When one foundation species supports another: Tubeworms facilitate an extensive kelp bed in a soft-sediment habitat
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1 When one foundation species supports another: Tubeworms facilitate an extensive kelp bed in a soft-sediment habitat MATTHEW E. S. Department of Ecology and Evolutionary Biology, University of California, 321 Steinhaus Hall, Irvine, California USA Citation: Bracken, M. E. S When one foundation species supports another: Tubeworms facilitate an extensive kelp bed in a soft-sediment habitat. Ecosphere 9(9):e /ecs Abstract. The role of foundation species dominant organisms that provide habitat for other organisms in enhancing the diversity and abundance of associated species is now well known. Less well studied are interactions between multiple, co-occurring foundation species, which collectively provide habitat for other organisms. Here, I document a unique interaction between tubeworms (Eudistylia vancouveri) and two kelp species (Alaria marginata and Saccharina latissima). Kelps large brown macroalgae in the order Laminariales require hard substrates for attachment and are therefore typically restricted to rocky reefs. However, while exploring a remote coastline in southeastern Alaska, USA, I observed an extensive kelp bed, composed of both Alaria and Saccharina, growing in a location where the substrate was a mixture of mud and sand. The leathery tubes of Eudistylia formed dense hummocks that protruded from the sediment and provided a hard substratum for attachment by the kelps. Given the role that kelps, including Alaria and Saccharina, play as important facilitators of fish and invertebrates, this interaction likely represents an example of a facilitation cascade, which occurs when one species facilitates another species that subsequently enhances the diversity or abundance of associated organisms. Furthermore, the high kelp biomass likely contributes detrital inputs to the local ecosystem, potentially enhancing productivity. More generally, this observation highlights the need to understand the habitat requirements of foundation species, including the potential for other species to facilitate them. Key words: Alaria; Alaska; Eudistylia; facilitation; foundation species; habitat; kelp; Saccharina; tubeworms. Received 26 July 2018; accepted 15 August Corresponding Editor: Debra P. C. Peters. Copyright: 2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. m.bracken@uci.edu Recent work has refocused attention on the role of positive interactions in ecological communities (Stachowicz 2001). For example, foundation species (sensu Dayton 1972) organisms that dominate habitats and provide physical structure (Ellison et al. 2005, Altieri et al. 2007) enhance the diversity and abundance of associated organisms in many habitats worldwide (Angelini et al. 2011). The majority of habitat complexity in benthic marine systems is contributed by foundation species, including mussel beds, oyster reefs, and kelp forests (Bracken et al. 2007). Most studies of foundation species have focused on a single, dominant organism that enhances the diversity and abundance of associated species. However, recent work has highlighted facilitation cascades (sensu Altieri et al. 2007) whereby one foundation species supports a second foundation species such as a plant or algal epiphyte that subsequently facilitates additional associated organisms (Angelini et al. 2011, Thomsen et al. 2018). Secondary foundation species are important facilitators of biodiversity: Their effect on the diversity of associated species 1 September 2018 Volume 9(9) Article e02429
2 can be equivalent to that of primary foundation species (Thomsen et al. 2018). For example, in southeastern Alaska, USA, I observed an extensive kelp bed supported entirely by tubeworms that provided a hard, stable substrate in an otherwise unstable softsediment habitat. I documented this interaction while exploring Keku Strait and the west coast of Kupreanof Island during the summer of As I came ashore in a remote, protected cove ( N, W), I observed a kelp bed composed of Alaria marginata Postels et Ruprecht (hereafter, Alaria) and Saccharina latissima (Linnaeus) C.E. Lane, C. Mayes, Druehl et G.W. Saunders (hereafter, Saccharina) growing in the mid (Alaria) and low (Saccharina) intertidal zone and extending into the shallow subtidal zone (Fig. 1). This seemed incongruous, as the Fig. 1. The sabellid tubeworm Eudistylia vancouveri allows growth of kelps in an otherwise inhospitable softsediment habitat. Here, Saccharina latissima grows on Eudistylia low on the shore. 2 September 2018 Volume 9(9) Article e02429
