in

Climate change and species facilitation affect the recruitment of macroalgal marine forests

  • Intergovernmental Panel on Climate Change (IPCC). The Ocean and Cryosphere in a Changing Climate: Special Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2022). https://doi.org/10.1017/9781009157964.

  • Doney, S. C. et al. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4, 11–37 (2012).

    ADS 

    Google Scholar 

  • Gattuso, J.-P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).

    PubMed 

    Google Scholar 

  • Hall-Spencer, J. M. & Harvey, B. P. Ocean acidification impacts on coastal ecosystem services due to habitat degradation. Emerg. Top. Life Sci. 3, 197–206 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Straub, S. C. et al. Resistance, extinction, and everything in between—The diverse responses of seaweeds to marine heatwaves. Front. Mar. Sci. 6, 763 (2019).

    Google Scholar 

  • Connell, S. D., Kroeker, K. J., Fabricius, K. E., Kline, D. I. & Russell, B. D. The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos. Trans. R. Soc. B Biol. Sci. 368, 20120442 (2013).

    Google Scholar 

  • Kroeker, K. J., Micheli, F., Gambi, M. C. & Martz, T. R. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl. Acad. Sci. 108, 14515–14520 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Harvey, B. P., Kon, K., Agostini, S., Wada, S. & Hall-Spencer, J. M. Ocean acidification locks algal communities in a species-poor early successional stage. Glob. Change Biol. 27, 2174–2187 (2021).

    ADS 
    CAS 

    Google Scholar 

  • Sunday, J. M. et al. Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat. Clim. Change 7, 81–85 (2017).

    ADS 
    CAS 

    Google Scholar 

  • Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Steneck, R. S. et al. Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environ. Conserv. 29, 436–459 (2002).

    Google Scholar 

  • Schiel, D. R. & Foster, M. S. The population biology of large brown seaweeds: Ecological consequences of multiphase life histories in dynamic coastal environments. Annu. Rev. Ecol. Evol. Syst. 37, 343–372 (2006).

    Google Scholar 

  • Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser. 612, 209–215 (2019).

    ADS 

    Google Scholar 

  • Cheminée, A. et al. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. J. Exp. Mar. Biol. Ecol. 442, 70–79 (2013).

    Google Scholar 

  • Smale, D. A., Burrows, M. T., Moore, P., O’Connor, N. & Hawkins, S. J. Threats and knowledge gaps for ecosystem services provided by kelp forests: A northeast Atlantic perspective. Ecol. Evol. 3, 4016–4038 (2013).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Carbajal, P., Gamarra Salazar, A., Moore, P. J. & Pérez-Matus, A. Different kelp species support unique macroinvertebrate assemblages, suggesting the potential community-wide impacts of kelp harvesting along the Humboldt Current System. Aquat. Conserv. Mar. Freshw. Ecosyst. 32, 14–27 (2022).

    Google Scholar 

  • Filbee-Dexter, K. & Wernberg, T. Rise of turfs: A new battlefront for globally declining kelp forests. Bioscience 68, 64–76 (2018).

    Google Scholar 

  • Pessarrodona, A. et al. Homogenization and miniaturization of habitat structure in temperate marine forests. Glob. Change Biol. 27, 5262–5275 (2021).

    CAS 

    Google Scholar 

  • Orfanidis, S. et al. Effects of natural and anthropogenic stressors on Fucalean brown seaweeds across different spatial scales in the Mediterranean Sea. Front. Mar. Sci. 8, 1330 (2021).

    Google Scholar 

  • Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. 113, 13785–13790 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Capdevila, P. et al. Warming impacts on early life stages increase the vulnerability and delay the population recovery of a long-lived habitat-forming macroalga. J. Ecol. 107, 1129–1140 (2019).

    Google Scholar 

  • Irving, A. D., Balata, D., Colosio, F., Ferrando, G. A. & Airoldi, L. Light, sediment, temperature, and the early life-history of the habitat-forming alga Cystoseira barbata. Mar. Biol. 156, 1223–1231 (2009).

    Google Scholar 

  • Smith, K. E., Moore, P. J., King, N. G. & Smale, D. A. Examining the influence of regional-scale variability in temperature and light availability on the depth distribution of subtidal kelp forests. Limnol. Oceanogr. 67, 314–328 (2022).

    ADS 

    Google Scholar 

  • Smale, D. A. et al. Climate-driven substitution of foundation species causes breakdown of a facilitation cascade with potential implications for higher trophic levels. J. Ecol. 00, 1–13 (2022).

