Feeding preference of the native sea urchin Arbacia dufresnii in an environment invaded by the kelp Undaria pinnatifida
Palabras clave:
Food preference, echinoid, invasive kelp, PatagoniaResumen
In Argentina, the invasive kelp Undaria pinnatifida has modified the benthic community of Nuevo Gulf, northern Patagonia, where it was first recorded and is currently showing advanced invasion. Arbacia dufresnii, an abundant generalist omnivore sea urchin, has fully incorporated U. pinnatifida into its diet. Since sea urchins can influence the structure and dynamics of benthic macroalgal assemblages, determining the importance of U. pinnatifida in the feeding preferences of A. dufresnii complements the evaluation of the modifications caused by this species. Thus, this study aimed to assess the feeding preference of A. dufresnii in an environment invaded by U. pinnatifida. We conducted feeding experiments to determine whether A. dufresnii feeds on different developmental stages of U. pinnatifida, and preference experiments of this invasive species against six macroalgal species abundant in the environment. Arbacia dufresnii consumed both blades and sporophylls of U. pinnatifida at all the developmental stages evaluated, showing a preference for blades over sporophylls. Arbacia dufresnii showed preference for U. pinnatifida only when it was offered together with species that possess defense mechanisms against herbivory. The lack of preference for other macroalgae species over U. pinnatifida suggests that this invasive species may alter resource use and thereby affect the trophic structure of native communities. These findings complement previous diet studies, corroborating the feeding plasticity of A. dufresnii, as well as its ability to adapt to newly available resources. This research enhances the understanding of the impacts caused by invasive macroalgal species through feeding ecology studies of native grazers.
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Aguilera, M.A. (2011). The functional roles of herbivores in the rocky intertidal systems in Chile: A review of food preferences and consumptive effects. Revista Chilena de Historia Natural, 84(2), 241-261.
Angell, A.R., Pirozzi, I., de Nys, R., & Paul, N.A. (2012). Feeding preferences and the nutritional value of tropical algae for the Abalone Haliotis asinina. PLoS One, 7(6), e38857. https://doi.org/10.1371/journal.pone.0038857
Ank, G., Paradas, W.D., Amado Filho, G.M., Gama, B.D., & Pereira, R. C. (2014). Within-thallus variation on phlorotannin contents and physodes amount in Stypopodium zonale (Phaeophyceae). Pan-American Journal of Aquatic Sciences, 9, 1-7
Arijón, M., Ponce, N.M., Solana, V., Dellatorre, F.G., Latour, E.A., & Stortz, C. A. (2021). Monthly fluctuations in the content and monosaccharide composition of fucoidan from Undaria pinnatifida sporophylls from northern Patagonia. Journal of Applied Phycology, 33(4), 2433-2441. https://doi.org/10.1007/s10811-021-02465-5
Arijón, M., Raffo, M. P., Sánchez, N., & Dellatorre, F. G. (2023). Photosynthetic pigments and color of wild Undaria pinnatifida for wakame production (Chubut, Patagonia Argentina). Algal Research, 69, 102918. https://doi.org/10.1016/j.algal.2022.102918
Boraso, A., & Zaixso, J.M. (2011). Atlas de sensibilidad ambiental de la costa y el Mar Argentino. Algas marinas bentónicas, 1-28.
Brogger, M.I., Gil, D.G., Rubilar, T., Martinez, M.I., Díaz de Vivar, M.E., Escolar, M., ... & Tablado, A. (2013). Echinoderms from Argentina: Biodiversity, distribution and current state of knowledge. In: Alvarado, J.J., & Marin Solís, F.A. (eds) Echinoderm research and diversity in Latin America, 359-402.