3 ECOSPHERE NATURALIST in the cove one of my photographs shows at least 50 hummocks collectively supporting a substantial kelp bed (Fig. 2B). Note, however, that this interaction between kelps and tubeworms has not been documented in any other location. Tubeworms are important facilitators and ecosystem engineers in many coastal habitats, where they can alter sediment structure (Woodin 1978, Rabaut et al. 2007) and provide locations for attachment and growth of other species, including seaweeds (Dubois et al. 2006). For example, the onuphid polychaete Diopatra cuprea incorporates bivalve shells into its leathery tubes, which provide hard substrates that facilitate macroalgae such as the green alga Ulva curvata and the red seaweed Gracilaria verrucosa (Thomsen and McGlathery 2005). Similarly, the invasive reef-forming polychaete Ficopomatus enigmaticus creates hard substrates in soft-sediment lagoon habitats, enhancing the abundance of the red alga Polysiphonia subtilissima (Bazterrica et al. substrate was a mixture of mud and sand, kelps typically require a hard substrate in order to attach (Dayton 1985, Graham et al. 2003), and Alaria and Saccharina are specifically described as living on rocks (Lindeberg and Lindstrom 2010). A closer look revealed that all of the kelp individuals were actually growing on the tubes of sabellid polychaete worms (Eudistylia vancouveri Kinberg [hereafter, Eudistylia]; Figs. 1, 2). Like Alaria and Saccharina, Eudistylia is typically associated with hard substrata (Kozloff 1983). However, it can also occur in sandy mudflats (Hiebert 2016), where it forms dense hummocks composed of several worm tubes growing on each other and creating a solid surface (the leathery tubes are constructed of mucus and cemented sediment) for attachment in an otherwise softsediment habitat (Figs. 1, 2). The haptera holdfasts of the kelps were wrapped around the leathery tubes of Eudistylia (Fig. 2A), and each tubeworm hummock supported several kelp individuals. I observed numerous worm hummocks Fig. 2. (A) Haptera holdfasts of the kelps wrap around the leathery tubes of Eudistylia. (B) An extensive kelp bed occurs on this mudflat, with each tubeworm hummock supporting numerous kelp individuals. 3 September 2018 Volume 9(9) Article e02429
4 2012). However, kelps including Alaria and Saccharina in southeastern Alaska (Murphy et al. 2000) are typically primary foundation species, growing on rocky reefs and providing habitat for other, associated organisms (Bracken et al. 2007, Thomsen et al. 2018). Note that Saccharina is somewhat unique among kelps in that it also attaches to shells or small stones, allowing it to grow in soft-sediment habitats (Schaffelke et al. 1996), but these individuals functionally become drift algae, as they are not anchored to the substratum. And Macrocystis in southern California can recruit to worm tubes in soft-sediment habitats (Neushul 1971). However, it quickly outgrows the tubes, so that large individuals effectively grow on the sandy bottoms unless swept away by storms (Dayton 1985). Alaria and Saccharina also grow on the shells of live mussels (Witman and Suchanek 1984). However, mussels primarily attach to hard substrates, so kelps growing on mussels are not usually gaining access to a new habitat type (Witman 1987). An exception, somewhat analogous to the interaction I describe here, is the formation of mussel beds in soft-sediment habitats. These beds, which harbor numerous associated species, can support populations of seaweeds such as Fucus vesiculosus (Albrecht and Reise 1994), but do not facilitate kelp. In fact, a similar bed of mussels (Mytilus trossulus) was present in the same cove where I observed the kelp tubeworm interactions. This mussel bed, which overlaid the sand-and-mud substratum, was too high on the shore to support kelps. Instead, it facilitated attachment by barnacles and fucoid macroalgae. The existence of kelps in an unusual (i.e., softsediment) habitat has potentially important implications for the structure and dynamics of the local marine community. In addition to their roles as a foundation species, facilitating commercially important species such as salmon and rockfish (Murphy et al. 2000), Alaria and Saccharina are extremely productive kelps (Paine 2002). However, they are also highly susceptible to grazers, especially the chiton Katharina tunicata and the green sea urchin Strongylocentrotus droebachiensis (Himmelman et al. 1983, Paine 2002), both of which are common on nearby rocky shores (M. E. S. Bracken, personal observation). Neither of these herbivores is adept at foraging in soft-sediment habitats, so the tubeworm hummocks may provide refuges from herbivory. Thus, tubeworms may benefit the kelps in two ways: (1) directly, by providing habitat, and (2) indirectly, by limiting access by grazers. The tubeworms could also potentially facilitate the kelps by excreting limiting nutrients (Aquilino et al. 2009) or by reducing sedimentation. The resulting extensive kelp biomass (Figs. 1, 2) likely contributes a substantial amount of detritus to the local marine food web (Duggins et al. 1989). This subsidy may be particularly important to the local