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Journal of Applied Phycology

, Volume 26, Issue 1, pp 569–575 | Cite as

Evidence of reproductive cost in the triphasic life history of the red alga Gracilaria chilensis (Gracilariales, Rhodophyta)

  • Marie Laure Guillemin
  • Paula Valenzuela
  • Juan Diego Gaitán-Espitia
  • Christophe Destombe
Article

Abstract

The extent of changes in basic physiological and demographic traits associated with reproduction was investigated in the highly cultivated haploid–diploid red alga, Gracilaria chilensis. Sixty individuals bearing vegetative and reproductive fronds collected in the natural population of Niebla (39°52′ S, 73°23′ W), in Chile, were cultivated under controlled culture conditions. Our results demonstrated that vegetative fronds have a higher survival rate and a better growth rate than reproductive ones irrespective of the type of individual analyzed (male gametophyte, female gametophyte, and tetrasporophyte). Moreover, the reproductive fronds clearly showed a decrease in photosynthetic activity compared to non-reproductive ones. In males and tetrasporophytes, the photosynthetic reduction in reproductive individuals could be explained by a physical effect of reproductive structure development as well as spores release, disrupting the continuity of the photosynthetic cortical tissues. Translocation of photoassimilates from nearby vegetative tissue or the previous accumulation of photosynthetic products seems to be a prerequisite for reproductive structure development in this species. Altogether, these results document for the first time in G. chilensis that reproduction has a strong physiological effect on male, female, and tetrasporophyte fronds. This trade-off between reproduction, growth, and survival suggest the existence of reproductive costs in the life history of G. chilensis.

Keywords

Short-term reproductive cost Dioecy Gametophyte Sporophyte Carposporophyte Haplo-diploidy Photosynthesis 

Notes

Acknowledgments

We thank P. Antileo and K. Contreras for their technical assistance in algae maintenance; I. Gómez, M. Orostegui, and C. Rosas (Inst. De Ciencias Marinas y Limnológicas, Universidad Austral de Chile) for providing their expertise and facilities for pigment analyses; and S. Woelfl (Inst. De Ciencias Marinas y Limnológicas, Universidad Austral de Chile) for facilitating us access to the oxymeter. JDGE acknowledges support provided by a CONICYT Doctoral fellowship. MLG was supported by FONDECYT grant no. 1090360.