Cacabelos, E., Olabarria, C., Incera, M., & Troncoso, J.S. (2010). Do grazers prefer invasive seaweeds? Journal of Experimental Marine Biology and Ecology, 393, 182–187. https://doi.org/10.1016/j.jembe.2010.07.024
Casas, G. N., & Piriz, M. L. (1996). Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia, 326(1), 213-215. https://doi.org/10.1007/BF00047809
Casas, G., Scrosati, R., & Luz Piriz, M. (2004). The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biological invasions, 6, 411-416. https://doi.org/10.1023/B:BINV.0000041555.29305.41
Casas, G.N., Piriz, M.L., & Parodi, E R. (2008). Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). Journal of the Marine Biological Association of the United Kingdom, 88(1), 21–28. https://doi.org/10.1017/S0025315408000246
Castro, K.L., Epherra, L., Raffo, M.P., Morsan, E., & Rubilar, T. (2022). Changes in the diet of the native sea urchin Arbacia dufresnii at different scenarios of the Undaria pinnatifida invasion (Patagonia, Argentina). Food Webs, 31, e00221. https://doi.org/10.1016/j.fooweb.2022.e00221
Choi, H.G., Kim, Y.S., Lee, S.J., & Nam, K.W. (2007). Growth and reproductive patterns of Undaria pinnatifida sporophytes in a cultivation farm in Busan, Korea. Journal of applied phycology, 19, 131-138. https://doi.org/10.1007/s10811-006-9119-6
Cronin, G., & Hay, M.E. (1996). Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology, 77, 1531-1543. https://doi.org/10.2307/2265549.
Cyrus, M., Bolton, J., Scholtz, R., & Macey, B. (2015). The advantages of Ulva (Chlorophyta) as an additive in sea urchin formulated feeds: effects on palatability, consumption and digestibility. Aquaculture Nutrition, 21(5), 578-591. https://doi.org/10.1111/anu.12182
Davidson, A.D., Campbell, M.L., Hewitt, C.L., & Schaffelke, B. (2015). Assessing the impacts of nonindigenous marine macroalgae: an update of current knowledge. Botanica Marina, 58(2), 55-79. https://doi.org/10.1515/bot-2014-0079
Dellatorre, F.G., Amoroso, R.O., Saravia, J., & Orensanz, J.M. (2014). Rapid expansion and potential range of the invasive kelp Undaria pinnatifida in the southwestern Atlantic. Aquatic Invasions, 9(4), 467–478. http://dx.doi.org/10.3391/ai.2014.9.4.05
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., & Robledo, C.W. (2019). InfoStat versión 2019. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL http://www.infostat.com.ar.
Haavisto, F., Koivikko, R., & Jormalainen, V. (2017) Defensive role of macroalgal phlorotannins: benefits and trade-offs under natural herbivory. Marine Ecology Progress Series, 566, 79-90. https://doi.org/10.3354/meps12004
Hay, M.E., Lee, R.R., & Guieb, R.A. (1986). Food preference and chemotaxis in the sea urchin Arbacia punctulata (Lamarck) Philippi. Journal of Experimental Marine Biology and Ecology, 96(2), 147-153. https://doi.org/10.1016/0022-0981(86)90239-X
Irigoyen, A.J., Trobbiani, G., Sgarlatta, M.P., & Raffo, M.P. (2011). Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biological Invasions, 13(7), 1521-1532. https://doi.org/10.1007/s10530-010-9910-9
Jackson, A.C., & Underwood, A.J. (2007). Application of new techniques for the accurate analysis of choice of prey. Journal of Experimental Marine Biology and Ecology, 341(1), 1-9. https://doi.org/10.1016/j.jembe.2006.11.002
Kulhanek, S.A., Ricciardi, A., & Leung, B. (2011). Is invasion history a useful tool for predicting the impacts of the world's worst aquatic invasive species?. Ecological Applications, 21(1), 189-202. https://doi.org/10.1890/09-1452.1
Lawrence, J.M. (1975). On the relationships between marine plants and sea urchin. Oceanography and marine biology: an annual review, 13, 213-286.
Littler, M. M., Littler, D.S., & Taylor, P.R. (1983). Evolutionary strategies in a tropical barrier reef system: functional‐form groups of marine macroalgae. Journal of Phycology, 19(2), 229-237. https://doi.org/10.1111/j.0022-3646.1983.00229.x
Lyons, D.A., & Scheibling, R.E. (2007). Effect of dietary history and algal traits on feeding rate and food preference in the green sea urchin Strongylocentrotus droebachiensis. Journal of Experimental Marine Biology and Ecology, 349, 194–204. https://doi.org/10.1016/j.jembe.2007.05.012
Manly, B.F.J. (1993). Comments on design and analysis of multiple-choice feeding-preference experiments. Oecologia, 93(1), 149-152.
