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Population persistence of the perennial kelp Eisenia arborea varies across local spatial scales

  • Gossard, Daniel J. (Moss Landing Marine Laboratories) ;
  • Steller, Diana L. (Moss Landing Marine Laboratories)
  • Received : 2021.08.31
  • Accepted : 2022.02.19
  • Published : 2022.03.15
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Abstract

Perennial stipitate kelps are globally distributed and individual species can inhabit broad latitudinal ranges, expressing notably longevous persistence. Despite the foundational role kelps provide to their communities, little is known about the variability in persistence of the stipitate kelps at local spatial scales. We studied the population persistence of Eisenia arborea, a heat- and wave force-tolerant perennial stipitate kelp with a distributional range extending from British Columbia to south of the range limit of all other northeast Pacific kelps, in Baja California Sur, Mexico. Persistence characteristics for E. arborea among sites were compared and used to test the hypothesis that stand persistence varied at local spatial scales around Isla Natividad, a Pacific island off the Baja California peninsula with documented spatiotemporal environmental heterogeneity. Collected individuals around the island were "aged" using the previously validated age estimation technique of counting annual cortical dark rings. After detecting no significant differences among sites in the covariation between estimated ages for collected individuals and stipe length, we utilized in-situ population-level stipe length measurements to more rapidly predict age structures within six stands around the island. Predicted age structures, and associated stand densities, revealed persistence characteristics and density varied at local scales and a strong positive relationship existed between stand density and stand mean and maximum ages. We speculate that stands responded differently to deterministic influences (e.g., the 2014-2016 marine heatwave and / or competition with Macrocystis) resulting in heterogenous local persistence of this foundation species.

Keywords

Acknowledgement

The authors are grateful for the support for this course and research from Rodrigo Beas-Luna of Universidad Autonoma de Baja California and James Harvey, Scott Hamilton, and Ivano Aiello from Moss Landing Marine Laboratories. Thanks to three anonymous reviewers and Michael Graham for comments on the manuscript. Facilitation of on-island access, logistics, diving, and all the caracol lunches was provided by the Sociedad Cooperativa de Produccion Pesquera Buzos y Pescadores de Isla Nativdad, Comunidad y Biodiversidad (COBI), Isla Natividad, and in particular our guides Raffy, Esteban, Ivan, and Johnny. Special thanks go to Jeremie Bauer and Andrea Paz-Lacavex for their support in all aspects. Thanks to Ann Bishop, Hali Rederer, Jackie Mohay, June Shrestha, Katie Cieri, Laurel Lam, Nikki Inglis, Rachel Brooks, Sloane Lofy, and Vivian Ton for help in the laboratory and the field. And lastly, thanks to MLML Administration, Marine Operations, and MLML Diving for overall support.

References

  1. Assis, J., Berecibar, E., Claro, B., Alberto, F., Reed, D., Raimondi, P. & Serrao, E. A. 2017. Major shifts at the range edge of marine forests: the combined effects of climate changes and limited dispersal. Sci. Rep. 7:44348. https://doi.org/10.1038/srep44348
  2. Bard, E., Hamelin, B., Fairbanks, R. G. & Zindler, A. 1990. Calibration of the 14C timescale over the past 30,000 years using mass spectrometric U-Th ages from Barbados corals. Nature 345:405-410. https://doi.org/10.1038/345405a0
  3. Benes, K. M. & Carpenter, R. C. 2015. Kelp canopy facilitates understory algal assemblage via competitive release during early stages of secondary succession. Ecology 96:241-251. https://doi.org/10.1890/14-0076.1
  4. Boch, C. A., Micheli, F., Al Najjar, M., Monismith, S. G., Beers, J. M., Bonilla, J. C., Espinoza, A. M., Vazquez-Vera, L. & Woodson, C. B. 2018. Local oceanographic variability influences the performance of juvenile abalone under climate change. Sci. Rep. 8:5501. https://doi.org/10.1038/s41598-018-23746-z
  5. Bolton, J. J. 2010. The biogeography of kelps (Laminariales, Phaeophyceae): a global analysis with new insights from recent advances in molecular phylogenetics. Helgol. Mar. Res. 64:263-279. https://doi.org/10.1007/s10152-010-0211-6
  6. Briand, C. H., Brazer, S. E. & Harter-Dennis, J. M. 2006. Tree rings and the aging of trees: a controversy in 19th century America. Tree-Ring Res. 62:51-65. https://doi.org/10.3959/1536-1098-62.2.51
  7. Burnett, N. P. & Koehl, M. A. R. 2019. Mechanical properties of the wave-swept kelp Egregia menziesii change with season, growth rate and herbivore wounds. J. Exp. Mar. Biol. 222:190595.
