Journal of Applied Phycology

, Volume 29, Issue 3, pp 1449–1459 | Cite as

Limited evolutionary responses to harvesting regime in the intensive production of algae

  • Rebecca J Lawton
  • Nicholas A Paul
  • Dustin J. Marshall
  • Keyne Monro


Plastic changes in the growth and productivity of algae in response to environment and stocking density are well established. In contrast, the capacity for such changes to persist once environmental differences cease, potentially signalling an evolutionary response, have rarely been tested for algae in intensive production systems. We tested whether continuous differences in harvesting regime (a high stocking density/low-yield regime versus low stocking density/high-yield regime) generated changes in biomass productivity and other growth metrics within several strains of the clonal macroalga Oedogonium (Chlorophyta, Oedogoniales) and whether such changes persisted once differential harvesting yields ceased. We found considerable plasticity in growth rate and biomass productivity over a 12-week period of active selection (i.e. repeated high-yield and low-yield harvesting of clonal lineages within strains) and that strains responded differently to this selection pressure over time. While small, but significant, differences in growth rates of clonal lineages exposed to high-yield vs low-yield harvesting regimes were maintained after prolonged culture under a common selection regime (i.e. medium-yield harvesting), differences in biomass productivity were not. There was no evidence for positive or negative effects of maintaining multiple strains in polyculture on growth and biomass productivity. Overall, we detected limited potential for evolutionary responses to harvesting regime in the main commercial trait of interest—biomass productivity. This outcome is important for commercial cultivation in intensive production systems, since it identifies a low risk that harvesting practices will impact negatively on biomass productivity in the longer term.


Aquaculture Oedogonium Chlorophyceae Growth Selection Polyculture Monoculture 



We thank M. Martinez, T. Mannering, N. Neveux and T. Carl for assistance with experiments. We thank S. Skinner for the morphological identification of O. intermedium and R. de Nys and two anonymous reviewers for providing comments on the manuscript. This project was supported by MBD Energy Ltd. The sponsors had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report and in the decision to submit the article for publication.