Martins, I., Leite, N., & Constantino, E. (2014). Consumption and feeding preference of Echinogammarus marinus on two different algae: Fucus vesiculosus and Ulva
intestinalis. Journal of Sea Research, 85, 443–446.
https://doi.org/10.1016/j.seares.2013.07.017.
Navarrete, A.H., Camus, P. A., & Opazo, L.F. (2008). Variación ambiental y patrones dietarios del erizo negro Tetrapygus niger en costas intermareales rocosas del norte de Chile. Revista Chilena de Historia Natural, 81, 305-319. http://dx.doi.org/10.4067/S0716-078X2008000300001
Newcombe, E.M., Cárdenas, C.A., & Geange, S.W. (2012). Green sea urchins structure invertebrate and macroalgal communities in the Magellan Strait, southern Chile. Aquatic Biology, 15(2), 135-144. https://doi.org/10.3354/ab00410
Paul, V.J., Cruz- Rivera, E., & Thacker, R.W. (2001). Chemical mediation of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In J.B. McClintock & B.J. Baker (Eds.), Marine chemical ecology (pp. 227-265). Boca Raton: CRC Press.
Pereira, R.C., Cavalcanti, D.N., & Teixeira, V.L. (2000). Effects of secondary metabolites from the tropical Brazilian brown alga Dictyota menstrualis on the amphipod Parhyale hawaiensis. Marine Ecology Progress Series, 205, 95-100. https://doi.org/10.3354/meps205095
Penchaszadeh, P., & Lawrence, J. (1999). Arbacia dufresnei (Echinodermata: Echinoidea): A carnivore in Argentinian waters In M. D. Candia Carnevali & F. Bonasoro (Eds.), Echinoderm Research (pp. 525-530). Rotterdarm: A.A. Balkema.
Raffo, M. P. (2014). Algas nativas y exóticas en los intermareales rocosos de la Patagonia argentina: patrones y procesos ecológicos. Doctoral dissertation, Universidad Nacional del Comahue, Bariloche.
Raffo, M.P., Faleschini, M., Casas, G.N., & Schwindt, E. (2015). Efecto de sombreado del alga exótica Undaria pinnatifida sobre la comunidad de macroalgas en pozas de marea (Patagonia, Argentina). In: Riccialdelli, L., Sotelano, P., Boy, C.C. (Eds.), IX Jornadas Nacionales de Ciencias del Mar y XVII Coloquio de Oceanografía: Ciencia y Sociedad: Integrando saberes en los estudios del mar. Ushuaia, Argentina, p. 287.
Roy, H.E., Pauchard, A., Stoett, P., Renard Truong, T., Lipinskaya, T., & Vicente, J. R. (2023). Chapter 1: Introducing biological invasions and the IPBES thematic assessment of invasive alien species and their control. In: Roy, H.E., Pauchard, A., Stoett, P., & Renard Truong, T. (eds.). Thematic Assessment Report on Invasive Alien Species and their Control of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES secretariat, Bonn, Germany. https://doi.org/10.5281/zenodo.7430723
Santamaría, J., Golo, R., Verdura, J., Tomas, F., Ballesteros, E., Alcoverro, T., Arthur, R., & Cebrian, E. (2022). Learning takes time: Biotic resistance by native herbivores
increases through the invasion process. Ecology Letters, 25(11), 2525-2539.
https://doi.org/10.1111/ele.14115.
Seebens, H., Meyerson, L.A., Rahlao, S.J., Lenzner, B., Tricarico, E., Aleksanyan, A., & Pyšek, P. (2023). Chapter 2. Trends and status of alien and invasive alien species. In: Roy, H.E., Pauchard, A., Stoett, P., & Renard Truong, T. (eds.). Thematic Assessment Report on Invasive Alien Species and Their Control of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, PBES secretariat, Bonn, Germany. 1-264. https://doi.org/10.5281/zenodo.7430725
Scheibling, R., & Anthony, S. (2001). Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Marine Biology, 139, 129-146. https://doi.org/10.1007/s002270100567
Singer, M. C. (2000). Reducing ambiguity in describing plant-insect interactions:" preference"," acceptability" and" electivity". Ecology Letters, 3(3), 159-162.