  8. Campana, S. E. & Neilson, J. D. 1985. Microstructure of fish otoliths. Can. J. Fish Aquat. Sci. 42:1014-1032. https://doi.org/10.1139/f85-127
  9. Cavanaugh, K. C., Reed, D. C., Bell, T. W., Castorani, M. C. N. & Beas-Luna, R. 2019. Spatial variability in the resistance and the resilience of giant kelp in southern and Baja California to a multiyear heatwave. Front. Mar. Sci. 6:413. https://doi.org/10.3389/fmars.2019.00413
  10. Christensen, M. S. 2018. Chemical competition between microscopic stages of Macrocystis pyrifera and five native kelp species: does giant kelp always lose? M.S. thesis, San Jose State University, San Jose, CA, USA, 45 pp.
  11. Christie, H., Fredriksen, S. & Rinde, E. 1998. Regrowth of kelp and colonization of epiphyte and fauna community after kelp trawling at the coast of Norway. Hydrobiologia 375:49-58. https://doi.org/10.1023/A:1017021325189
  12. Christie, H., Norderhaug, K. M. & Fredriksen, S. 2009. Macrophytes as habitat for fauna. Mar. Ecol. Prog. Ser. 396:221-233. https://doi.org/10.3354/meps08351
  13. Clark, R. P., Edwards, M. S. & Foster, M. S. 2004. Effects of shade from multiple kelp canopies on an understory algal assemblage. Mar. Ecol. Prog. Ser. 267:107-119. https://doi.org/10.3354/meps267107
  14. Davis, T. R., Champion, C. & Coleman, M. A. 2021. 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
  15. Dawson, E. Y. 1952. Circulation within Bahia Vizcaino, Baja California, and its effects on marine vegetation. Am. J. Bot. 39:425-432. https://doi.org/10.2307/2438325
  16. Dayton, P. K., Currie, V., Gerrodette, T., Keller, B. D., Rosenthal, R. & Van Tresca, D. 1984. Patch dynamics and stability of some California Kelp Communities. Ecol. Monogr. 54:253-289. https://doi.org/10.2307/1942498
  17. Dayton, P. K., Tegner, M. J., Edwards, P. B. & Riser, K. L. 1999. Temporal and spatial scales of kelp demography: the role of oceanographic climate. Ecol. Monogr. 69:219-250. https://doi.org/10.1890/0012-9615(1999)069[0219:TASSOK]2.0.CO;2
  18. Dayton, P. K., Tegner, M. J., Parnell, P. E. & Edwards, P. B. 1992. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol. Monogr. 62:421-445. https://doi.org/10.2307/2937118
  19. De Wreede, R. E. 1984. Growth and age class distribution of Pterygophora californica (Phaeophyta). Mar. Ecol. Prog. Ser. 19:93-100. https://doi.org/10.3354/meps019093
  20. De Wreede, R. E. 1986. Demographic characteristics of Pterygophora californica (Laminariales, Phaeophyta). Phycologia 25:11-17. https://doi.org/10.2216/i0031-8884-25-1-11.1
  21. Proo, S. A. G., Palau, L. C., Perez, J. B., Laguna, J. C. & Fragoso, R. H. 2003. Effects of the 'El Nino' event on the recruitment of benthic invertebrates in Bahia Tortugas, Baja California Sur. Geofis. Int. 42:429-438.
