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Ecological priming of artificial aquaculture structures: kelp farms as an example

Published online by Cambridge University Press:  27 September 2018

AM Walls Open the ORCID record for AM Walls [Opens in a new window] ,
MD Edwards ,
LB Firth  and
MP Johnson
AM Walls*
Affiliation:
Irish Seaweed Research Group, Ryan Institute, National University of Ireland, Galway, Ireland
MD Edwards
Affiliation:
Irish Seaweed Research Group, Ryan Institute, National University of Ireland, Galway, Ireland
LB Firth
Affiliation:
School of Biological and Marine Sciences, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK
MP Johnson
Affiliation:
Irish Seaweed Research Group, Ryan Institute, National University of Ireland, Galway, Ireland
*
Author for correspondence: AM Walls, E-mail: [email protected]
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Abstract

The continued development of the aquaculture industry is contributing to the proliferation of artificial structures in the marine environment. Observations of seaweed farms (infrastructure and biomass) suggest they act as a habitat for associated species. Seaweed farms differ from other forms of artificial infrastructure as the material deployed already has marine organisms (i.e. culture species) growing on it. This ‘priming’ of ropes with juvenile sporophytes may affect future development of communities by facilitating colonizing species or suppressing competitors. We call this process ‘ecological priming’: the provision of a biological platform that influences the successional development of specific communities. The communities that developed on ropes primed with Alaria esculenta individuals were compared with unprimed ropes to assess the ecological priming effect, at a commercial kelp farm in south-west Ireland. Species richness increased over two cultivation seasons and species composition was consistent between years, with distinct communities developing on primed and unprimed treatments. Timing of species occurrence on primed ropes was predictable with no predictable pattern occurring on unprimed ropes. Multivariate tests indicated distinct communities between treatments, with suppression of other algal species and potential facilitation of some species that have a particular association with A. esculenta on primed ropes. Communities from primed holdfasts contained a lower diversity of algal species compared with unprimed communities. Cultivated kelp holdfasts represent a habitat for distinct assemblages that reflect ecological priming of the substratum.

Keywords

Alaria esculentaaquacultureartificial structuresepibiontsfacilitationholdfastskelp farmmacroalgaepredictability
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 4 , June 2019 , pp. 729 - 740
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Airoldi, L and Beck, MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanography and Marine Biology: An Annual Review 35, 345–405.Google Scholar
Anderson, MJ, Gorley, RN and Clarke, KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. Plymouth: PRIMER-E.Google Scholar
Antoniadou, C (2014) Succession patterns of polychaetes on algal-dominated rocky cliffs (Aegean Sea, Eastern Mediterranean). Marine Ecology 35, 281–291.Google Scholar
Arroyo, NL, Maldonado, M, Pérez-Portela, R and Benito, J (2004) Distribution patterns of meiofauna associated with a sublittoral Laminaria bed in the Cantabrian Sea (north-eastern Atlantic). Journal of Marine Biology 144, 231–242.Google Scholar
Baselga, A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19, 134–143.Google Scholar
Beaumont, NJ, Austen, MC, Atkins, JP, Burdon, D, Degraer, S, Dentinho, TP, Derous, S, Holm, P, Horton, T, van Ierland, E, Marboe, AH, Starkey, DJ, Townsend, M and Zarzycki, T (2007) Identification, definition and quantification of goods and services provided by marine biodiversity: implications for the ecosystem approach. Marine Pollution Bulletin 54, 253–265.Google Scholar
