Skip to main content
Log in

Physiological stress modulates epiphyte (Rhizoclonium sp.)-basiphyte (Agarophyton chilense) interaction in co-culture under different light regimes

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Epiphytism is a common phenomenon in macroalgal aquaculture worldwide. This problem can affect the productivity and quality of the farmed species which may have socioeconomic consequences for the human communities that depend on this activity. In southern Chile, the aquaculture of the red macroalga Agarophyton chilense in the area of Maullín River has suffered losses in local production (> 90%) due to the proliferation of the filamentous green epiphyte Rhizoclonium sp. This epiphyte becomes entangled with A. chilense fronds, diminishing its quality and preventing its sale as raw material. Thus, the aim of this study was to investigate the effects of light intensity (90 and 180 μmol photons m−2 s−1) on the competitive interaction between the epiphyte Rhizoclonium sp. and the basiphyte A. chilense co-cultured at different initial biomass proportions in a replace series experiment. At the end of the experiment, the presence of Rhizoclonium sp. did not affect negatively the growth of A. chilense, but both species showed stress responses (i.e. reduced Fv/Fm and C:N ratio, suggesting nutrient limitation) in co-culture compared with monocultures. The epiphyte-basiphyte interaction was not modulated by light availability at any initial co-culture proportion and could have been related to nutrient availability during experimentation. Using the replacement series approach, an interspecific competition was observed at all initial co-culture proportion under 180 μmol photons m−2 s−1 while competition was found at the initial co-culture 1:1 under 90 μmol photons m−2 s−1. Our results suggest that the interaction in co-culture between both A. chilense and Rhizoclonium sp. seems to be regulated by nutrient availability as well as it demands utilization rather than light availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abreu MH, Varela DA, Henríquez LA, Villarroel A, Yarish C, Sousa-Pinto I, Buschmann AH (2009) Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis C. J. Bird, J. McLachlan & E. C. Oliveira: productivity and physiological performance. Aquaculture 293:211–220

    Google Scholar 

  • Adee SR, Pfender WF, Hartnett DC (1990) Competition between Pyrenophora tritici-repentis and Septoria nodorum in the wheat leaf as measured with de Wit replacement series. Ecol Epidemiol 80:1177–1182

    Google Scholar 

  • Ale MT, Mikkelsen JD, Meyer AS (2011) Differential growth response of Ulva lactuca to ammonium and nitrate assimilation. J Appl Phycol 23:345–351

    CAS  Google Scholar 

  • Alemañ AE, Robledo D, Hayashi L (2019) Development of seaweed cultivation in Latin America: current trends and future prospects. Phycologia 58:462–471

    Google Scholar 

  • Aminpanah H, Sharifi P, Firouzi S (2012) Interference interactions of two species of Echinochloa genus with rice. Chil J Agric Res 72:364–370

    Google Scholar 

  • Anderson RJ, Monteiro PMS, Levitt GJ (1996) The effect of localised eutrophication on competition between Ulva lactuca (Ulvaceae, Chlorophyta) and a commercial resource of Gracilaria verrucosa (Gracilariaceae, Rhodophyta). Hydrobiologia 326:291–296

    Google Scholar 

  • Andria J, Vergara JJ, Perez-Llorens JL (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cadiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504

    Google Scholar 

  • Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110:689–696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bi H, Turvey ND (1994) Inter-specific competition between seedlings of Pinus radiata, Eucalyptus regnans and Acacia melanoxylon. Aust J Bot 42:61–70

    Google Scholar 

  • Buschmann AH, Camus C, Infante J, Neori A, Israel A, Hernández-González MC, Pereda SV, Gomez-Pinchetti JL, Golberg A, Tadmor-Shalev N, Critchley AT (2017) Seaweed production: overview of the global state of exploitation, farming and emerging research activity. Eur J Phycol 52:391–406

    Google Scholar 

  • Buschmann AH, Correa JA, Westermeier R, Hernández-González MC, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220

    Google Scholar 

  • Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260–261:345–351

    Google Scholar 

  • Buschmann AH, Hernández-González MC, Astudillo C, de la Fuente L, Gutierrez A, Aroca G (2005) Seaweed cultivation, product development and integrated aquaculture studies in Chile. Aquaculture 36:51–53

    Google Scholar 

  • Buschmann AH, Retamales CA, Figueroa C (1997) Ceramialean epiphytismin an intertidal Gracilaria chilensis (Rhodophyta) bed in southern Chile. J Appl Phycol 9:129–135

    Google Scholar 

  • Buschmann AH, Westermeier R, Retamales CA (1995) Cultivation of Gracilaria on the sea-bottom in southern Chile: a review. J Appl Phycol 7:291–301