Skriptsova, A.V., Shevchenko, N.M., Zvyagintseva, T.N., & Imbs, T. I. (2010). Monthly changes in the content and monosaccharide composition of fucoidan from Undaria pinnatifida (Laminariales, Phaeophyta). Journal of Applied Phycology, 22, 79-86. https://doi.org/10.1007/s10811-009-9438-5
Skriptsova, A.V. (2016). Seasonal variations in the fucoidan content of brown algae from Peter the Great Bay, Sea of Japan. Russian Journal of Marine Biology, 42, 351-356. https://doi.org/10.1134/S1063074016040106
Solana, V.P. (2022). Caracterización fisicoquímica y nutricional del alga invasora Undaria pinnatifida (Phaeophyceae, Laminariales) y estudio de parámetros de procesamiento y almacenamiento para su utilización en la producción de wakame. Doctoral dissertation, Universidad Nacional de La Plata.
Souza, C.F., Oliveira, A.S.d., & Pereira, R.C. (2008). Feeding preference of the sea urchin Lytechinus variegatus (Lamarck, 1816) on seaweeds. Brazilian Journal of Oceanography, 56, 239-247.
Spiers, L. J., Harrison, S. J., Deutsch, J. M., Garg, N., & Paul, V. J. (2021). The role of algal chemical defenses in the feeding preferences of the long-spined sea urchin Diadema antillarum. Aquatic Ecology, 55(3), 941-953. https://doi.org/10.1007/s10452-021-09873-2
Teso, S.V., Bigatti, G., Casas, G.N., Piriz, M.L., & Penchaszadeh, P.E. (2009). Do native grazers from Patagonia, Argentina consume the invasive kelp Undaria pinnatifida? Revista Museo Argentino de Ciencias Naturales, 11(1), 7-14.
Thornber, C.S., Kinlan, B.P., Graham, M.H., & Stachowicz, J.J. (2004). Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and
biological controls on demography. Marine Ecology Progress Series, 268, 69–80. https://doi.org/10.3354/meps268069
Trowbridge, C.D. (1995). Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. Journal of Ecology, 83(6), 949-965. https://doi.org/10.2307/2261177
Underwood, A.J., & Clarck, K.R. (2005). Solving some statistical problems in analyses of experiments on choices of food and on associations with habitat. Journal of Experimental Marine Biology and Ecology, 318, 227–237. https://doi.org/10.1016/j.jembe.2004.12.014.
Valentine, J.P., & Johnson, C.R. (2003). Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. Journal of Experimental Marine Biology and Ecology, 295(1), 63-90. https://doi.org/10.1016/S0022-0981(03)00272-7
Vásquez, J., Castilla, J.C., & Santelices, B. (1984) Distributional patterns and diets of four species of sea urchins in giants kelp forest (Macrocystis pyrifera) of Puerto Toro, Navarino Islands, Chile. Marine Ecology Progress Series, 9(1), 55-63.
Van Alstyne, K.L., Whitman, S.L., & Ehlig, J.M. (2001). Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Marine Biology, 139, 201-210. https://doi.org/10.1007/s002270000507
Van Alstyne, K.L., Pelletreau, K.N., & Kirby, A. (2009). Nutritional preferences override chemical defenses in determining food choice by a generalist herbivore, Littorina sitkana. Journal of Experimental Marine Biology and Ecology, 379(1), 85-91. https://doi.org/10.1016/j.jembe.2009.08.002
Zaixso, H.E., & Lizarralde, Z.I. (2000). Distribución de equinodermos en el golfo San José y sur del golfo San Matías (Chubut, Argentina). Revista de biología marina y oceanografía, 35(2), 127-145. http://dx.doi.org/10.4067/S0718-19572000000100002
Zárate, E.V. (2014) Biomarkers (lipids, fatty acids and stable isotopes) to examine diet of the sea urchin Evechinus chloroticus. PhD dissertation, The University of Auckland
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