Abstract
Seaweed farming for the production of carrageenan is a growing economic activity. Like everywhere in the marine environment, farmed algae such as Kappaphycus alvarezii can host algal organisms as epiphytes. Epiphytes ensure important functions in natural ecosystems, but these organisms can have negative impacts on their hosts and, in aquaculture be considered a plague responsible for significant economic losses. The mechanisms by which epiphytes act functionally on their hosts are multiple: shading effects, competition for nutrients or parasitism. Parasitism is characterised by the epiphyte diverting a proportion of the host’s resources. The objective of our work was to assess the impact of the epiphyte Polysiphonia sp. on the N and C acquisition of its farmed host K. alvarezii using two isotopic experiments with 13C and 15N as tracers. Our results demonstrated a double cumulative action: epiphytes could be capable of quickly outcompeting their hosts in terms of nutrient acquisition because of their better efficiency in C and N uptake, while also functionally qualifying as true parasites, as they divert some of the N resources acquired by their host. In terms of biocontrol, we suggest that the choice of nutrient-rich areas to practice Kappaphycus farming is likely to favour the epiphytes rather than their hosts, considering their relative needs and abilities to incorporate nutrients.
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Experimental data are available upon request by e-mailing G.Lepoint@uliege.be.
References
Ateweberhan M, Rougier A, Rakotomahazo C (2015) Influence of environmental factors and farming technique on growth and health of farmed Kappaphycus alvarezii (cottonii) in south-west Madagascar. J Appl Phycol 27:923–934
Behera DP, Ingle KN, Mathew DE, Dhimmar A, Sahastrabudhe H, Sahu SK, Krishnan MG, Shinde PB, Ganesan M, Mantri VA (2022) Epiphytism, diseases and grazing in seaweed aquaculture: A comprehensive review. Rev Aquac 14:1345–1370
Berger R, Henriksson E, Kautsky L, Malm T (2003) Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea. Aquat Ecol 37:1–11
Borowitzka MA, Lavery PS, van Keulen M (2006) Epiphytes of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: Biology, Ecology and Conservation. Kluwer, Dordrecht, pp 441–461
Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260–261:345–351
Campbell S (2001) Ammonnium requirements of fast-growing ephemeral macroalgae in a nutrient-enriched marine embayment (Port Phillip Bay, Australia). Mar Ecol Prog Ser 209:99–107
Ciciotte SL, Thomas RJ (1997) Carbon exchange between Polysiphonia lanosa (Rhodophyceae) and its brown algal host. Am J Bot 84:1614–1616
Dawes CJ, Teasdale BW, Friedlander M (2000) Cell wall structure of the agarophytes Gracilaria tikvahiae and G. cornea (Rhodophyta) and penetration by the epiphyte Ulva lactuca (Chlorophyta). J Appl Phycol 12:567–575
Dodds WK (1991) Micro-environmental characteristics of filamentous algal communities in flowing freshwaters. Freshw Biol 25:199–209
Doty MS, Alvarez VB (1975) Status, problems, advances and economics of Eucheuma farms. Mar Technol Soc J 9:30–35
Hammer Ø, Harper DAT, Ryan PD (2001) Past: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:19–20
Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed Ecology and Physiology, 2nd edn. Cambridge University Press, Cambridge
Hurtado AQ, Critchley AT, Trespoey A, Lhonneur GB (2006) Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Is., Camarines Norte. Phillippines. J Appl Phycol 18:301–306
Hurtado AQ, Neish IC, Critchley AT (2015) Developments in production technology of Kappaphycus in the Philippines: more than four decades of farming. J Appl Phycol 27:1945–1961
Ingle KN, Polikovsky M, Chemodanov A, Golberg A (2018) Marine integrated pest management (MIPM) approach for sustainable seagriculture. Algal Res 29:223–232
Ingle KN, Traugott H, Golberg A (2020) Challenges for marine macroalgal biomass production in Indian coastal waters. Bot Mar 63:327–340
Karez R, Engelbert S, Sommer U (2000) “Co-consumption” and “protective coating”: Two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte-host interactions. Mar Ecol Prog Ser 205:85–93
Leal PP, Ojeda J, Sotomayor C, Buschmann AH (2020) Physiological stress modulates epiphyte (Rhizoclonium sp.)-basiphyte (Agarophyton chilense) interaction in co-culture under different light regimes. J Appl Phycol 32:3219–3232
Leonardi PI, Miravalles AB, Faugeron S, Flores V, Beltrán J, Correa JA (2006) Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile. Eur J Phycol 41:247–257
Lepoint G, Gobert S, Dauby P, Bouquegneau JM (2004) Contributions of benthic and planktonic primary producers to nitrate and ammonium uptake fluxes in a nutrient-poor shallow coastal area (Corsica, NW Mediterranean). J Exp Mar Biol Ecol 302:107–122
Lepoint G, Jacquemart J, Bouquegneau JM, Demoulin V, Gobert S (2007) Field measurements of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). J Phycol 43:208–218
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513–518
Liao LM (1996) Validation of names transferred to Kappaphycus Doty from Eucheuma J. Agardh (Rhodophyta: Solieriaceae). Philipp J Sci 125:158–160
Masuda M, Abe T, Kawaguchi S, Phang SM (2001) Taxonomic notes on marine algae from Malaysia. VI. Five species of Ceramiales (Rhodophyceae). Bot Mar 44:467–477