    Google Scholar 

  • Camus C, Hernández-González MC, Buschmann AH (2019) The seaweed resources of Chile over the period 2006–2016: moving from gatherers to cultivators. Bot Mar 62:237–247

    Google Scholar 

  • Chen B, Zou D, Jiang H (2015) Elevated CO2 exacerbates competition for growth and photosynthesis between Gracilaria lemaneiformis and Ulva lactuca. Aquaculture 443:49–55

  • Chirapart A, Ohno M (1993) Seasonal variation in the physical properties of agar and biomass of Gracilaria sp. (chorda type) from Tosa Bay, southern Japan. Hydrobiologia 260–261:541–547

    Google Scholar 

  • De Wit CT (1960) On competition. Versl Landbouwkd Onderz 66

  • Ekman P, Pedersén M (1990) The influence of photon irradiance, day length, dark treatment, temperature, and growth rate on the agar composition of Gracilaria sordida W. Nelson and Gracilaria verrucosa (Hudson) Papenfuss (Gigartinales, Rhodophyta). Bot Mar 33:483–496

    Google Scholar 

  • Fernández PA, Gaitán-Espitia JD, Leal PP, Schmid M, Revill AT, Hurd CL (2020) Nitrogen sufficiency enhances thermal tolerance in habitat- forming kelp: implications for acclimation under thermal stress. Sci Rep 10:3186

    PubMed  PubMed Central  Google Scholar 

  • Figueroa FL, Jerez CG, Korbee N (2013) Use of in vivo chlorophyll fluorescence to estimate photosynthetic activity and biomass productivity in microalgae grown in different culture systems. Lat Am J Aquat Res 41:801–819

    Google Scholar 

  • Fletcher RL (1995) Epiphytism and fouling in Gracilaria cultivation: an overview. J Appl Phycol 7:325–333

    Google Scholar 

  • Friedlander M (1992) Gracilaria conferta and its epiphytes: the effect of culture conditions on growth. Bot Mar 35:423–428

    Google Scholar 

  • Friedlander M, Gonen Y, Kashman Y, Beer S (1996) Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed by Ulva cf lactuca. J Appl Phycol 8:21–25

    Google Scholar 

  • Friedlander M, Shalev R, Ganor T, Strimling S, Ben-Amotz A, Klar H, Wax Y (1987) Seasonal fluctuations of growth rate and chemical composition of Gracilaria cf. conferta in outdoor culture in Israel. Hydrobiologia 151:501–507

    Google Scholar 

  • Gerard VA (1982) Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar Biol 66:27–35

    CAS  Google Scholar 

  • González MA, Barrales HL, Candiab A, Cid L (1993) Spatial and temporal distribution of dominant epiphytes on Gracilaria from a natural subtidal bed in central-southern Chile. Aquaculture 116:135–148

    Google Scholar 

  • Gordillo FJL, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322

    CAS  PubMed  Google Scholar 

  • Gorman L, Kraemer GP, Yarish C, Boo SM, Kim JK (2017) The effects of temperature on the growth rate and nitrogen content of invasive Gracilaria vermiculophylla and native Gracilaria tikvahiae from Long Island Sound, USA. Algae 32:57–66

    CAS  Google Scholar 

  • Guiry MD, Guiry GM (2016) AlgaeBase. In: AlgaeBase. World-wide Electron. Publ. Natl. Univ. Ireland, Galw. http://www.algaebase.org. Accessed 7 Jan 2020

  • Gurgel CFD, Norris JN, Schmidt WE, Le HN, Fredericq S (2018) Systematics of the Gracilariales (Rhodophyta) including new subfamilies, tribes, subgenera, and two new genera, Agarophyton gen nov and Crassa gen nov Phytotaxa 374:1–23.

  • Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci Mar 60:243–248

    CAS  Google Scholar 

  • Hayashi L, Bulboa C, Kradolfer P, Soriano G, Robledo D (2013) Cultivation of red seaweeds: a Latin American perspective. J Appl Phycol 26:719–727

    Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Jolliffe PA (2000) The replacement series. J Ecol 88:371–385

  • Karez R (2003) Competitive ranks of three Fucus spp. (Phaeophyta) in laboratory experiment-testing of Keddy’s competitive hierarchy model. Helgol Mar Res 57:83–90

    Google Scholar 

  • Karez R, Chapman ARO (1998) A competitive hierarchy model integrating roles of physiological competence and competitive ability does not provide a mechanistic explanation for the zonation of three intertidal Fucus species in Europe. Oikos 81:471–494

    Google Scholar 

  • Kuschel FA, Buschmann AH (1991) Abundance, effects and management of epiphytism in intertidal cultures of Gracilaria (Rhodophyta) in southern Chile. Aquaculture 92:7–19

