Abstract
The diversity of epiphytes, their temporal abundance variation and the anatomical structure of host–epiphyte interfaces were studied in the agarophyte Gracilaria gracilis from a natural bed in Bahía Bustamante, Chubut Province, Argentina. Twenty-nine algal species were recorded as epiphytes during 2 years of monthly sampling (March 2006–February 2008). Total epiphyte density ranged between 0.037 ind. cm−2 (November 2006) and 39.37 ind. cm−2 (April 2007), with higher density values throughout the second sampling year. Ceramiales species were the most abundant epiphytes. The density of Ceramium rubrum ranged from 0.09 ind. cm−2 (52 % of the total amount) in September 2006 to 17.4 ind. cm−2 (44.18 % of the total amount) in April 2007. Epiphyte infection was more dependent on spore recruitment and sporeling development, especially on thalli derived from fragmentation, than on seasonal environmental variations. The different infections were analysed, taking into account the epiphytic attachment strength and invasiveness and the degree of damage inflicted on the host. Calothrix confervicola was one of the most abundant species. This epiphyte, weakly attached to the host surface, generated no host tissue damage. In contrast, C. rubrum, Polysiphonia abscissa and other Ceramiales were the species that caused more damage to the host because their rhizoids penetrated the cortical portion of the host thallus, sometimes reaching the medullary tissue. Some generalisations and characterisations of the different epiphyte groups in relation to their consequences to Gracilaria spp. are presented.
Similar content being viewed by others
References
Boraso de Zaixso AL, Akselman R (2005) Anotrichium furcellatum (Ceramiaceae, Rhodophyta) en Argentina. Una posible especie invasora. Bol Soc Argent Bot 40:207–213
Brawley SH, Xiugeng F (1988) Ecological studies of Gracilaria asiatica and Gracilaria lemaneiformis in Zhanshan Bay, Qingdao. Chin J Oceanol Limnol 6:22–34
Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 261:345–351
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
Buschmann AH, Retamales CA, Figueroa C (1997) Ceramialean epiphytism in an intertidal Gracilaria chilensis (Rhodophyta) bed in southern Chile. J Appl Phycol 9:129–135
Buschmann AH, Correa JA, Westermeier R, Hernández-González M, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220
Casas GN, Scrosati R, Piriz ML (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invas 6:411–416
Dawes CJ (1992) Rope cultivation of Gracilaria in Namibia: prospects. In: Mshigeni KE (ed) Proc Intl Workshop on Sustainable Seaweed Res Development. Windhoek. Namibia: 99–102
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
Boraso de Zaixso AL (1983) Ecología de Gracilaria verrucosa (Hudson) Papenfus en poblaciones de la provincia de Chubut (Argentina). PhD Thesis, Universidad Nacional de Buenos Aires, 172 pp
Boraso de Zaixso AL (1995) Utilización de algas marinas. In Macroalgas de Interés Económico (Ferrario M & Sar E, eds), 15–55. Universidad Nacional de La Plata. Red de Editoriales Universitarias
Boraso de Zaixso AL, Zaixso JM (2007) Algas marinas bentónicas. In Atlas de sensibilidad ambiental de la costa y el Mar Argentino. D Boltovskoy (Ed) (PNUD). 28 pp
Boraso de Zaixso AL, Ciancia M, Cerezo A (2006) Seaweed resources of Argentina. In Critchley AT, Ohno M, Largo DB (eds) World seaweed resources—an authoritative reference system. Electronic version 1.0. Eti Information Services Ltd: www.etiis.org.uk. 26 pp
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2012) InfoStat versión 2012. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL: http://www.infostat.com.ar
Edding M, Macchiavello J, Black J (1987) Culture of Gracilaria sp. in outdoor tanks: Productivity. Hydrobiologia 151:369–379
Eyras C, Sar EA (2003) Arribazones estivales en Puerto Madryn, Argentina, como materiales para la obtención de compost. Bol Soc Argent Bot 38:105–111
Fletcher RL (1995) Epiphytism and fouling in Gracilaria cultivation: an overview. J Appl Phycol 7:325–333
Friedlander M (1992) Gracilaria conferta and its epiphytes: the effect of culture conditions on growth. Bot Mar 35:423–428
Friedlander M, Gonen Y, Kashman Y, Beer S (1996) Gracilaria conferta and its epiphytes: 3. Allelopathic inhibitions of the red seaweed by Ulva cf. lactuca. J Appl Phycol 8:21–25
Friedlander M, Kashman Y, Weinberger F, Dawes CJ (2001) Gracilaria and its epiphytes: 4. The response of two Gracilaria species to Ulva lactuca in a bacteria-limited environment. J Appl Phycol 13:501–507
González MA, Barrales HL, Candia 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