  22. Demes, K. W., Graham, M. H. & Suskiewicz, T. S. 2009. Phenotypic plasticity reconciles incongruous molecular and morphological taxonomies: the giant kelp, Macrocystis (Laminariales, Phaeophyceae), is a monospecific genus. J. Phycol. 45:1266-1269. https://doi.org/10.1111/j.1529-8817.2009.00752.x
  23. Douglass, A. E. 1909. Weather cycles in the growth of big trees. Monthly Weather Rev. 37:225-237. https://doi.org/10.1175/1520-0493(1909)37[225d:WCITGO]2.0.CO;2
  24. Edwards, M. S. & Hernandez-Carmona, G. 2005. Delayed recovery of giant kelp near its southern range limit in the North Pacific following El Nino. Mar. Biol. 147:273-279. https://doi.org/10.1007/s00227-004-1548-7
  25. Fernandez, P. A., Navarro, J. M., Camus, C., Torres, R. & Buschmann, A. H. 2021. 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. https://doi.org/10.1038/s41598-021-82094-7
  26. Filbee-Dexter, K. & Wernberg, T. 2018. Rise of turfs: a new battlefront for globally declining kelp forests. BioScience 68:64-76. https://doi.org/10.1093/biosci/bix147
  27. Frank, P. W. 1968. Life histories and community stability. Ecology 49:355-357. https://doi.org/10.2307/1934470
  28. Gaylord, B., Nickols, K. J. & Jurgens, L. 2012. Roles of transport and mixing processes in kelp forest ecology. J. Exp. Bio. 215:997-1007. https://doi.org/10.1242/jeb.059824
  29. Graham, M. H. 1997. Factors determining the upper limit of giant kelp, Macrocystis pyrifera Agardh, along the Monterey Peninsula, central California, USA. J. Exp. Mar. Biol. Ecol. 218:127-149. https://doi.org/10.1016/S0022-0981(97)00072-5
  30. Graham, M. H. 2004. Effects of local deforestation of the diversity and structure on southern California giant kelp forest food webs. Ecosystems 7:341-357. https://doi.org/10.1007/s10021-003-0245-6
  31. Graham, M. H., Kinlan, B. P., Druehl, L. D., Garske, L. E. & Banks, S. 2007. Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc. Natl. Acad. Sci. U. S. A. 104:16576-16580. https://doi.org/10.1073/pnas.0704778104
  32. Gunnill, F. C. 1980. Recruitment and standing stocks in populations of one green alga and five brown algae in the intertidal zone near La Jolla, California during 1973-1977. Mar. Ecol. Prog. Ser. 3:231-243. https://doi.org/10.3354/meps003231
  33. Harper, J. L. 1977. Population biology of plants. Academic Press, San Diego, CA, pp. 599-643.
  34. Hughes, B. B. 2010. Variable effects of a kelp foundation species on rocky intertidal diversity and species interaction in central California. J. Exp. Mar. Biol. Ecol. 393:90-99. https://doi.org/10.1016/j.jembe.2010.07.003
  35. Hymanson, Z. P., Reed, D. C., Foster, M. S. & Carter, J. W. 1990. The validity of using morphological characteristics as predictors of age in the kelp Pterygophora californica (Laminariales, Phaeophyta). Mar. Ecol. Prog. Ser. 59:295-304. https://doi.org/10.3354/meps059295
  36. Jones, C. M. 1992. Development and application of the otolith increment technique. Can. Spec. Publ. Fish. Aquat. Sci. 117:1-11.
  37. Kain, J. M. & Jones, N. S. 1963. Aspects of the biology of Laminaria hyperborea: II. Age, weight and length. J. Mar. Biol. Assoc. U. K. 43:129-151. https://doi.org/10.1017/S0025315400005312
  38. Kinlan, B. P., Graham, M. H., Sala, E. & Dayton, P. K. 2003. Arrested development of giant kelp (Macrocystis pyrifera, Phaeophyceae) embryonic sporophytes: a mechanism for delayed recruitment in perennial kelps? J. Phycol. 39:47-57.
  39. Koehl, M. A. R., Silk, W. K., Liang, H. & Mahadevan, L. 2008. How kelp produce blade shapes suited to different flow regimes: a new wrinkle. Integr. Comp. Biol. 48:834-851. https://doi.org/10.1093/icb/icn069
  40. Ladah, L. B., Zertuche-Gonzalez, J. A. & Hernandez-Carmona, G. 1999. Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997-1998. J. Phycol. 35:1106-1112. https://doi.org/10.1046/j.1529-8817.1999.3561106.x
  41. Luning, K. & Freshwater, W. 1988. Temperature tolerance of Northeast Pacific marine algae. J. Phycol. 24:310-315. https://doi.org/10.1111/j.1529-8817.1988.tb00178.x