Benedetti-Cecchi, L (2000) Predicting direct and indirect interactions during succession in a mid-littoral rocky shore assemblage. Ecological Monographs 70, 45–72.Google Scholar
Benedetti-Cecchi, L and Cinelli, F (1993) Early patterns of algal succession in a midlittoral community of the Mediterranean sea: a multifactorial experiment. Journal of Experimental Marine Biology and Ecology 169, 15–31.Google Scholar
Bishop, MJ, Mayer-Pinto, M, Airoldi, L, Firth, LB, Morris, RL, Loke, LHL, Hawkins, SJ, Naylor, LA, Coleman, RA, Chee, SY and Dafforn, KA (2017) Effects of ocean sprawl on ecological connectivity: impacts and solutions. Journal of Experimental Marine Biology and Ecology 492, 7–30.Google Scholar
Blight, AJ and Thompson, RC (2008) Epibiont species richness varies between holdfasts of a northern and a southerly distributed kelp species. Journal of the Marine Biological Association of the United Kingdom 88, 469–475.Google Scholar
Bunker, FSD, Maggs, CA, Brodie, JA and Bunker, AR (2012) Seaweeds of Britain and Ireland. Plymouth: Wild Nature Press.Google Scholar
Carney, LT, Waaland, JR, Klinger, T and Ewing, K (2005) Restoration of the bull kelp Nereocystis luetkeana in nearshore rocky habitats. Marine Ecology Progress Series 302, 49–61.Google Scholar
Chapman, MG and Underwood, AJ (2011) Evaluation of ecological engineering of “armoured” shorelines to improve their value as habitat. Journal of Experimental Marine Biology and Ecology 400, 302–313.Google Scholar
Christie, H, Jørgensen, NM, Norderhaug, KM and Waage-Nielsen, E (2003) Species distribution and habitat exploitation of fauna associated with kelp (Laminaria digitata) along the Norwegian coast. Journal of the Marine Biological Association of the United Kingdom 83, 687–699.Google Scholar
Christie, H, Jørgensen, NM and Norderhaug, KM (2007) Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp. Journal of Sea Research 58, 198–208.Google Scholar
Cifuentes, M, Krueger, I, Dumont, CP, Lenz, M and Thiel, M (2010) Does primary colonization or community structure determine the succession of fouling communities? Journal of Experimental Marine Biology and Ecology 395, 10–20.Google Scholar
Clarke, KR and Warwick, RM (1994) Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd Edn. Plymouth: PRIMER-E.Google Scholar
Colebrook, JM (1979) Continuous plankton records: seasonal cycles of phytoplankton and copepods in the North Atlantic Ocean and the North Sea. Marine Biology 51, 23–32.Google Scholar
Connell, JH and Slatyer, RO (1977) Mechanisms of succession in natural communities and their role in community stability and organisation. American Naturalist 111, 1119–1144.Google Scholar
Dafforn, KA, Glasby, TM, Airoldi, L, Rivero, NK, Mayer-Pinto, M and Johnston, EL (2015) Marine urbanization: an ecological framework for designing multifunctional artificial structures. Frontiers in Ecology and the Environment 13, 82–90.Google Scholar
Dayton, PK, Currie, V, Gerrodette, T, Keller, BD, Rosenthal, R and Tresca, DV (1984) Patch dynamics and stability of some California kelp communities. Ecological Monographs 54, 253–289.Google Scholar
Dean, RL and Connell, JH (1987) Marine invertebrates in an algal succession. I. Variations in abundance and diversity with succession. Journal of Experimental Marine Biology and Ecology 109, 195–215.Google Scholar
Duarte, CM, Pitt, KA, Lucas, CH, Purcell, JE, Uye, S-I, Robinson, K, Brotz, L, Decker, MB, Sutherland, KR, Malej, A, Madin, L, Mianzan, H, Gili, J-M, Fuentes, V, Atienza, D, Pagés, F, Breitburg, D, Malek, J, Graham, WM and Condon, RH (2012) Is global ocean sprawl a cause of jelly fish blooms? Frontiers in Ecology and the Environment 11, 91–97.Google Scholar
Edwards, M and Richardson, AJ (2004) Impacts of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884.Google Scholar
Edwards, M and Watson, L (2011) Cultivating Laminaria digitata. Aquaculture Explained No. 26. Dublin: Irish Seas Fisheries Board.Google Scholar