Hurtado AQ, Critchley AT, Trespoey A, Bleicher Lhonneur G (2006) Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Is., Camarines Norte, Phillippines. J Appl Phycol 18:301–306
Kuschel FA, Buschmann AH (1991) Abundance, effects and management of epiphytes in intertidal cultures of Gracilaria (Rhodophyta) in Southern Chile. Aquaculture 92:7–19
Leonardi PI, Miravalles AB, Faugeron S, Flores V, Beltran J, Correa JA (2006) Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile. Eur J Phycol 41:247–257
Lignell A, Ekman P, Pedersén M (1987) Cultivation technique of marine seaweeds allowing controlled and optimized conditions in the laboratory and on a pilot scale. Bot Mar 30:417–424
Lobban CS, Baxter DM (1983) Distribution of the red algal epiphyte Polysiphonia lanosa on its brown algal host Ascophyllum nodosum in the Bay of Fundy, Canada. Bot Mar 26:533–538
Martín LA, Boraso de Zaixso AL, Leonardi PI (2011) Biomass variation and reproductive phenology of Gracilaria gracilis in a Patagonic natural bed (Chubut, Argentina). J Appl Phycol 23:643–654
Miravalles AB (2009) Biología y ultraestructura de Codium spp. (Bryopsidophyceae, Chlorophyta): morfologías vegetativa y reproductiva, ciclos de vida y epifitismo. PhD Thesis, Universidad Nacional del Sur, 196
Muñoz J, Fotedar R (2010) Epiphytism of Gracilaria cliftonii (Withell, Millar & Kraft) from Western Australia. J Appl Phycol 22:371–379
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
Pizarro A (1986) Conocimiento actual y avances recientes sobre el manejo y cultivo de Gracilaria en Chile. Monog Biol 4:63–96
Pizarro A, Santelices B (1993) Environmental variation and large-scale Gracilaria production. Hydrobiologia 260(261):357–363
Poblete A, Inostroza I (1987) Management of a Gracilaria natural bed in Lenga, Chile: a case study. Hydrobiologia 151(152):307–311
Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63
Santelices B, Varela D (1993) Exudates from Gracilaria chilensis stimulate settlement of epiphytic ulvoids. Hydrobiologia 261:327–333
Santelices B, Hoffmann AJ, Aedo D, Bobadilla M, Otaíza R (1995) A bank of microscopic forms on disturbed boulders and stones in tide pools. Mar Ecol Progr Ser 129:215–228
Svirski E, Beer S, Friedlander M (1993) Gracilaria conferta and its epiphytes: 2. Interrelationship between the red seaweed and Ulva cf. lactuca. Proc Int Seaweed Symp 14:391–396
Ugarte R, Santelices B (1992) Experimental tank cultivation of Gracilaria chilensis in central Chile. Aquaculture 101:7–16
Vairappan CS (2006) Seasonal occurrences of epiphytic algae on the commercially cultivated red alga Kappaphycus alvarezii (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 18:611–617
Vairappan CS (2009) Effects of epiphyte infection on the quantity and quality of carrageenan produced by carrageenophytes, Kappaphycus alvarezii (Gigartinales, Rhodophyta). Phycologia 48(Suppl):136
Vairappan CS, Chung CS, Hurtado AQ, Soya FE, Lhonneur GB, Critchley A (2008) Distribution and symptoms of epiphyte infection in major carragenophyte-producing farms. J Appl Phycol 20:477–483
Vásquez JA, Vega A (2001) Ecological considerations related to the management of Chondracanthus chamissoi (Rhodophyta, Gigartinales) in northern Chile. J Appl Phycol 13:267–277
Weinberger F, Friedlander M (2000) Response of Gracilaria conferta (Rhodophyta) to oligoagars results in defence against agar-degrading epiphytes. J Phycol 36:1079–1086
Westermeier R, Rivera P, Gómez I (1991) Cultivo de Gracilaria chilensis Bird, McLachlan y Oliveira, en la zona intermareal y submareal del estuario Cariquilda, Maullín, Chile. Rev Chilena Hist Nat 64:307–321
Westermeier R, Gómez I, Rivera P (1993) Suspended farming of Gracilaria chilensis (Rhodophyta, Gigartinales) at Cariquilda River, Maullin, Chile. Aquaculture 113:215–229
Acknowledgments
This study is part of the PhD thesis of LAM in the Universidad Nacional del Sur, República Argentina (UNS). Funds have been provided by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), grant PIP 5045 and by the Agencia Nacional de Promoción Científica y Tecnológica, grant BID 1728/OC-AR-PICT 632. We would like to thank Soriano S.A. for their logistic assistance during our work in the field. ALB and PIL are research members of CONICET.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Martín, L.A., de Zaixso, A.L.B., Miravalles, A.B. et al. Epiphytism in a subtidal natural bed of Gracilaria gracilis of southwestern Atlantic coast (Chubut, Argentina). J Appl Phycol 25, 1319–1329 (2013). https://doi.org/10.1007/s10811-012-9961-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-012-9961-7