. & McDevit, D. C. Acquiring DNA sequence data from dried archival red algae (Florideophyceae) for the purpose of applying available names to contemporary genetic species: A critical assessment. Botany 90, 191–203 (2012).

    Article 
    CAS 

    Google Scholar 

  • Kearse, M. et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).

    Article 

    Google Scholar 

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340 (2004).

    Article 
    CAS 

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215(3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 (1990).

    Article 
    CAS 

    Google Scholar 

  • Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34(12), 3299–3302. https://doi.org/10.1093/molbev/msx248 (2017).

    Article 
    CAS 

    Google Scholar 

  • Clement, M., Posada, D. & Crandall, K. A. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9(10), 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x (2000).

    Article 
    CAS 

    Google Scholar 

  • Leigh, J. & Bryant, D. PopART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6(9), 1110–1116. https://doi.org/10.1111/2041-210X.12410 (2015).

    Article 

    Google Scholar 

  • Inkscape Project. Inkscape Project. https://inkscape.org/ (2020).

  • Coleman, M. A. et al. Connectivity within and among a network of temperate marine reserves. PLoS ONE 6(5), e20168. https://doi.org/10.1371/journal.pone.0020168 (2011).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Davis, T. R., Cadiou, G., Champion, C. & Coleman, M. A. Environmental drivers and indicators of change in habitat and fish assemblages within a climate change hotspot. Reg. Mar. Stud. https://doi.org/10.1016/j.rsma.2020.101295 (2020).

    Article 

    Google Scholar 

  • Mix, A. C., Bard, E. & Schneider, R. Environmental processes of the ice age: Land, oceans, glaciers (EPILOG). Quat. Sci. Rev. 20(4), 627–657. https://doi.org/10.1016/S0277-3791(00)00145-1 (2001).

    Article 
    ADS 

    Google Scholar 

  • Waters, J. M. Competitive exclusion: Phylogeography’s ‘elephant in the room’? Mol. Ecol. 20(21), 4388–4394. https://doi.org/10.1111/j.1365-294X.2011.05286.x (2011).

    Article 

    Google Scholar 

  • Cresswell, G. R., Peterson, J. L. & Pender, L. F. The East Australian current, upwellings and downwellings off eastern-most Australia in summer. Mar. Freshw. Res. 68(7), 1208–1223. https://doi.org/10.1071/MF16051 (2016).

    Article 

    Google Scholar 

  • Hewitt, G. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58(3), 247–276. https://doi.org/10.1006/bijl.1996.0035 (1995).

    Article 

    Google Scholar 

  • Waters, J. M., Fraser, C. I. & Hewitt, G. M. Founder takes all: Density-dependent processes structure biodiversity. Trends Ecol. Evol. 28(2), 78–85. https://doi.org/10.1016/j.tree.2012.08.024 (2013).

    Article 

    Google Scholar 

  • Wernberg, T. et al. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep. 8(1851), 1–8. https://doi.org/10.1038/s41598-018-20009-9 (2018).

    Article 
    CAS 

    Google Scholar 

  • Coleman, M. A. & Kelaher, B. P. Connectivity among fragmented populations of a habitat-forming alga, Phyllospora comosa (Phaeophyceae, Fucales) on an urbanised coast. Mar. Ecol. Prog. Ser. 381, 63–70 (2009).

    Article 
    ADS 

    Google Scholar 

  • Drábková, L. Z. DNA extraction from herbarium specimens. In Molecular Plant Taxonomy. Methods in Molecular Biology Vol. 1115 (ed. Besse, P.) (Humana Press, 2014).

    Google Scholar 

  • Goff, L. J. & Moon, D. A. PCR amplification of nuclear and plastid genes from algal herbarium specimens and algal spores 1. J. Phycol. 29, 381 (1993).

    Article 
    CAS 

    Google Scholar 

  • Nahor, O., Luzzatto-Knaan, T. & Israel, A. A new genetic lineage of Asparagopsis taxiformis (Rhodophyta) in the Mediterranean Sea: As the DNA barcoding indicates a recent Lessepsian introduction. Front. Mar. Sci. https://doi.org/10.3389/fmars.2022.873817 (2022).

    Article 

    Google Scholar 

  • Coleman, M. A. & Brawley, S. H. Variability in temperature and historical patterns in reproduction in the Fucus distichus complex (Heterokontophyta; Phaeophyceae): Implications for speciation and collection of herbarium specimens. J. Phycol. 41, 1110–1119 (2005).

    Article 

    Google Scholar 

  • Martins, N. et al. Hybrid vigour for thermal tolerance in hybrids between the allopatric kelps Laminaria digitata and L. pallida (Laminariales, Phaeophyceae) with contrasting thermal affinities. Eur. J. Phys. 54(4), 548–561 (2019).

    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

    Schooling behavior driven complexities in a fear-induced prey–predator system with harvesting under deterministic and stochastic environments

    Multifunctionality of temperate alley-cropping agroforestry outperforms open cropland and grassland