Local adaptation of juvenile giant kelp, Macrocystis pyrifera, from their southern limit in the northern hemisphere explored using reciprocal transplantation

References

• Arafeh-Dalmau, N. Schoeman, D.S., Montaño-Moctezuma, G., Micheli, F., Rogers-Bennett, L., C Olguin-Jacobson, C. & Possingham, H.P. (2020). Marine heat waves threaten kelp forests. Science, V367: 635.
   Google Scholar
• Bridle, J.R., Kawata, M. & Butlin, R.K. (2019). Local adaptation stops where ecological gradients steepen or are interrupted. Evolutionary Applications, 12: 1449–1462.
   PubMed Web of Science ®Google Scholar
• Cabello‐Pasini, A. & Alberte, R.S. (1997). Seasonal patterns of photosynthesis and light‐independent carbon fixation in marine macrophytes. Journal of Phycology, 33: 321–329.
   Web of Science ®Google Scholar
• Cavanaugh, K., Reed, D., Bell, T., Castorani, M. & Beas-Luna, R. (2019). Spatial variability in the resistance and resilience of giant kelp in Southern and Baja California to a multiyear heatwave. Frontiers in Marine Science, 6: 413.
   Web of Science ®Google Scholar
• Claisse, J., Williams, J., Ford, T., Pondella, D., Meux, B. & Protopapadakis, L. (2013). Kelp forest habitat restoration has the potential to increase sea urchin gonad biomass. Ecosphere, 43: 1–19.
   Google Scholar
• Coleman, M. & Goold, H. (2019). Harnessing synthetic biology for kelp forest conservation. Journal of Phycology, 55: 745–751.
   PubMed Web of Science ®Google Scholar
• Davison, I. (1991). Environmental effects on algal photosynthesis: temperature. Journal of Phycology, 27: 2–8.
   Web of Science ®Google Scholar
• Dumas, A. (1826). Annales de chimie, 33: 342.
   Google Scholar
• Edwards, M.S. (2004). Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia, 138: 436–447.
   PubMed Web of Science ®Google Scholar
• Edwards, M.S. & Hernández-Carmona, G. (2005). Delayed recovery of giant kelp near its southern range limit in the North Pacific following El Niño. Marine Biology, 147: 273-279.
   Web of Science ®Google Scholar
• Espinoza, J. & Chapman, A.R.O. (1983). Ecotypic differentiation of Laminaria longicruris in relation to seawater nitrate concentration. Marine Biology, 74: 213–218.
   Web of Science ®Google Scholar
• Gao, X., Endo, H., Taniguchi, K. & Agatsuma, Y. (2013). Genetic differentiation of high-temperature tolerance in the kelp Undaria pinnatifida sporophytes from geographically separated populations along the Pacific coast of Japan. Journal of Applied Phycology, 25: 567–574.
   Web of Science ®Google Scholar
• Gaylord, B., Reed, D.C., Raimondi, P.T. & Washburn, L. (2006). Macroalgal spore dispersal in coastal environments: mechanistic insights revealed by theory and experiment. Ecological Monographs, 76: 481–502.
   Web of Science ®Google Scholar
• Gerard, V. (1982). In situ rates of nitrate uptake by giant kelp, Macrocystis pyrifera (L.) C.Agardh: tissue differences, environmental effects, and predictions of nitrogen-limited growth. Journal of Experimental Marine Biology and Ecology, 62: 211–224.
   Web of Science ®Google Scholar
• Gerard, V. (1986). Photosynthetic characteristics of giant kelp (Macrocystis pyrifera) determined in situ. Marine Biology, 90: 473–482.
   Web of Science ®Google Scholar
• Gerard, V. (1997). The role of nitrogen nutrition in high-temperature tolerance of the kelp, Laminaria saccharina (Chromophyta). Journal of Phycology, 33: 800–810.