References

  1. Åberg P (1992) A demographic study of two populations of the seaweed Ascophyllum nodosum in stochastic environment. Ecology 73:1473–1487CrossRefGoogle Scholar
  2. Åberg P (1996) Patterns of reproductive effort in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 138:199–207CrossRefGoogle Scholar
  3. Ang PO (1992) Cost of reproduction in Fucus distichus. Mar Ecol Prog Ser 28:25–35CrossRefGoogle Scholar
  4. Ashman T (1994) A dynamic perspective on the physiological cost of reproduction in plants. Am Nat 144:300–316CrossRefGoogle Scholar
  5. Bazzaz FA, Ackerly DD, Reekie EG (2000) Reproductive allocation in plants. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI Publishing, Wallingford, pp 1–30CrossRefGoogle Scholar
  6. Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aquaeous crude extracts of red algae. Aust J Mar Freshw Res 36:785–792CrossRefGoogle Scholar
  7. Bell G (1984) Measuring the cost of reproduction. 1. The correlation structure of the life table of a plankton rotifer. Evolution 38:300–313CrossRefGoogle Scholar
  8. Bird CJ, McLachlan J (1986) The effect of salinity on distribution of species of Gracilaria Grev. (Rhodophyta, Gigartianles): an experimental assessment. Bot Mar 29:231–238CrossRefGoogle Scholar
  9. Bisang I, Ehrlén J (2002) Reproductive effort and cost of sexual reproduction in female Dicranum polysetum. Bryologist 105:384–397CrossRefGoogle Scholar
  10. Buschmann AH, Correa JA, Westermeier R, Hernandez-Gonzalez MDC, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–20CrossRefGoogle Scholar
  11. Chu S, Zhang Q, Liu S, Zhang S, Tang Y, Lu Z, Yu Y (2011) Trade-off between vegetative regeneration and sexual reproduction of Sargassum thunbergii. Hydrobiologia 678:127–135CrossRefGoogle Scholar
  12. Clifton KE, Clifton LM (1999) The phenology of sexual reproduction by green algae (Bryopsidales) on Caribbean coral reefs. J Phycol 35:24–34CrossRefGoogle Scholar
  13. Correa JA, McLachlan JL (1991) Endophytic algae of Chondrus crispus (Rhodophyta). III. Host specificity. J Phycol 27:448–459CrossRefGoogle Scholar
  14. De Wreede R, Klinger T (1990) Reproductive strategies in algae. In: Lovett-Doust J, Lovett-Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, New York, pp 267–284Google Scholar
  15. Dyck LJ, DeWreede RE (2006) Reproduction and survival in Mazzaella splendens (Gigartinales, Rodophyta). Phycologia 45:302–310CrossRefGoogle Scholar
  16. Engel C, Åberg P, Gaggiotti O, Destombe C, Valero M (2001) Population dynamics and stage structure in a haploid–diploid red seaweed, Gracilaria gracilis. J Ecol 89:436–450CrossRefGoogle Scholar
  17. Fisher RA (1930) The genetical theory of natural selection. Claredon Press, OxfordGoogle Scholar
  18. Ganzon-Fortes ET (1999) Photosynthetic and respiratory responses of the agarophyte Gelidiella acerosa collected from tidepool, intertidal and subtidal habitats. Hydrobiologia 398/399:321–328CrossRefGoogle Scholar
  19. Gao S, Chen XY, Yi QQ, Wang GC, Pan GH, Lin AP, Peng G (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS One 5:e8571PubMedCentralPubMedCrossRefGoogle Scholar
  20. Gómez IM, Westermeier RC (1991) Frond regrowth from basal disc in Iridaea laminarioides (Rhodophyta, Gigartinales) at Mehuín, southern Chile. Mar Ecol Prog Ser 73:83–91CrossRefGoogle Scholar
  21. Gómez I, Figueroa F, Huovin P, Ulloa N, Morales V (2005) Photosynthesis of the red alga Gracilaria chilensis under natural solar radiation in an estuary in southern Chile. Aquaculture 244:369–382CrossRefGoogle Scholar
  22. Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JA, Valero M (2008) Genetic variation in wild and cultivated populations of the haploid–diploid red alga Gracilaria chilensis: how farming practices favour asexual reproduction and heterozygosity. Evolution 62:1500–1519PubMedCrossRefGoogle Scholar
  23. Guimarães M, Plastino E, Oliveira E (1999) Life history, reproduction and growth of Gracilaria domingensis (Graciliariales, Rhodophyta) from Brazil. Bot Mar 42:481–486CrossRefGoogle Scholar
  24. Guzmán-Urióstegui A, García-Jiménez P, Marián FD, Robledo D, Robaina RR (2002) Polyamines influence maturation in reproductive structures of Gracilaria cornea (Gracilariales, Rhodophyta). J Phycol 38:1169–75CrossRefGoogle Scholar
  25. Halling C, Aroca G, Cifuentes M, Buschmann A, Troell M (2005) Comparison of spore inoculated and vegetative propagated cultivation methods of Gracilaria chilensis in an integrated seaweed and fish cage culture. Aquacult Int 13:409–422CrossRefGoogle Scholar
  26. Harper JL (1967) A Darwinian approach to plant ecology. J Ecol 55:247–270CrossRefGoogle Scholar
  27. Hommersand MH, Fredericq S (1995) Sexual reproduction and cystocarp development. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, New York, pp 305–345Google Scholar