Eriksson, BK, Johansson, G and Snoeijs, P (2002) Long-term changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak coast. Journal of Phycology 38, 284–296.Google Scholar
Evans, AJ, Firth, LB, Hawkins, SJ, Morris, ES, Goudge, H and Moore, PJ (2016) Drill-cored rock pools: an effective method of ecological enhancement on artificial structures. Marine and Freshwater Research 67, 123–130.Google Scholar
FAO (2016) The State of World Fisheries and Aquaculture 2016. Rome: FAO.Google Scholar
Ferrario, F, Iveša, L, Jaklin, A, Perkol-Finkel, S and Airoldi, L (2016) The overlooked role of biotic factors in controlling the ecological performance of artificial marine habitats. Journal of Applied Ecology 53, 16–24.Google Scholar
Firth, LB and Hawkins, SJ (2011) Introductory comments – global change in marine ecosystems: patterns, processes and interactions with regional and local scale impacts. Journal of Experimental Marine Biology and Ecology 400, 1–6.Google Scholar
Firth, LB, Thompson, RC, White, FJ, Schofield, M, Skov, MW, Hoggart, SPG, Jackson, J, Knights, AM and Hawkins, SJ (2013) The importance of water-retaining features for biodiversity on artificial intertidal coastal defence structures. Diversity and Distributions 19, 1275–1283.Google Scholar
Firth, LB, Knights, AM, Bridger, D, Evans, AJ, Mieszkowska, N, Moore, PJ, O'Connor, NE, Sheehan, EV, Thompson, RC and Hawkins, SJ (2016a) Ocean sprawl: challenges and opportunities for biodiversity management in a changing world. Oceanography and Marine Biology: An Annual Review 54, 189–262.Google Scholar
Firth, LB, Browne, KA, Knights, AM, Hawkins, SJ and Nash, R (2016b) Eco-engineered rock pools: a concrete solution to biodiversity loss and urban sprawl in the marine environment. Environmental Research Letters 11, 94015.Google Scholar
Førde, H, Forbord, S, Handå, A, Fossberg, J, Ariff, J, Johnsen, G and Reitan, KI (2016) Development of bryozoan fouling on cultivated kelp (Saccharina latissim) in Norway. Journal of Applied Phycology 28, 1225–1234.Google Scholar
Guiry, MD (1989) Uses and Cultivation of Seaweed. Lecce: Camera di Commercio Industria Artigiantoe Agricoltura; Università Degli Studi.Google Scholar
Hauser, A, Attrill, MJ and Cotton, PA (2006) Effects of habitat complexity on the diversity and abundance of macrofauna colonising artificial kelp holdfasts. Marine Ecology Progress Series 325, 93–100.Google Scholar
Hayward, PJ (1988) Animals on Seaweed. Great Britain. Richmond: The Richmond Publishing Co.Google Scholar
Hayward, PJ and Ryland, JS (2002) Handbook of the Marine Fauna of North-West Europe. Oxford: Oxford University Press.Google Scholar
Heery, EC, Bishop, MJ, Critchley, LP, Bugnot, AB, Airoldi, L, Mayer-Pinto, M, Sheehan, EV, Coleman, RA, Loke, LH, Johnston, EL and Komyakova, V (2017) Identifying the consequences of ocean sprawl for sedimentary habitats. Journal of Experimental Marine Biology and Ecology 492, 31–48.Google Scholar
Herben, T (2005) Species pool size and invasibility of island communities: a null model of sampling effects. Ecology Letters 8, 909–917.Google Scholar
Hood, GM (2014) PopTools version 3.2.5. Available at http://www.poptools.org.Google Scholar
Jenkins, S and Martins, G (2010) Succession on hard substrata In Dürr, S and Thomason, J (eds), Biofouling. Oxford: Wiley-Blackwell, pp. 60–72.Google Scholar
Jessopp, M, Mulholland, OR, McAllen, R, Johnson, MP, Crowe, TP and Allcock, AL (2007) Coastline configuration as a determinant of structure in larval assemblages. Marine Ecology Progress Series 352, 67–75.Google Scholar
Jones, DJ (1971) Ecological studies on macroinvertebrate populations associated with polluted kelp forests in the North Sea. Helgoländer Wissenschaftliche Meeresuntersuchungen 22, 417–441.Google Scholar
Jones, DJ (1972) Changes in the ecological balance of invertebrate communities in kelp holdfast habitats of some polluted North Sea waters. Helgoländer Wissenschaftliche Meeresuntersuchungen 23, 417–441.Google Scholar
Kain, JM (1963) Aspects of the biology of Laminaria hyperborea. II. Age. Weight. Length. Journal of the Marine Biological Association of the United Kingdom 43, 129–151.Google Scholar