   Web of Science ®Google Scholar
• Hallfors, M., Liao, J., Dzurisin, J., Grundel, R., Hyvarinen, M., Towle, K., Wu, G. & Hellman, J. (2016). Addressing potential local adaptation in species distribution models: implications for conservation under climate change. Ecological Applications, 26: 1154–1169.
   PubMed Web of Science ®Google Scholar
• Hampe, A. & Petit, R. J. (2005), Conserving biodiversity under climate change: the rear edge matters. Ecology Letters, 8: 461–467.
   PubMed Web of Science ®Google Scholar
• Hernández-Carmona, G., Robledo, D. & Serviere-Zaragoza, E. (2001). Effect of nutrient availability on Macrocystis pyrifera recruitment and survival near its southern limit off Baja California. Botanica Marina, 44: 221–229.
   Web of Science ®Google Scholar
• Kawecki, T. & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7: 1225–1241.
   Web of Science ®Google Scholar
• Kawecki, T. J. (2008). Adaptation to marginal habitats. Annual Review of Ecology, Evolution, and systematics. 39: 321–342.
   Web of Science ®Google Scholar
• King, N., McKeown, N., Smale, D., Wilcockson, D., Hoelters, L., Groves, E., Stamp, T. & Moore, P. (2019). Evidence for different thermal ecotypes in range centre and trailing edge kelp populations. Journal of Experimental Marine Biology and Ecology, 514: 10–17.
   Web of Science ®Google Scholar
• Kopczak, C., Zimmerman, R. & Kremer, J. (1991). Variation in nitrogen physiology and growth among geographically isolated populations of the giant kelp Macrocystis pyrifera (Phaeophyta). Journal of Phycology, 27: 149–158.
   Web of Science ®Google Scholar
• Ladah, L.B. (2003). The shoaling of nutrient-enriched subsurface waters as a mechanism to sustain primary productivity off Central Baja California during El Niño winters. Journal of Marine Systems, 42: 145–152.
   Web of Science ®Google Scholar
• Ladah, L., Leichter, J., Filonov, A. & Tereshchenko I. (2017). Diurnal frequency internal waves in the southern part of the California Current ecosystem as a nutrient source. Ciencias Marinas, 43: 203–215.
   Web of Science ®Google Scholar
• Ladah, L. & Zertuche-González, J.A. (2004). Giant kelp (Macrocystis pyrifera) survival in deep water (25–40 m) during El Niño of 1997–1998 in Baja California, Mexico. Botanica Marina, 47: 367–372.
   Web of Science ®Google Scholar
• Ladah, L. & Zertuche-González, J.A. (2007). Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the northern hemisphere after exposure to simulated El Niño stress. Marine Biology, 152: 677–686.
   Web of Science ®Google Scholar
• Ladah, L., Zertuche-González, J.A. & Hernández-Carmona, G. (1999). Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997–1998. Journal of Phycology, 35: 1106–1112.
   Web of Science ®Google Scholar
• Ladah L.B., Filanov, A., Lavin, M.F., Leichter, J.J., Zertuche-Gonzalez, J.A. & Pérez-Mayorga, D. (2012). Cross-shelf transport of sub-thermocline nitrate by internal tides and rapid (3-6 hr) incorporation by inshore marcroalgae. Continental Shelf Research, 42: 10–19.
   Web of Science ®Google Scholar
• Liesner, D., Fouqueau, L., Valero, M., Roleda, M.Y., Pearson, G.A., Bischof, K., Klaus Valentin, K. & Bartsch, I. (2020). Heat stress responses and population genetics of the kelp Laminaria digitata (Phaeophyceae) across latitudes reveal differentiation among North Atlantic populations. Ecology and Evolution, 10: 9144–77.
   Google Scholar
• Mabin, C., Johnson, C. & Wright, J. (2019). Physiological response to temperature, light, and nitrates in the giant kelp Macrocystis pyrifera from Tasmania, Australia. Marine Ecology Progress Series, 614: 1–19.