  42. MacMillan, C. 1902. Observations on Pterygophora. Minn. Bot. Stud. 2:723-741.
  43. Matson, P. G. & Edwards, M. S. 2006. Latitudinal variation in stipe hollowing in Eisenia arborea (Phaeophyceae, Laminariales). Phycologia 45:343-348. https://doi.org/10.2216/05-41.1
  44. Matson, P. G. & Edwards, M. S. 2007. Effects of ocean temperature on the southern range limits of two understory kelps, Pterygophora californica and Eisenia arborea, at multiple life-stages. Mar. Biol. 151:1941-1949. https://doi.org/10.1007/s00227-007-0630-3
  45. McPherson, M. L., Finger, D. J. I., Houskeeper, H. F., Bell, T. W., Carr, M. H., Rogers-Bennett, L. & Kudela, R. M. 2021. Large-scale shift in the structure of a kelp forest ecosystem co-occurs with an epizootic and marine heatwave. Commun. Biol. 4:298. https://doi.org/10.1038/s42003-021-01827-6
  46. Micheli, F., Saenz-Arroyo, A., Greenley, A., Vazquez, L., Antonio Espinoza Montes, J., Rossetto, M. & De Leo, G. A. 2012. Evidence that marine reserves enhance resilience to climatic impacts. PLoS ONE 7:e40832. https://doi.org/10.1371/journal.pone.0040832
  47. Muth, A. F., Graham, M. H., Lane, C. E. & Harley, C. D. G. 2019. Recruitment tolerance to increased temperature present across multiple kelp clades. Ecology 100:e02594. https://doi.org/10.1002/ecy.2594
  48. Parada, G. M., Riosmena Rodriguez, R., Martinez, E. A. & Hernandez-Carmona, G. 2012. Dinamica poblacional de Eisenia arborea Areschoug (Laminariales, Ochrophyta) en el intermareal de Punta Eugenia, Baja California Sur, Mexico. Cienc. Mar. 13:3-13.
  49. Pfister, C. A., Berry, H. D. & Mumford, T. 2018. The dynamics of kelp forests in the Northeast Pacific Ocean and the relationship with environmental drivers. J. Ecol. 106:1520-1533. https://doi.org/10.1111/1365-2745.12908
  50. Provost, E. J., Kelaher, B. P., Dworjanyn, S. A., Russell, B. D., Connell, S. D., Ghedini, G., Gillanders, B. M., Figueria, W. & Coleman, M. A. 2017. Climate-driven disparities among ecological interactions threaten kelp forest persistence. Glob. Change Biol. 23:353-361. https://doi.org/10.1111/gcb.13414
  51. Reed, D. C., Laur, D. R. & Ebeling, A. W. 1988. Variation in algal dispersal and recruitment: the importance of episodic events. Ecol. Monogr. 58:321-335. https://doi.org/10.2307/1942543
  52. Roberson, L. M. & Coyer, J. A. 2004. Variation in blade morphology of the kelp Eisenia arborea: incipient speciation due to local water motion? Mar. Ecol. Prog. Ser. 282:115-128. https://doi.org/10.3354/meps282115
  53. Rogers-Bennett, L. & Catton, C. A. 2019. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep. 9:15050. https://doi.org/10.1038/s41598-019-51114-y
  54. Rothman, M. D., Bolton, J. J., Stekoll, M. S., Boothroyd, C. J. T., Kemp, F. A. & Anderson, R. J. 2017. Geographical variation in morphology of the two dominant kelp species, Ecklonia maxima and Laminaria pallida (Phaeophyceae, Laminariales), on the west coast of Southern Africa. J. Appl. Phycol. 29:2627-2639. https://doi.org/10.1007/s10811-017-1255-7
  55. Schiel, D. R. & Foster, M. S. 2015. The biology and ecology of giant kelp forests. University of California Press, Oakland, CA, 395 pp.
  56. Serviere-Zaragoza, E., Garcia-Hernandez, V. C. & SiqueirosBeltrones, D. A. 2003. Diversity and distribution of macroalgae associated with abalone (Haliotis spp.) habitats in Baja California Sur, Mexico. Bull. Mar. Sci. 72:725-739.
  57. Serviere-Zaragoza, E., Gomez-Lopez, D. & Ponce-Diaz, G. 1998. The natural diet of the green abalone (Haliotis fulgens Philippi) in the southern part of its range, Baja California Sur, Mexico, assessed by an analysis of gut contents. J. Shellfish Res. 17:777-782.