Kruskal, JB (1964a) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29, 115–129.Google Scholar
Kruskal, JB (1964b) Multidimensional scaling by optimizing goodness-of-fit to a nonmetric hypothesis. Psychometrika 29, 115–129.Google Scholar
Marzinelli, EM, Zagal, CJ, Chapman, MG and Underwood, AJ (2009) Do modified habitats have direct or indirect effects on epifauna? Ecology 90, 2948–2955.Google Scholar
Marzinelli, EM, Leong, MR, Campbell, AH, Steinberg, PD and Vergés, A (2016) Does restoration of a habitat-forming seaweed restore associated faunal diversity? Restoration Ecology 24, 81–90.Google Scholar
Moore, P (1972) Particulate matter in the sublittoral zone of an exposed coast and its ecological significance with special reference to the fauna inhabiting kelp holdfasts. Journal of Experimental Marine Biology and Ecology 10, 59–80.Google Scholar
Moore, P (1973) The kelp fauna of northeast Britain. I. Introduction and the physical environment. Journal of Experimental Marine Biology and Ecology 13, 97–125.Google Scholar
Moore, PJ, Thompson, RC and Hawkins, SJ (2011) Phenological changes in intertidal conspecific gastropods in response to climate warming. Global Change Biology 17, 709–719.Google Scholar
Norderhaug, KM (2004) Use of red algae as hosts by kelp-associated amphipods. Marine Biology 144, 225–230.Google Scholar
Norderhaug, KM, Christie, H and Rinde, E (2002) Colonisation of kelp imitations by epiphyte and holdfast fauna; a study of mobility patterns. Journal of Marine Biology 141, 965–973.Google Scholar
Ojeda, FP and Santelices, B (1984) Invertebrate communities in holdfasts of the kelp Macrocystis pyrifera from southern Chile. Marine Ecology Progress Series 16, 65–73.Google Scholar
Paalvast, P, van Wesenbeeck, BK, van der Velde, G and de Vries, MB (2012) Pole and pontoon hulas: an effective way of ecological engineering to increase productivity and biodiversity in the hard-substrate environment of the port of Rotterdam. Ecological Engineering 44, 199–209.Google Scholar
Park, TS, Rho, YG, Gong, YG and Lee, DY (1990) A harpacticoid copepod parasitic in the cultivated brown alga Undaria pinnatifida in Korea. Bulletin of the Korean Fisheries Society 23, 439–442.Google Scholar
Perkol-Finkel, S and Sella, I (2015) Harnessing urban coastal infrastructure for ecological enhancement. Proceedings of the Institution of Civil Engineers 168, 102–110.Google Scholar
Perkol-Finkel, S, Ferrario, F, Nicotera, V and Airoldi, L (2012) Conservation challenges in urban seascapes: promoting the growth of threatened species on coastal infrastructures. Journal of Applied Ecology 49, 1457–1466.Google Scholar
Peteiro, C and Freire, Ó (2013) Epiphytism on blades of the edible kelps Undaria pinnatifida and Saccharina latissima farmed under different abiotic conditions. Journal of the World Aquaculture Society 44, 706–715.Google Scholar
Platt, WJ and Connell, JH (2003) Natural disturbances and directional replacement of species. Ecological Monographs 73, 507–522.Google Scholar
Ryland, J (1962) The association between polyzoa and algal substrata. Journal of Animal Ecology 31, 331–338.Google Scholar
Ryland, JS and Hayward, PJ (1977) British Anascan Bryozoans. London: Academic Press.Google Scholar
Scarratt, DJ (1961) The Fauna of Laminaria Holdfasts (PhD thesis). University of Wales, Aberystwyth.Google Scholar
Schaal, G, Riera, P and Leroux, C (2009) Trophic significance of the kelp Laminaria digitata (Lamour.) for the associated food web: a between-sites comparison. Estuarine, Coastal and Shelf Science 85, 565–572.Google Scholar
Schaal, G, Riera, P and Leroux, C (2012) Food web structure within kelp holdfasts (Laminaria): a stable isotope study. Journal of Marine Ecology 33, 370–376.Google Scholar
Schultze, K, Janke, K, Krüß, A and Weidemann, W (1990) The macrofauna and macroflora associated with Laminaria digitata and L. hyperborea at the island of Helgoland (German Bight, North Sea). Helgoländer Meeresuntersuchungen 44, 39–51.Google Scholar