   Web of Science ®Google Scholar
• Machado-Monteiro, C.M., Li, H., Bischof, K., Bartsch, I., Valentin, K., Corre, E., Collén, J., Harms, L., Glöckner, G. & Heinrich, S. (2019). Is geographical variation driving the transcriptomic responses to multiple stressors in the kelp Saccharina latissima? BMC Plant Biology, 19: 513.
   PubMed Web of Science ®Google Scholar
• Olischläger, M., Iñiguez, C., Koch, K., Weincke, C. & Lopez Gordillo F. (2017). Increased pCO2 and temperature reveal ecotypic differences in growth and photosynthetic performance of temperate and Arctic populations of Saccharina latissima. Planta, 245: 119–136.
   Google Scholar
• Olischläger M, Iñiguez C, Gordillo FJL, Wiencke C (2014) Biochemical composition of temperate and Arctic populations of Saccharina latissima after exposure to increased pCO2 and temperature reveals ecotypic variation. Planta, 240: 1213–1224
   PubMed Web of Science ®Google Scholar
• Pang, S.J., Jin, Z.H., Sun, J.Z. & Gao, S.Q. (2007). Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture, 262: 493–503.
   Web of Science ®Google Scholar
• Pérez-Mayorga, D., Ladah, L., Zertuche-González, J.A., Leichter, J., Filonov, A. & Lavin, M. (2011). Nitrate uptake and growth by the opportunistic macroalga Ulva lactuca during the internal tide. Journal of Experimental Marine Biology and Ecology, 406: 108–115.
   Web of Science ®Google Scholar
• Roleda, M.Y. & Hurd, C.L. (2019). Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation. Phycologia, 58: 552–562.
   Web of Science ®Google Scholar
• Sánchez-Barredo, M., Sandoval-Gil, J.M., Zertuche-González, J.A., Ladah, L.B., Belando-Torrentes, M.D., Beas-Lunas, R. & Cabello-Passini, A. (2020). Effect of heatwaves and light deprivation in giant kelp juveniles (Macrocystis pyrifera, Laminariales, Phaeophyceae). Journal of Phycology, 56: 880–894.
   PubMed Web of Science ®Google Scholar
• Sato,Y., Hirano, T., Niwa, K., Suzuki, T., Fukunishi, N., Abe, T. & Kawano, S. (2016). Phenotypic differentiation in the morphology and nutrient uptake kinetics among Undaria pinnatifida cultivated at six sites in Japan. Journal of Applied Phycology, 28: 3447–3458.
   Web of Science ®Google Scholar
• Schiel, D. R. & Foster, M. S. (2015). The Biology and Ecology of Giant Kelp Forests. University of California Press, Oakland California, USA, 395 pp.
   Google Scholar
• Sexton, J.P., McIntyre, P.J., Angert, A.L. & Rice, K.J. (2009). Evolution and ecology of species range limits. Annual Review of Ecology, Evolution, and Systematics, 40: 415–436.
   Web of Science ®Google Scholar
• Smale, D.A. & Wernberg, T. (2013). Extreme climatic event drives range contraction of a habitat-forming species. Proceedings of the Royal Society B, 280: 20122829.
   PubMed Web of Science ®Google Scholar
• Smale, D.A., Wernberg, T., Oliver, E.C.J., Thomsen, M., Harvey, B.P., Straub, S.C., Burrows, M.T., Alexander, L.V., Benthuysen, J.A., Donat, M.G., Feng, M., Hobday, A., Holbrook, N.J., Perkins-Kirkpatrick, S.E., Scannell, H.A., Gupta, A.S., Payne, B.L. & Moore, P.J. (2019). Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nature Climate Change, 9: 306–312.
   Web of Science ®Google Scholar
• Smale, D. A. (2020). Impacts of ocean warming on kelp forest ecosystems. New Phytologist, 225: 1447–54.
   PubMed Web of Science ®Google Scholar
• Steneck, R., Graham, M., Bourque, B., Corbett, D., Erlandson, J., Estes, J. & Tegner, M. (2002). Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation, 29: 436–459.