    Google Scholar 

  • Hollarsmith, J. A., Buschmann, A. H., Camus, C. & Grosholz, E. D. Varying reproductive success under ocean warming and acidification across giant kelp (Macrocystis pyrifera) populations. J. Exp. Mar. Biol. Ecol. 522, 151247 (2020).

    Google Scholar 

  • Verdura, J. et al. Local-scale climatic refugia offer sanctuary for a habitat-forming species during a marine heatwaves. J. Ecol. 109, 1758–1773 (2021).

    Google Scholar 

  • Mariani, S. et al. Past and present of Fucales from shallow and sheltered shores in Catalonia. Reg. Stud. Mar. Sci. 32, 100824 (2019).

    Google Scholar 

  • Smale, D. A. Impacts of ocean warming on kelp forest ecosystems. New Phytol. 225, 1447–1454 (2020).

    PubMed 

    Google Scholar 

  • Coelho, S. M., Rijstenbil, J. W. & Brown, M. T. Impacts of anthropogenic stresses on the early development stages of seaweeds. J. Aquat. Ecosyst. Stress Recov. 7, 317–333 (2000).

    CAS 

    Google Scholar 

  • de Caralt, S., Verdura, J., Vergés, A., Ballesteros, E. & Cebrian, E. Differential effects of pollution on adult and recruits of a canopy-forming alga: Implications for population viability under low pollutant levels. Sci. Rep. 10, 17825 (2020).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Capdevila, P. et al. Recruitment patterns in the Mediterranean deep-water alga Cystoseira zosteroides. Mar. Biol. 162, 1165–1174 (2015).

    CAS 

    Google Scholar 

  • Vadas, R. L., Johnson, S. & Norton, T. A. Recruitment and mortality of early post-settlement stages of benthic algae. Br. Phycol. J. 27, 331–351 (1992).

    Google Scholar 

  • Koch, M., Bowes, G., Ross, C. & Zhang, X.-H. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19, 103–132 (2013).

    ADS 

    Google Scholar 

  • Shih, P. M. et al. Biochemical characterization of predicted Precambrian RuBisCO. Nat. Commun. 7, 10382 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cornwall, C. E. et al. Inorganic carbon physiology underpins macroalgal responses to elevated CO2. Sci. Rep. 7, 46297 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hepburn, C. D. et al. Diversity of carbon use strategies in a kelp forest community: Implications for a high CO2 ocean. Glob. Change Biol. 17, 2488–2497 (2011).

    ADS 

    Google Scholar 

  • Porzio, L., Buia, M. C. & Hall-Spencer, J. M. Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400, 278–287 (2011).

    CAS 

    Google Scholar 

  • Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

    ADS 

    Google Scholar 

  • Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms: Biological responses to ocean acidification. Ecol. Lett. 13, 1419–1434 (2010).

    PubMed 

    Google Scholar 

  • Rindi, F. et al. Coralline algae in a changing Mediterranean Sea: How can we predict their future, if we do not know their present?. Front. Mar. Sci. 6, 723 (2019).

    Google Scholar 

  • James, R. K., Hepburn, C. D., Cornwall, C. E., McGraw, C. M. & Hurd, C. L. Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification. Mar. Biol. 161, 1687–1696 (2014).

    CAS 

    Google Scholar 

  • Comeau, S. & Cornwall, C. E. Contrasting effects of ocean acidification on coral reef “animal forests” versus seaweed “kelp forests.” In Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots (eds Rossi, S. et al.) 1–25 (Springer International Publishing, 2016) https://doi.org/10.1007/978-3-319-17001-5_29-1.

    Chapter 

    Google Scholar 

  • Airoldi, L. Effects of disturbance, life histories, and overgrowth on coexistence of algal crusts and turfs. Ecology 81, 798–814 (2000).

    Google Scholar 

  • Asnaghi, V. et al. Colonisation processes and the role of coralline algae in rocky shore community dynamics. J. Sea Res. 95, 132–138 (2015).

    ADS 

    Google Scholar 

  • Bulleri, F., Bertocci, I. & Micheli, F. Interplay of encrusting coralline algae and sea urchins in maintaining alternative habitats. Mar. Ecol. Prog. Ser. 243, 101–109 (2002).