Michel LN, Dauby P, Dupont A, Gobert S, Lepoint G (2015) Selective top-down control of epiphytic biomass by amphipods from Posidonia oceanica meadows: Implications for ecosystem functioning. Belg J Zool 145:83–93
Ndawala MA, Msuya FE, Cabarubias JP, Kambey CSB, Buriyo AS, Mvungi EF, Cottier-Cook EJ (2022) Effect of biosecurity practices and diseases on growth and carrageenan properties of Kappaphycus alvarezii and Eucheuma denticulatum cultivated in Zanzibar, Tanzania. J Appl Phycol 34:2069–2085
Orth RJ, Van Montfrans J (1984) Epiphyte-seagrass relationships with an emphasis on the role of micrograzing: A review. Aquat Bot 18:43–69
Padilla DK, Allen BJ (2000) Paradigm lost: Reconsidering functional form and group hypotheses in marine ecology. J Exp Mar Biol Ecol 250:207–221
Parmentier E, Michel L (2013) Boundary lines in symbiosis forms. Symbiosis 60:1–5
Pedersen MF (1995) Nitrogen limitation of photosynthesis and growth: Comparison across aquatic plant communities in a Danish estuary (Roskilde Fjord). Ophelia 41:261–272
Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: Growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161:155–163
Penot M, Hourmant A, Penot M (1993) Comparative study of metabolism and forms of transport of phosphate between Ascophyllum nodosum and Polysiphonia lanosa. Physiol Plantarum 87:291–296
Saco JA, Ganzon-Fortes ET (2022) Linking thallus morphology with P-I curves of 50 macrobenthic algae from Bolinao, Pangasinan, Philippines. Philipp J Sci 151:207–221
Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63
Silberstein K, Chiffings AW, McComb AJ (1986) The loss of seagrass in cockburn Sound, Western Australia. III. The effect of epiphytes on productivity of Posidonia australis Hook. F. Aquat Bot 24:355–371
Steel JB, Bastow Wilson J (2003) Which is the phyte in Epiphyte? Folia Geobot 38:97–99
Tsiresy G (2016) Analyses biologiques intégratives (influence sur l'incorporation de l'azote et du carbone, phénologie et phylogénie) des algues épiphytes responsables de l’EFAD (“Epiphytic Filamentous Algal Disease”) dans les champs de Kappaphycus alvarezii Doty à Madagascar. PhD Thesis, University of Mons, Mons, Belgium
Tsiresy G, Preux J, Lavitra T, Dubois P, Lepoint G, Eeckhaut I (2016) Phenology of farmed seaweed Kappaphycus alvarezii infestation by the parasitic epiphyte Polysiphonia sp. in Madagascar. J Appl Phycol 28:2903–2914
Vairappan CS, Chung CS, Hurtado AQ, Soya FE, Lhonneur GB, Critchley A (2008) Distribution and symptoms of epiphyte infection in major carrageenophyte-producing farms. J Appl Phycol 20:477–483
Vairappan CS, Chung CS, Matsunaga S (2014) Effect of epiphyte infection on physical and chemical properties of carrageenan produced by Kappaphycus alvarezii Doty (Soliericeae, Gigartinales, Rhodophyta). J Appl Phycol 26:923–931
Ward GM, Faisan JP Jr, Cottier-Cook EJ, Gachon C, Hurtado AQ, Lim PE, Matoju I, Msuya FE, Bass D, Brodie J (2020) A review of reported seaweed diseases and pests in aquaculture in Asia. J World Aquac Soc 51:815–828
Ward GM, Kambey CSB, Faisan JP Jr, Tan PL, Daumich CC, Matoju I, Stentiford GD, Bass D, Lim PE, Brodie J, Poong SW (2022) Ice-Ice disease: An environmentally and microbiologically driven syndrome in tropical seaweed aquaculture. Rev Aquac 14:414–439
Yamamoto K, Endo H, Yoshikawa S, Ohki K, Kamiya M (2013) Various defense ability of four sargassacean algae against the red algal epiphyte Neosiphonia harveyi in Wakasa Bay, Japan. Aquat Bot 105:11–17
Acknowledgements
The authors are grateful to Fisheries and Marine Science Institute (IH.SM., University of Toliara, Madagascar) for access to their aquarium facilities, lab and logistical resources. The authors thank the local seaweed farmers of Sorodrano village for providing the biological material used in the experiments. G.L. is a senior researcher at the National Fund for Scientific Research (F.R.S. -FNRS, Belgium).
Funding
This study was funded by the project ‘Développement de la polyaquaculture dans les villages côtiers du sud-ouest et de nord de Madagascar’ and financed by universitary cooperation for the development of the Wallonia Brussel community (ARES-CCD).
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G.L., G.T. and I.E. contributed to the study’s conception and design. Experiments were conducted by G.L., G.T. and B.F. Biological material was provided by F.P. Material preparation and analyses were performed by M.D., G.T. and G.L. The first draft of the manuscript was written by G.L., and all authors commented on previous versions of the manuscript. Financial resources were secured by I.E. All authors read and approved the final manuscript.
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Gilles Lepoint and Gaëtan Tsiresy these two authors contributed equally as co-first authors.
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Lepoint, G., Tsiresy, G., Deydier, M. et al. Functional effects of Polysiphonia sp. epiphytism on the farmed Kappaphycus alvarezii (Doty) Liao: Competition for the resource, parasitism or both?. J Appl Phycol 35, 1821–1830 (2023). https://doi.org/10.1007/s10811-023-03009-9
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DOI: https://doi.org/10.1007/s10811-023-03009-9