    Google Scholar 

  • Lapointe BE, Duke CS (1984) Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J Phycol 20:488–495

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • MacIntyre HL, Cullen JJ (2005) Using cultures to investigate the physiological ecology of microalgae. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Burlington, pp 287–326

    Google Scholar 

  • Marinho-Soriano E, Silva TSF, Moreira WSC (2001) Seasonal variation in the biomass and agar yield from Gracilaria cervicornis and Hydropuntia cornea from Brazil. Bioresour Technol 77:115–120

    CAS  PubMed  Google Scholar 

  • Martín LA, de Zaixso ALB, Miravalles AB, Rodríguez MC, Leonardi PI (2013a) Epiphytism in a subtidal natural bed of Gracilaria gracilis of southwestern Atlantic coast (Chubut, Argentina). J Appl Phycol 25:1319–1329

    Google Scholar 

  • Martín LA, Rodríguez MC, Matulewicz MC, Fissore EN, Gerschenson LN, Leonardi PI (2013b) Seasonal variation in agar composition and properties from Gracilaria gracilis (Gracilariales, Rhodophyta) of the Patagonian coast of Argentina. Phycol Res 61:163–171

    Google Scholar 

  • Muñoz J, Fotedar R (2011) Seasonal variations of agar extracted from different life stages of Gracilaria cliftonii (Gracilariales, Rhodophyta) from Western Australia. African J Mar Sci 33:59–65

    Google Scholar 

  • Øverland M, Mydland LT, Skrede A (2019) Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J Sci Food Agric 99:13–24

    PubMed  Google Scholar 

  • Pangestuti R, Kim SK (2015) An overview of phycocolloids: the principal commercial seaweed extracts. In: Kim S-K, Chojnacka K (eds) Marine algae extracts: processes, products, and applications. Wiley, New York, pp 319–330

    Google Scholar 

  • Pantone DJ (1995) Replacement series analysis of the competitive interaction between a weed and a crop as influenced by a plant parasitic nematode. Fundam Appl Nematol 18:81–85

    Google Scholar 

  • 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

    Google Scholar 

  • Pickering TD, Gordon ME, Tong LJ (1993) Effect of nutrient pulse concentration and frequency on growth of Gracilaria chilensis plants and levels of epiphytic algae. J Appl Phycol 5:525–533

    Google Scholar 

  • Potvin C, Roff DA (1993) Distribution-free and robust statistical methods: viable alternatives to parametric statistics. Ecology 74:1617–1628

    Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126

    CAS  Google Scholar 

  • Rodriguez DJ (1997) A method to study competition dynamics using de Wit replacement series experiments. Oikos 78:411–415

    Google Scholar 

  • Santelices B (2014) Cultured aquatic species information programme. Gracilaria spp. In: FAO Fish. Aquac. Dep. [online]. http://www.fao.org/fishery/culturedspecies/Gracilaria_spp/en. Accessed 21 Jun 2019

  • Schreiber U, Hormann H, Neubauer C, Klughammer C (1995) Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust J Plant Physiol 22:209–220

    CAS  Google Scholar 

  • Seely GR, Duncan MJ, Vidaver WE (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12:184–188

    CAS  Google Scholar 

  • Shannon E, Abu-Ghannam N (2019) Seaweeds as nutraceuticals for health and nutrition. Phycologia 58:563–577

    CAS  Google Scholar 

  • Speziale BJ, Schreiner SP, Giammatteo PA, Schindler JE (1984) Comparison of N,N-dimethylformamide, dimethyl sulfoxide, and acetone for extraction of phytoplankton chlorophyll. Can J Fish Aquat Sci 41:1519–1522

    CAS  Google Scholar 

  • Stetina SR, Russin JS, McGawley EC (1997) Replacement series: a tool for characterizing competition between phytoparasitic nematodes. J Nematol 29:35–42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su S, Zhou Y, Qin JG, Yao W, Ma Z (2010) Optimization of the method for chlorophyll extraction in aquatic plants. J Freshw Ecol 25:531–538

    CAS  Google Scholar 

  • Subpesca (2013) Visualizador de mapas. In: Subsecr. Pesca y Acuic. http://mapas.subpesca.cl/ideviewer/. Accessed 25 Jun 2019

  • Subpesca (2015) Informe Técnico D. AC. N°273/2015. Propuesta de declaración de área plaga para la macroalga Rhizoclonium spp. en el sector de la ribera norte del río Maullín, región de los Lagos

  • Svirski E, Beer S, Friedlander M (1993) Gracilaria conferta and its epiphytes: (2) interrelationship between the red seaweed and Ulva cf. lactuca. Hydrobiologia 260:391–396