    ADS 

    Google Scholar 

  • Villas Bôas, A. B. & Figueiredo, M. A. D. O. Are anti-fouling effects in coralline algae species specific?. Braz. J. Oceanogr. 52, 11–18 (2004).

    Google Scholar 

  • Bulleri, F., Benedetti-Cecchi, L., Acunto, S., Cinelli, F. & Hawkins, S. J. The influence of canopy algae on vertical patterns of distribution of low-shore assemblages on rocky coasts in the northwest Mediterranean. J. Exp. Mar. Biol. Ecol. 267, 89–106 (2002).

    Google Scholar 

  • Maggi, E., Bertocci, I., Vaselli, S. & Benedetti-Cecchi, L. Connell and Slatyer’s models of succession in the biodiversity era. Ecology 92, 1399–1406 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • Irving, A. D., Connell, S. D., Johnston, E. L., Pile, A. J. & Gillanders, B. M. The response of encrusting coralline algae to canopy loss: An independent test of predictions on an Antarctic coast. Mar. Biol. 147, 1075–1083 (2005).

    Google Scholar 

  • Irving, A. D., Connell, S. D. & Elsdon, T. S. Effects of kelp canopies on bleaching and photosynthetic activity of encrusting coralline algae. J. Exp. Mar. Biol. Ecol. 310, 1–12 (2004).

    Google Scholar 

  • Melville, A. J. & Connell, S. D. Experimental effects of kelp canopies on subtidal coralline algae. Austral. Ecol. 26, 102–108 (2001).

    Google Scholar 

  • Breitburg, D. L. Residual effects of grazing: Inhibition of competitor recruitment by encrusting coralline algae. Ecology 65, 1136–1143 (1984).

    Google Scholar 

  • Bulleri, F., Bruno, J. F., Silliman, B. R. & Stachowicz, J. J. Facilitation and the niche: Implications for coexistence, range shifts and ecosystem functioning. Funct. Ecol. 30, 70–78 (2016).

    Google Scholar 

  • van der Heide, T., Angelini, C., de Fouw, J. & Eklöf, J. S. Facultative mutualisms: A double-edged sword for foundation species in the face of anthropogenic global change. Ecol. Evol. 11, 29–44 (2021).

    PubMed 

    Google Scholar 

  • Molinari-Novoa, E. A. & Guiry, E. Reinstatement of the genera Gongolaria Boehmer and Ericaria Stackhouse (Sargassaceae, Phaeophyceae). Notulae Algarum 1–10 (2020).

  • Celis-Plá, P. S. M., Martinez, B., Korbee, N., Hall-Spencer, J. M. & Figueroa, F. L. Ecophysiological responses to elevated CO2 and temperature in Cystoseira tamariscifolia (Phaeophyceae). Clim. Change 142, 67–81 (2017).

    ADS 

    Google Scholar 

  • Falace, A. et al. Is the South-Mediterranean canopy-forming Ericaria giacconei (= Cystoseira hyblaea) a loser from ocean warming?. Front. Mar. Sci. 8, 1758 (2021).

    Google Scholar 

  • Hernández, C. A., Sangil, C., Fanai, A. & Hernández, J. C. Macroalgal response to a warmer ocean with higher CO2 concentration. Mar. Environ. Res. 136, 99–105 (2018).

    PubMed 

    Google Scholar 

  • Falace, A., Kaleb, S., Fuente, G. D. L., Asnaghi, V. & Chiantore, M. Ex situ cultivation protocol for Cystoseira amentacea var. stricta (Fucales, Phaeophyceae) from a restoration perspective. PLoS ONE 13, e0193011 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bevilacqua, S. et al. Climatic anomalies may create a long-lasting ecological phase shift by altering the reproduction of a foundation species. Ecology 100, 1–4 (2019).

    Google Scholar 

  • Savonitto, G. et al. Addressing reproductive stochasticity and grazing impacts in the restoration of a canopy-forming brown alga by implementing mitigation solutions. Aquat. Conserv. Mar. Freshw. Ecosyst. 31, 1611–1623 (2021).

    Google Scholar 

  • Mangialajo, L. et al. Zonation patterns and interspecific relationships of fucoids in microtidal environments. J. Exp. Mar. Biol. Ecol. 412, 72–80 (2012).

    Google Scholar 

  • Verlaque, M., Boudouresque, C.-F. & Perret-Boudouresque, M. Mediterranean seaweeds listed as threatened under the Barcelona Convention: A critical analysis. Sci. Rep. Port-Cros Natl. Park. 33, 179–214 (2019).