   Web of Science ®Google Scholar
• Stephens, T.A. & Hepburn, C.D. (2016). A kelp with integrity: Macrocystis pyrifera prioritizes tissue maintenance in response to nitrogen fertilization. Oecologia, 182: 71–84.
   PubMed Web of Science ®Google Scholar
• Straub, S., Wernberg, T., Thomsen, M.S., Moore, P.J., Burrows, M.T., Harvey, B.P. & Smale, D.A. (2019). Resistance, extinction, and everything in between – the diverse responses of seaweeds to marine heatwaves. Frontiers in Marine Science, 6: 763.
   Web of Science ®Google Scholar
• Sutherland, W., Dias, M., Dicks, L., Doran, H., Entwistle, A., Fleishman, E., Gibbons, D.W., Hails, R., Hughes, A.C., Hughes, J., Kelman, R., Le Roux, X., LeAnstey, B., Lickorish, F.A., Maggs, L., Pearce-Higgins, J.W., Peck, L.S., Pettorelli, N., Pretty, J., Spalding, M.D., Tonneijck, F.H., Wentworth, J. & Thornton, A. (2020). A horizon scan of emerging global biological conservation issues for 2020. Trends in Ecology & Evolution, 35: 81–90.
   PubMed Web of Science ®Google Scholar
• Tait, L. & Schiel, D.R. (2013). Impacts of temperature on primary productivity and respiration in naturally structured macroalgal assemblages. PLoS ONE, 8: 1–10.
   Web of Science ®Google Scholar
• Turpin, D. (1991). Effects of inorganic N availability on algal photosynthesis and carbon metabolism. Journal of Phycology, 27: 14–20.
   Web of Science ®Google Scholar
• Umanzor, S., Sandoval-Gil, J.M., Sánchez-Barredo, M., Ladah, L., Ramírez-García, M. & Zertuche-González, J.A. (2021). Short-term stress responses and recovery of giant kelp (Macrocystis pyrifera, Laminariales, Phaeophyceae) juvenile sporophytes to a simulated marine heatwave and nitrate scarcity. Journal of Phycology. 57: 1204–1618.
   PubMed Web of Science ®Google Scholar
• Vasquez, X., Gutierrez, A., Buschmann, A.H., Flores, R., Farias, D. & Leal, P. (2014). Evaluation of repopulation techniques for the giant kelp Macrocystis pyrifera (Laminariales). Botanica Marina, 57: 123–130.
   Web of Science ®Google Scholar
• Wernberg, T., de Bettignies, T., Joy, B.A. & Finnegan, P.M. (2016). Physiological responses of habitat-forming seaweeds to increasing temperatures. Limnology and Oceanography, 61: 2180–2190.
   Web of Science ®Google Scholar
• Westermeier, R., Murúa, P., Patiño, D., Muñoz, L., Atero, C. & Müller D. (2014). Repopulation techniques for Macrocystis integrifolia (Phaeophyceae: Laminariales) in Atacama, Chile. Journal of Applied Phycology, 26: 511–518.
   Web of Science ®Google Scholar
• Williams, G.C. (1966). Adaptation and Natural Selection. Princeton University Press,Princeton.
   Google Scholar
• Wood, G., Marzinelli, E.M., Coleman, M.A., Campbell, A.H., Santini, N.S., Kajlich, L., Verdura, J., Wodak, J., Steinberg, P., & Vergés, A. (2019). Restoring subtidal marine macrophytes in the Anthropocene: trajectories and future-proofing. Marine and Freshwater Research, 70: 936–951
   Web of Science ®Google Scholar
• Zimmerman, R.C. & Kremer, J.N. (1984). Episodic nutrient supply to a kelp forest ecosystem in Southern California. Journal of Marine Research, 42: 591–604.
   Web of Science ®Google Scholar
• Zimmerman, R.C. & Kremer, J.N. (1986). In situ growth and chemical composition of the giant kelp Macrocystis pyrifera: response to temporal changes in ambient nutrient availability. Marine Ecology Progess Series, 27: 277–285.
   Web of Science ®Google Scholar