  28. Howarth R, Michaels A (2000) The measurement of primary production in aquatic ecosystems. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer-Verlag, New York, pp 74–85Google Scholar
  29. Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80 % acetone. Plant Physiol 77:483–485PubMedCentralPubMedCrossRefGoogle Scholar
  30. Kain JM, Destombe C (1995) A review of the life history, reproduction and phenology of Gracilaria. J Appl Phycol 7:269–281CrossRefGoogle Scholar
  31. Kamiya M, Kawai H (2002) Dependence of the carposporophyte on the maternal gametophyte in three ceramiacean algae (Rhodophyta), with respect to carposporophyte development, spore production and germination success. Phycologia 41:107–115CrossRefGoogle Scholar
  32. Mathieson AC, Guo Z (1992) Patterns of fucoid reproductive biomass allocation. Br Phycol J 27:37–41CrossRefGoogle Scholar
  33. McCourt RM (1985) Reproductive biomass allocation in three Sargassum species. Oecologia 67:113–117CrossRefGoogle Scholar
  34. Meneses I (1996) Sources of morphological variation in populations of Gracilaria chilensis Bird, McLachlan & Oliviera of Chile. Rev Chil Hist Nat 69:35–44Google Scholar
  35. Obeso J (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  36. Perrone C, Felicini GP (1988) Physiological ecology of Schottera nicaeensis (Phyllophoraceae, Rhodophyta): functional significance of heterotrichy. Phycologia 27:347–354CrossRefGoogle Scholar
  37. Pfister C (1992) Costs of reproduction in an intertidal kelp: patterns of allocation and life history consequences. Ecology 73:1586–1596CrossRefGoogle Scholar
  38. Rameau C, Gouyon PH (1991) Resource allocation to growth, reproduction and survival in Gladiolus: the cost of male function. J Evol Biol 4:291–307CrossRefGoogle Scholar
  39. Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the cost of reproduction. Trends Ecol Evol 15:421–425PubMedCrossRefGoogle Scholar
  40. Rydgren K, Økland RH (2003) Short-term costs of sexual reproduction in the clonal moss Hylocomium splendens. Bryologist 106:212–220CrossRefGoogle Scholar
  41. Sánchez I, Fernández C, Rico JM (2003) Distribution, abundance and phenology of two species of Liagora (Nemaliales, Rhodophyta) in northern Spain. Phycologia 42:7–17CrossRefGoogle Scholar
  42. Santelices B (1990) Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr Mar Biol Annu Rev 28:177–276Google Scholar
  43. Santelices B, Ugarte R (1990) Ecological differences among Chilean populations of commercial Gracilaria. J Appl Phycol 2:17–26CrossRefGoogle Scholar
  44. Santelices B, Varela D (1995) Regenerative capacity of Gracilaria fragments: effects of size, reproductive state and position along the axis. J Appl Phycol 7:501–506CrossRefGoogle Scholar
  45. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  46. Thornber CS (2006) Functional properties of the isomorphic biphasic algal life cycle. Integr Comp Biol 46:605–614PubMedCrossRefGoogle Scholar
  47. Vernet P, Harper JL (1980) The costs of sex in seaweeds. Biol J Linn Soc 13:129–138CrossRefGoogle Scholar
  48. Wheelwright N, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proc Natl Acad Sci USA 101:8051–8055PubMedCentralPubMedCrossRefGoogle Scholar
  49. Yang RL, Zhou W, Shen SD, Wang GC, He LW, Pan GH (2012) Morphological and photosynthetic variations in the process of spermatia formation from vegetative cells in Porphyra yezoensis Ueda (Bangiales, Rhodophyta) and their responses to desiccation. Planta 235:885–893PubMedCrossRefGoogle Scholar
  50. Yokoya YS, Necchi O Jr, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 19:197–205CrossRefGoogle Scholar
  51. Zhang X, van de Meer JP (1988) A genetic study on Gracilaria sjoestedtii. Can J Bot 66:2022–2026Google Scholar
  52. Zou DH, Gao KS, Ruan ZX (2006) Seasonal pattern of reproduction of Hizikia fusiformis (Sargassaceae, Phaeophyta) from Nanao Island, Shantou, China. J Appl Phycol 18:195–201CrossRefGoogle Scholar
  53. Zou D, Gao K, Chen W (2011) Photosynthetic carbon acquisition in Sargassum henslowianum (Fucales, Phaeophyta), with special reference to the comparison between the vegetative and reproductive tissues. Photosynth Res 107:159–168PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Marie Laure Guillemin
    • 1
    • 2
  • Paula Valenzuela
    • 1
    • 2
  • Juan Diego Gaitán-Espitia
    • 1
    • 2
  • Christophe Destombe
    • 3
    • 4
  1. 1.Instituto de Ciencias Ambientales y Evolutivas – Laboratorio de recursos aquaticos de CalfucoUniversidad Austral de Chile, Facultad de CienciasValdiviaChile
  2. 2.Laboratorio Costero CalfucoInstituto de Biología Marina “Jürgen Winter” Universidad Austral de ChileValdiviaChile
  3. 3.UPMC, UMR 7144, Adaptation & Diversité en Milieu Marin, Equipe “BEDIM”, Station BiologiqueRoscoff CedexFrance
  4. 4.CNRS, UMR 7144, Adaptation & Diversité en Milieu Marin, Equipe “BEDIM”, Station BiologiqueRoscoff CedexFrance

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