    Google Scholar 

  • Benedetti-Cecchi, L. & Cinelli, F. Effects of canopy cover, herbivores and substratum type on patterns of Cystoseira spp. settlement and recruitment in littoral rockpools. Mar. Ecol. Prog. Ser. 90, 183–191 (1992).

    ADS 

    Google Scholar 

  • Fuente, G. D. L., Chiantore, M., Asnaghi, V., Kaleb, S. & Falace, A. First ex situ outplanting of the habitat-forming seaweed Cystoseira amentacea var. stricta from a restoration perspective. PeerJ 7, e7290 (2019).

    Google Scholar 

  • Orlando-Bonaca, M. et al. First restoration experiment for Gongolaria barbata in Slovenian coastal waters. What can go wrong?. Plants 10, 239 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Christie, H. et al. Shifts between sugar kelp and turf algae in Norway: Regime shifts or fluctuations between different opportunistic seaweed species?. Front. Mar. Sci. 6, 72 (2019).

    Google Scholar 

  • Orlando-Bonaca, M., Pitacco, V. & Lipej, L. Loss of canopy-forming algal richness and coverage in the northern Adriatic Sea. Ecol. Indic. 125, 107501 (2021).

    Google Scholar 

  • Thibaut, T., Blanfune, A., Boudouresque, C.-F. & Verlaque, M. Decline and local extinction of Fucales in French Riviera: The harbinger of future extinctions?. Mediterr. Mar. Sci. 16, 206–224 (2015).

    Google Scholar 

  • Thibaut, T., Pinedo, S., Torras, X. & Ballesteros, E. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50, 1472–1489 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Leal, P. P. et al. Copper pollution exacerbates the effects of ocean acidification and warming on kelp microscopic early life stages. Sci. Rep. 8, 14763 (2018).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fernández, P. A., Navarro, J. M., Camus, C., Torres, R. & Buschmann, A. H. Effect of environmental history on the habitat-forming kelp Macrocystis pyrifera responses to ocean acidification and warming: A physiological and molecular approach. Sci. Rep. 11, 2510 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Lind, A. C. & Konar, B. Effects of abiotic stressors on kelp early life-history stages. Algae 32, 223–233 (2017).

    CAS 

    Google Scholar 

  • Fernández, P. A. et al. Nitrogen sufficiency enhances thermal tolerance in habitat-forming kelp: Implications for acclimation under thermal stress. Sci. Rep. 10, 3186 (2020).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Celis-Plá, P. S. M. et al. Macroalgal responses to ocean acidification depend on nutrient and light levels. Front. Mar. Sci. 2, 26 (2015).

    Google Scholar 

  • Mancuso, F. P. et al. Influence of ambient temperature on the photosynthetic activity and phenolic content of the intertidal Cystoseira compressa along the Italian coastline. J. Appl. Phycol. 31, 3069–3076 (2019).

    CAS 

    Google Scholar 

  • Vergés, A. et al. The tropicalization of temperate marine ecosystems: Climate-mediated changes in herbivory and community phase shifts. Proc. R. Soc. B Biol. Sci. 281, 20140846 (2014).

    Google Scholar 

  • Vergés, A. et al. Tropical rabbitfish and the deforestation of a warming temperate sea. J. Ecol. 102, 1518–1527 (2014).

    Google Scholar 

  • Gaitán-Espitia, J. D. et al. Interactive effects of elevated temperature and pCO2 on early-life-history stages of the giant kelp Macrocystis pyrifera. J. Exp. Mar. Biol. Ecol. 457, 51–58 (2014).

    Google Scholar 

  • Leal, P. P., Hurd, C. L., Fernández, P. A. & Roleda, M. Y. Ocean acidification and kelp development: Reduced pH has no negative effects on meiospore germination and gametophyte development of Macrocystis pyrifera and Undaria pinnatifida. J. Phycol. 53, 557–566 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Roleda, M. Y., Morris, J. N., McGraw, C. M. & Hurd, C. L. Ocean acidification and seaweed reproduction: Increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob. Change Biol. 18, 854–864 (2011).

    ADS 

    Google Scholar 

  • Zhang, X. et al. Elevated CO2 concentrations promote growth and photosynthesis of the brown alga Saccharina japonica. J. Appl. Phycol. https://doi.org/10.1007/s10811-020-02108-1 (2020).