    Google Scholar 

  • Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20

    CAS  Google Scholar 

  • Tyler AC, McGlathery KJ (2006) Uptake and release of nitrogen by the macroalgae Gracilaria vermiculophylla (Rhodophyta). J Phycol 42:515–525

    CAS  Google Scholar 

  • Ursi S, Costa VL, Hayashi L, Pereira RTL, Paula EJ, Plastino EM (2013) Intraspecific variation in Gracilaria birdiae (Gracilariales, Rhodophyta): growth, and agar yield and quality of color strains under aquaculture. Bot Mar 56:241–248

    CAS  Google Scholar 

  • Usov AI (2011) Polysaccharides of the red algae. Adv Carbohydr Chem Biochem 65:115–217

    CAS  PubMed  Google Scholar 

  • Vergara-Rodarte MA, Hernández-Carmona G, Rodríguez-Montesinos YE, Arvizu-Higuera DL, Riosmena-Rodríguez R, Murillo-Álvarez JI (2010) Seasonal variation of agar from Gracilaria vermiculophylla, effect of alkali treatment time, and stability of its Colagar. J Appl Phycol 22:753–759

    Google Scholar 

  • Vidal G, Contreras H, Rojas P, Pinilla E, Murillo V, Ojeda J, Aguirre C, Besoain V (2017) Estudio de seguimiento del desempeño ambientalde la acuicultura en Chile y su efecto en losecosistemas de emplazamiento. Puerto Montt, Chile

  • Vivian R, Dourado-Neto D, Filho RV, Silva AA, Franco RB, Correa STR (2013) Interactions between soybean and weeds in a replacement series system, considering the effects of water stress. Planta Daninha 31:749–763

    Google Scholar 

  • Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438

    PubMed  Google Scholar 

  • Walck JL, Baskin JM, Baskin CC (1999) Effects of competition from introduced plants on establishment, survival, growth and reproduction of the rare plant Solidago shortii (Asteraceae). Biol Conserv 88:213–219

    Google Scholar 

  • Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar Biol 80:215–225

    CAS  Google Scholar 

  • Warton DII, Hui FKCKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    PubMed  Google Scholar 

  • Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of southern California. Mar Biol 64:59–69

    CAS  Google Scholar 

  • Williams AC, McCarthy BC (2001) A new index of interspecific competition for replacement and additive designs. Ecol Res 16:29–40

    Google Scholar 

  • Wilson M, Lindow SE (1994a) Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl Environ Microbiol 60:4468–4477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson M, Lindow SE (1994b) Ecological similarity and coexistence of epiphytic ice-nucleating (Ice+) Pseudomonas syringae strains and a non-ice-nucleating (Ice-) biological control agent. Appl Environ Microbiol 60:3128–3137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yong YS, Yong WTL, Anton A (2013) Analysis of formulae for determination of seaweed growth rate. J Appl Phycol 25:1831–1834

    Google Scholar 

  • Zhu Z, Wu Q, Di X et al (2017) Multistage recovery process of seaweed pigments: investigation of ultrasound assisted extraction and ultra-filtration performances. Food Bioprod Process 104:40–47

    CAS  Google Scholar 

  • Zitko SE, Timmer LW (1994) Competitive parasitic abilities of Phytophthora parasitica and P. palmivora on fibrous roots of citrus. Ecol Epidemiol 84:1000–1004

    Google Scholar 

Download references

Acknowledgements

The authors thank Pamela A. Fernández and Luis Henríquez-Antipa for their constructive comments on an earlier draft. We also thank the editor and reviewer for the critical and helpful comments.

Funding

Pablo P. Leal received financial support from “Programa Integral de Desarrollo de Acuicultura de Algas para Pescadores Artesanales (Etapa 3, Convenio 2016)”, funded by the Subsecretaría de Economía y Empresas de Menor Tamaño. Johana Ojeda and Carolina Sotomayor were supported by “Estudio del desempeño ambiental de la acuicultura en Chile y su efecto en los ecosistemas de emplazamiento (Convenio 2018)” funded by the Subsecretaría de Economía y Empresas de Menor Tamaño. Alejandro H. Buschmann was supported by the Center of Biotechnology and Bioengineering (CeBiB) of CONICYT (FB-0001) and FONDECYT (1180647).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johana Ojeda.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leal, P.P., Ojeda, J., Sotomayor, C. et al. Physiological stress modulates epiphyte (Rhizoclonium sp.)-basiphyte (Agarophyton chilense) interaction in co-culture under different light regimes. J Appl Phycol 32, 3219–3232 (2020). https://doi.org/10.1007/s10811-020-02153-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02153-w

Keywords

Navigation