community, because their interaction with tubeworms allows highly productive kelps to contribute directly to a less-productive soft-sediment habitat where macroalgae do not typically grow in situ (Graham et al. 2003). More broadly, given the importance of foundation species for enhancing the biodiversity and abundance of associated organisms, this observation highlights the need to understand the habitat requirements of foundation species, including the potential for other species to facilitate them. ACKNOWLEDGMENTS I am grateful to Barry Bracken for facilitating and skippering our gunkholing expedition aboard the Island Dream. Cascade Sorte and two anonymous reviewers provided valuable comments on this contribution. LITERATURE CITED Albrecht, A., and K. Reise Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgol ander Meeresuntersuchungen 48: Altieri, A. H., B. R. Silliman, and M. D. Bertness Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. American Naturalist 169: Angelini, C., A. H. Altieri, B. R. Silliman, and M. D. Bertness Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience 61: Aquilino, K. M., M. E. S. Bracken, M. N. Faubel, and J. J. Stachowicz Local-scale nutrient regeneration facilitates seaweed growth on wave-exposed rocky shores in an upwelling system. Limnology and Oceanography 54: Bazterrica, M. C., F. Botto, and O. Iribarne Effects of an invasive reef-building polychaete on 4 September 2018 Volume 9(9) Article e02429
5 the biomass and composition of estuarine macroalgal assemblages. Biological Invasions 14: Bracken, M. E. S., B. E. Bracken, and L. Rogers- Bennett Species diversity and foundation species: potential indicators of fisheries yields and marine ecosystem functioning. California Cooperative Oceanic Fisheries Investigations Reports 48: Dayton, P. K Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Pages in Proceedings of the colloquium on conservation problems in Antarctica. Allen Press, Lawrence, Kansas, USA. Dayton, P. K Ecology of kelp communities. Annual Review of Ecology and Systematics 16: Dubois, S., J. A. Commito, F. Olivier, and C. Retiere Effects of epibionts on Sabellaria alveolata (L.) biogenic reefs and their associated fauna in the Bay of Mont Saint-Michel. Estuarine, Coastal and Shelf Science 68: Duggins, D. O., C. A. Simenstad, and J. A. Estes Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245: Ellison, A. M., et al Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3: Graham, M. H., P. K. Dayton, and J. M. Erlandson Ice ages and ecological transitions on temperate coasts. Trends in Ecology and Evolution 18: Hiebert, T. C Eudistylia vancouveri. Pages in Oregon estuarine invertebrates: Rudy s illustrated guide to common species. Third edition. University of Oregon Libraries and Oregon Institute of Marine Biology, Charleston, Oregon, USA. Himmelman, J. H., A. Cardinal, and E. Bourget Community development following removal of urchins, Strongylocentrotus droebachiensis, from the rocky subtidal zone of the St. Lawrence Estuary, Eastern Canada. Oecologia 59: Kozloff, E. N Seashore life of the northern Pacific coast. University of Washington Press, Seattle, Washington, USA. Lindeberg, M. R., and S. C. Lindstrom Field guide to seaweeds of Alaska. Alaska Sea Grant College Program, Fairbanks, Alaska, USA. Murphy, M. L., S. W. Johnson, and D. J. Csepp A comparison of fish assemblages in eelgrass and adjacent subtidal habitats near Craig, Alaska. Alaska Fishery Research Bulletin 7: Neushul, M The species of Macrocystis with particular references to those of North and South America. Beihefte zur Nova Hedwigia 32: Paine, R. T Trophic control of production in a rocky intertidal community. Science 296: Rabaut, M., K. Guilini, G. Van Hoey, M. Vincx, and S. Degraer A bio-engineered soft-bottom environment: the impact of Lanice conchilega on the benthic species-specific densities and community structure. Estuarine, Coastal and Shelf Science 75: Schaffelke, B., A. K. Peters, and T. B. H. Reusch Factors influencing depth distribution of soft bottom inhabiting Laminaria saccharina (L.) Lamour. in Kiel Bay, Western Baltic. Hydrobiologia 326(327): Stachowicz, J. J Mutualism, facilitation, and the structure of ecological communities. BioScience 51: Thomsen, M., and K. McGlathery Facilitation of macroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuarine, Coastal and Shelf Science 62: Thomsen, M. S., et al Secondary foundation species enhance biodiversity. Nature Ecology & Evolution 2: Witman, J. D Subtidal coexistence: storms, grazing, mutualism, and the zonation of kelps and mussels. Ecological Monographs 57: Witman, J. D., and T. H. Suchanek Mussels in flow: drag and dislodgement by epizoans. Marine Ecology Progress Series 16: Woodin, S. A Refuges, disturbance, and community structure: a marine soft-bottom example. Ecology 59: September 2018 Volume 9(9) Article e02429
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