    Article 

    Google Scholar 

  • Falkenberg, L. J., Russell, B. D. & Connell, S. D. Contrasting resource limitations of marine primary producers: Implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172, 575–583 (2013).

    ADS 
    PubMed 

    Google Scholar 

  • Nagelkerken, I., Russell, B. D., Gillanders, B. M. & Connell, S. D. Ocean acidification alters fish populations indirectly through habitat modification. Nat. Clim. Change 6, 89–93 (2016).

    ADS 
    CAS 

    Google Scholar 

  • Connell, S. D. & Russell, B. D. The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc. R. Soc. B Biol. Sci. 277, 1409–1415 (2010).

    Google Scholar 

  • Cornwall, C. E., Comeau, S. & McCulloch, M. T. Coralline algae elevate pH at the site of calcification under ocean acidification. Glob. Change Biol. 23, 4245–4256 (2017).

    ADS 

    Google Scholar 

  • Martin, S. & Gattuso, J.-P. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob. Change Biol. 15, 2089–2100 (2009).

    ADS 

    Google Scholar 

  • Cornwall, C. E. et al. Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. PLoS ONE 9, e97235 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gefen-Treves, S. et al. The microbiome associated with the reef builder Neogoniolithon sp. in the eastern Mediterranean. Microorganisms 9, 1374 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Johnson, C. R. & Mann, K. H. The crustose coralline alga, Phymatolithon Foslie, inhibits the overgrowth of seaweeds without relying on herbivores. J. Exp. Mar. Biol. Ecol. 96, 127–146 (1986).

    Google Scholar 

  • Keats, D. W., Knight, M. A. & Pueschel, C. M. Antifouling effects of epithallial shedding in three crustose coralline algae (Rhodophyta, Coralinales) on a coral reef. J. Exp. Mar. Biol. Ecol. 213, 281–293 (1997).

    Google Scholar 

  • Mancuso, F., D’Hondt, S., Willems, A., Airoldi, L. & Clerck, O. Diversity and temporal dynamics of the epiphytic bacterial communities associated with the canopy-forming seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin. Front. Microbiol. 7, 476 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Blanfuné, A., Boudouresque, C. F., Verlaque, M. & Thibaut, T. The ups and downs of a canopy-forming seaweed over a span of more than one century. Sci. Rep. 9, 1–10 (2019).

    Google Scholar 

  • Cebrian, E. et al. A roadmap for the restoration of Mediterranean macroalgal forests. Front. Mar. Sci. 8, 1456 (2021).

    Google Scholar 

  • Gianni, F. et al. Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of Marine Protected Areas. Adv. Oceanogr. Limnol. 4, 83–101 (2013).

    Google Scholar 

  • Gorman, D. & Connell, S. D. Recovering subtidal forests in human-dominated landscapes. J. Appl. Ecol. 46, 1258–1265 (2009).

    Google Scholar 

  • Riquet, F. et al. Highly restricted dispersal in habitat-forming seaweed may impede natural recovery of disturbed populations. Sci. Rep. 11, 16792 (2021).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Halpern, B. S., McLeod, K. L., Rosenberg, A. A. & Crowder, L. B. Managing for cumulative impacts in ecosystem-based management through ocean zoning. Ocean Coast. Manag. 51, 203–211 (2008).

    Google Scholar 

  • Verdura, J., Sales, M., Ballesteros, E., Cefalì, M. E. & Cebrian, E. Restoration of a canopy-forming alga based on recruitment enhancement: Methods and long-term success assessment. Front. Plant Sci. 9, 1832 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).

    ADS 
    CAS 

    Google Scholar 

  • Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to Best Practices for Ocean CO2 Measurements. https://repository.oceanbestpractices.org/handle/11329/249 (2007).

  • Spencer Davies, P. Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar. Biol. 101, 389–395. https://doi.org/10.1007/BF00428135 (1989).

    Article 

    Google Scholar 

  • Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. ArXiv14065823 Stat (2015).

  • R: The R Project for Statistical Computing. https://www.r-project.org/.

  • Fox, J. & Weisberg, S. An R Companion to Applied Regression (SAGE Publications, 2018).

    Google Scholar 

  • Lenth, R. V. et al. emmeans: Estimated Marginal Means, aka Least-Squares Means (2022).


  • Source: Ecology - nature.com

    Coordinating climate and air-quality policies to improve public health

    Pesticide innovation takes top prize at Collegiate Inventors Competition