  58. Sievers, K. T., Barr, R. J., Maloney, J. M., Driscoll, N. W. & Anderson, T. W. 2016. Impact of habitat structure on fish populations in kelp forests at a seascape scale. Mar. Ecol. Prog. Ser. 557:51-63. https://doi.org/10.3354/meps11885
  59. Springer, Y. P., Hays, C. G., Carr, M. H. & Mackey, M. R. 2010. Toward ecosystem-based management of marine macroalgae: the bull kelp, Nereocystis luetkeana. Oceanogr. Mar. Biol. Annu. Rev. 48:1-42.
  60. Starko, S., Bailey, L. A., Creviston, E., James, K. A., Warren, A., Brophy, M. K., Danasel, A., Fass, M. P., Townsend, J. A. & Neufeld, C. J. 2019. Environmental heterogeneity mediates scale-dependent declines in kelp diversity on intertidal rocky shores. PLoS ONE 14:e0213191. https://doi.org/10.1371/journal.pone.0213191
  61. Starko, S., Demes, K. W., Neufeld, C. J. & Martone, P. T. 2020. Convergent evolution of niche structure in Northeast Pacific kelp forests. Funct. Ecol. 34:2131-2146. https://doi.org/10.1111/1365-2435.13621
  62. Straub, S. C., Wernberg, T., Marzinelli, E. M., Verges, A., Kelaher, B. P. & Coleman, M. A. 2021. Persistence of seaweed forests in the anthropocene will depend on warming and marine heatwave profiles. J. Phycol. 58:22-35.
  63. Swetnam, T. W. 1993. Fire history and climate change in Giant Sequoia groves. Science 262:885-889. https://doi.org/10.1126/science.262.5135.885
  64. Tegner, M. J. & Dayton, P. K. 1987. El Nino effects on southern California kelp forest communities. Adv. Ecol. Res. 17:243-279. https://doi.org/10.1016/S0065-2504(08)60247-0
  65. Tegner, M. J., Dayton, P. K., Edwards, P. B. & Riser, K. L. 1997. Large-scale, low-frequency oceanographic effects on kelp forest succession: a tale of two cohorts. Mar. Ecol. Prog. Ser. 146:117-134. https://doi.org/10.3354/meps146117
  66. Toohey, B. D. & Kendrick, G. A. 2007. Survival of juvenile Ecklonia radiata sporophytes after canopy loss. J. Exp. Mar. Biol. Ecol. 349:170-182. https://doi.org/10.1016/j.jembe.2007.05.008
  67. Vega, J. M. A., Vasquez, J. A. & Buschmann, A. H. 2005. Population biology of the subtidal kelps Macrocystis integrifolia and Lessonia trabeculata (Laminariales, Phaeophyceae) in an upwelling ecosystem of northern Chile: interannual variability and El Nino 1997-1998. Rev. Chil. Hist. Nat. 78:33-50.
  68. Vilalta-Navas, A., Beas-Luna, R., Calderon-Aguilera, L. E., Ladah, L., Micheli, F., Christensen, V. & Torre, J. 2018. A mass-balanced food web model for a kelp forest ecosystem near its southern distributional limit in the northern hemisphere. Food Webs 17:e00091. https://doi.org/10.1016/j.fooweb.2018.e00091
  69. Watson, J. C., Hawkes, M. W., Lee, L. C. & Lamb, A. 2021. The dynamics and geographic disjunction of the kelp Eisenia arborea along the west coast of Canada. Bot. Mar. 64:395-406. https://doi.org/10.1515/bot-2021-0040
  70. Wernberg, T. 2005. Holdfast aggregation in relation to morphology, age, attachment and drag for the kelp Ecklonia radiata. Aquat. Bot. 82:168-180. https://doi.org/10.1016/j.aquabot.2005.04.003
  71. Wernberg, T., Krumhansl, K., Filbee-Dexter, K. & Pedersen, M. F. 2019. Status and trends for the world's kelp forests. In Sheppard, C. (Ed.) World Seas: An Environmental Evaluation. Vol. 3. Ecological Issues and Environmental Impacts. Academic Press, Cambridge, MA, pp. 57-78.
  72. Young, M., Cavanaugh, K., Bell, T., Raimondi, P., Edwards, C. A., Drake, P. T., Erikson, L. & Storlazzi, C. 2016. Environmental controls on spatial patterns in the long-term persistence of giant kelp in central California. Ecol. Monogr. 86:45-60. https://doi.org/10.1890/15-0267.1