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http://dx.doi.org/10.4490/algae.2022.37.2.19

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)

Publication Information

ALGAE / v.37, no.1, 2022 , pp. 63-74 More about this Journal

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

age estimation; Eisenia arborea; kelp; local spatial heterogeneity; persistence;

Citations & Related Records

Reference

1	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. DOI
2	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. DOI
3	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. DOI
4	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. DOI
5	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.
6	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.
7	Swetnam, T. W. 1993. Fire history and climate change in Giant Sequoia groves. Science 262:885-889. DOI
8	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. DOI
9	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. DOI
10	Frank, P. W. 1968. Life histories and community stability. Ecology 49:355-357. DOI
11	Matson, P. G. & Edwards, M. S. 2006. Latitudinal variation in stipe hollowing in Eisenia arborea (Phaeophyceae, Laminariales). Phycologia 45:343-348. DOI
12	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. DOI
13	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. DOI
14	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.
15	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.
16	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. DOI
17	Wernberg, T. 2005. Holdfast aggregation in relation to morphology, age, attachment and drag for the kelp Ecklonia radiata. Aquat. Bot. 82:168-180. DOI
18	Jones, C. M. 1992. Development and application of the otolith increment technique. Can. Spec. Publ. Fish. Aquat. Sci. 117:1-11.
19	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.
20	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. DOI
21	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. DOI
22	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. DOI
23	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.
24	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. DOI
25	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. DOI
26	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. DOI
27	Luning, K. & Freshwater, W. 1988. Temperature tolerance of Northeast Pacific marine algae. J. Phycol. 24:310-315. DOI
28	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. DOI
29	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. DOI
30	MacMillan, C. 1902. Observations on Pterygophora. Minn. Bot. Stud. 2:723-741.
31	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. DOI
32	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. DOI
33	Schiel, D. R. & Foster, M. S. 2015. The biology and ecology of giant kelp forests. University of California Press, Oakland, CA, 395 pp.
34	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.
35	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. DOI
36	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. DOI
37	Christie, H., Norderhaug, K. M. & Fredriksen, S. 2009. Macrophytes as habitat for fauna. Mar. Ecol. Prog. Ser. 396:221-233. DOI
38	Dawson, E. Y. 1952. Circulation within Bahia Vizcaino, Baja California, and its effects on marine vegetation. Am. J. Bot. 39:425-432. DOI
39	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. DOI
40	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.
41	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. DOI
42	Campana, S. E. & Neilson, J. D. 1985. Microstructure of fish otoliths. Can. J. Fish Aquat. Sci. 42:1014-1032. DOI
43	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.
44	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. DOI
45	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. DOI
46	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. DOI
47	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. DOI
48	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. DOI
49	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. DOI
50	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. DOI
51	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. DOI
52	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. DOI
53	Harper, J. L. 1977. Population biology of plants. Academic Press, San Diego, CA, pp. 599-643.
54	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. DOI
55	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.
56	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. DOI
57	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. DOI
58	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.
59	Tegner, M. J. & Dayton, P. K. 1987. El Nino effects on southern California kelp forest communities. Adv. Ecol. Res. 17:243-279. DOI
60	Toohey, B. D. & Kendrick, G. A. 2007. Survival of juvenile Ecklonia radiata sporophytes after canopy loss. J. Exp. Mar. Biol. Ecol. 349:170-182. DOI
61	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. DOI
62	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. DOI
63	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. DOI
64	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. DOI
65	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. DOI
66	De Wreede, R. E. 1984. Growth and age class distribution of Pterygophora californica (Phaeophyta). Mar. Ecol. Prog. Ser. 19:93-100. DOI
67	De Wreede, R. E. 1986. Demographic characteristics of Pterygophora californica (Laminariales, Phaeophyta). Phycologia 25:11-17. DOI
68	Filbee-Dexter, K. & Wernberg, T. 2018. Rise of turfs: a new battlefront for globally declining kelp forests. BioScience 68:64-76. DOI
69	Douglass, A. E. 1909. Weather cycles in the growth of big trees. Monthly Weather Rev. 37:225-237. DOI
70	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. DOI
71	Gaylord, B., Nickols, K. J. & Jurgens, L. 2012. Roles of transport and mixing processes in kelp forest ecology. J. Exp. Bio. 215:997-1007. DOI
72	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. DOI