Shepard, R (1962) The analysis of proximities: multidimensional scaling with an unknown distance function. II. Psychometrika 27, 219–246.Google Scholar
Sheppard, CRC, Bellamy, DJ and Sheppard, ALS (1980) Study of the fauna inhabiting the holdfasts of Laminaria hyperborea (gunn.) fosl. along some environmental and geographical gradients. Marine Environmental Research 4, 25–51.Google Scholar
Smale, DA, Burrows, MT, Moore, P, O'Connor, N and Hawkins, SJ (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution 3, 4016–4038.Google Scholar
Smith, SDA (1996) The macrofaunal community of Ecklonia radiata holdfasts: variation associated with sediment regime, sponge cover and depth. Australian Journal of Ecology 21, 144–153.Google Scholar
Smith, SDA (2000) Evaluating stress in rocky shore and shallow reef habitats using the macrofauna of kelp holdfasts. Journal of Aquatic Ecosystem Stress and Recovery 7, 259–272.Google Scholar
Smith, SDA, Simpson, RD and Cairns, SC (1996) The macrofaunal community of Ecklonia radiata holdfasts: description of the faunal assemblage and variation associated with differences in holdfast volume. Australian Journal of Ecology 21, 81–95.Google Scholar
Sousa, WP (1979) Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecological Monographs 49, 227–254.Google Scholar
Steneck, RS and Dethier, MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69, 476.Google Scholar
Strain, EMA, Morris, RL, Coleman, RA, Figueira, WF, Steinberg, PD, Johnston, EL and Bishop, MJ (2017a) Increasing microhabitat complexity on seawalls can reduce fish predation on native oysters. Ecological Engineering 7, 9567–9579.Google Scholar
Strain, EMA, Olabarria, C, Mayer-Pinto, M, Cumbo, V, Morris, RL, Bugnot, AB, Dafforn, KA, Heery, E, Firth, LB, Brooks, P and Bishop, MJ (2017b) Eco-engineering urban infrastructure for marine and coastal biodiversity: which interventions have the greatest ecological benefit? Journal of Applied Ecology 55, 426–441.Google Scholar
Teagle, H, Hawkins, SJ, Moore, PJ and Smale, DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology 492, 81–98.Google Scholar
Tett, P (1990) A three layer vertical and microbiological process model for shelf seas. Birkenhead: Proudman Oceanographic Laboratory, Report no. 14, 85 pp.Google Scholar
Thiel, M and Vásquez, J (2000) Are kelp holdfasts islands on the ocean floor? Indication for temporarily closed aggregations of peracarid crustaceans. Hydrobiologia 440, 45–54.Google Scholar
Tuya, F, Larsen, K and Platt, V (2011) Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658, 373–382.Google Scholar
Underwood, AJ and Chapman, MG (2006) Early development of subtidal macrofaunal assemblages: relationships to period and timing of colonization. Journal of Experimental Marine Biology and Ecology 330, 221–233.Google Scholar
Valdivia, N, Buschbaum, C and Thiel, M (2014) Succession in intertidal mussel bed assemblages on different shores: species mobility matters. Marine Ecology Progress Series 497, 131–142.Google Scholar
Walls, AM, Kennedy, R, Fitzgerald, RD, Blight, AJ, Johnson, MP and Edwards, MD (2016) Potential novel habitat created by holdfasts from cultivated Laminaria digitata: assessing the macroinvertebrate assemblages. Aquaculture Environment Interactions 8, 157–169.Google Scholar
Walls, AM, Edwards, MD, Firth, LB and Johnson, MP (2017) Successional changes of epibiont fouling communities of the cultivated kelp Alaria esculenta: predictability and influences. Aquaculture Environment Interactions 9, 55–69.Google Scholar
WoRMS Editorial Board (2016) World Register of Marine Species. Available at http://www.marinespecies.org.Google Scholar
Yu, YQ, Zhang, QS, Tang, YZ, Zhang, SB, Lu, ZC, Chu, SH and Tang, XX (2012) Establishment of intertidal seaweed beds of Sargassum thunbergii through habitat creation and germling seeding. Ecological Engineering 44, 10–17.Google Scholar
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