Supplementary material

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  1. Adams JMM, Ross AB, Anastasakis K, Hodgson EM, Gallagher JA, Jones JM, Donnison IS (2011) Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresource Technol 102:226–234CrossRefGoogle Scholar
  2. Borowitzka LJ, Borowitzka MA (1990) Commercial production of β-carotene by Dunaliella salina in open ponds. Bull Mar Sci 47:244–252Google Scholar
  3. Bruno JF, Boyer KE, Duffy J, Lee SC, Kertesz JS (2005) Effects of macroalgal species identity and richness on primary production in benthic marine communities. Ecol Lett 8:1165–1174CrossRefPubMedGoogle Scholar
  4. Bruno JF, Lee SC, Kertesz JS, Carpenter RC, Long ZT, Emmett Duffy J (2006) Partitioning the effects of algal species identity and richness on benthic marine primary production. Oikos 115:170–178CrossRefGoogle Scholar
  5. Capo T, Jaramillo J, Boyd A, Lapointe B, Serafy J (1999) Sustained high yields of Gracilaria (Rhodophyta) grown in intensive large-scale culture. J Appl Phycol 11:143–147CrossRefGoogle Scholar
  6. Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature 472:86–89CrossRefPubMedGoogle Scholar
  7. Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotech Adv 29:686–702CrossRefGoogle Scholar
  8. Cole AJ, de Nys R, Paul NA (2014) Removing constraints on the biomass production of freshwater macroalgae by manipulating water exchange to manage nutrient flux. PLoS One 9(7):e101284CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cole AJ, de Nys R, Paul NA (2015) Biorecovery of nutrient waste as protein in freshwater macroalgae. Algal Res 7:56–65CrossRefGoogle Scholar
  10. Coltman DW, O'Donoghue P, Jorgenson JT, Hogg JT, Strobeck C, Festa-Bianchet M (2003) Undesirable evolutionary consequences of trophy hunting. Nature 426:655–658CrossRefPubMedGoogle Scholar
  11. Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297:94–96CrossRefPubMedGoogle Scholar
  12. de Castro AS, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246:405–412Google Scholar
  13. Edeline E, Carlson SM, Stige LC, Winfield IJ, Fletcher JM, James JB, Haugen TO, Vøllestad LA, Stenseth NC (2007) Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. Proc Nat Acad Sci 104:15799–15804CrossRefPubMedPubMedCentralGoogle Scholar
  14. Elliott DC, Biller P, Ross AB, Schmidt AJ, Jones SB (2015) Hydrothermal liquefaction of biomass: developments from batch to continuous process. Bioresource Technol 178:147–156CrossRefGoogle Scholar
  15. Enberg K, Jørgensen C, Dunlop ES, Heino M, Dieckmann U (2009) Implications of fisheries-induced evolution for stock rebuilding and recovery. Evol Appl 2:394–414CrossRefPubMedPubMedCentralGoogle Scholar
  16. Engelhardt KAM, Ritchie ME (2001) Effects of macrophyte species richness on wetland ecosystem functioning and services. Nature 411:687–689CrossRefPubMedGoogle Scholar
  17. Entwisle TJ, Skinner S, Lewis SH, Foard HJ (2007) Algae of Australia: Batrachospermales, Thoreales, Oedogoniales and Zygnemaceae. CSIRO Publishing/Australian Biological Resources Study Collingwood, AustraliaGoogle Scholar
  18. Ernande B, Dieckmann U, Heino M (2004) Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation. Proc R Soc London B 271:415–423CrossRefGoogle Scholar
  19. Fagerström T, Briscoe DA, Sunnucks P (1998) Evolution of mitotic cell-lineages in multicellular organisms. Trends Ecol Evol 13:117–120CrossRefPubMedGoogle Scholar
  20. Garel M, Cugnasse J-M, Maillard D, Gaillard J-M, Hewison AJM, Dubray D (2007) Selective harvesting and habitat loss produce long-term life history changes in a mouflon population. Ecol Appl 17:1607–1618CrossRefPubMedGoogle Scholar
  21. Garland T Jr, Rose MR (2009) Experimental evolution: concepts, methods and applications of selection experiments. University of California PressGoogle Scholar
  22. Gellenbeck K (2012) Utilization of algal materials for nutraceutical and cosmeceutical applications—what do manufacturers need to know? J Appl Phycol 24:309–313CrossRefGoogle Scholar
  23. Gill DE, Chao L, Perkins SL, Wolf JB (1995) Genetic mosaicism in plants and clonal animals. Annu Rev Ecol Syst 26:423–444CrossRefGoogle Scholar
  24. Goldman JC, Ryther JH (1975) Mass production of marine algae in outdoor cultures. Nature 254:594–595CrossRefGoogle Scholar
  25. Gosch BJ, Magnusson M, Paul NA, Nys R (2012) Total lipid and fatty acid composition of seaweeds for the selection of species for oil-based biofuel and bioproducts. GCB Bioenergy 4:919–930CrossRefGoogle Scholar
  26. Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotech 21:210–216CrossRefGoogle Scholar
  27. Guillemin M-L, 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 favor asexual reproduction and heterozygosity. Evolution 62:1500–1519CrossRefPubMedGoogle Scholar
  28. Hafting J, Critchley A, Cornish ML, Hubley S, Archibald A (2012) On-land cultivation of functional seaweed products for human usage. J Appl Phycol 24:385–392CrossRefGoogle Scholar
  29. Hector A, Bazeley-White E, Loreau M, Otway S, Schmid B (2002) Overyielding in grassland communities: testing the sampling effect hypothesis with replicated biodiversity experiments. Ecol Lett 5:502–511CrossRefGoogle Scholar
  30. Hector A, Schmid B, Beierkuhnlein C, Caldeira M, Diemer M, Dimitrakopoulos P, Finn J, Freitas H, Giller P, Good J (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127CrossRefPubMedGoogle Scholar
  31. Hendry AP, Kinnison MT, Heino M, Day T, Smith TB, Fitt G, Bergstrom CT, Oakeshott J, Jørgensen PS, Zalucki MP, Gilchrist G, Southerton S, Sih A, Strauss S, Denison RF, Carroll SP (2011) Evolutionary principles and their practical application. Evol Appl 4:159–183CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hooper DU, Dukes JS (2004) Overyielding among plant functional groups in a long-term experiment. Ecol Lett 7:95–105CrossRefGoogle Scholar
  33. Jiménez-Escrig A, Gómez-Ordóñez E, Rupérez P (2012) Brown and red seaweeds as potential sources of antioxidant nutraceuticals. J Appl Phycol 24:1123–1132CrossRefGoogle Scholar
  34. Larkin PJ, Scowcroft WR (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theoret Appl Genet 60:197–214CrossRefGoogle Scholar
  35. Law R (2000) Fishing, selection, and phenotypic evolution. ICES J Mar Sci 57:659–668CrossRefGoogle Scholar
  36. Law W, Salick J (2005) Human-induced dwarfing of Himalayan snow lotus, Saussurea laniceps (Asteraceae). Proc Nat Acad Sci U S A 102:10218–10220CrossRefGoogle Scholar
  37. Lawton RJ, Carl C, de Nys R, Paul NA (2015) Heritable variation in growth and biomass productivity in the clonal freshwater macroalga Oedogonium. Algal Res 8:108–114CrossRefGoogle Scholar
  38. Lawton RJ, de Nys R, Paul NA (2013) Selecting reliable and robust freshwater macroalgae for biomass applications. PLoS One 8(5):e64168CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lawton RJ, de Nys R, Skinner S, Paul NA (2014) Isolation and identification of Oedogonium species and strains for biomass applications. PLoS One 9(3):e90223CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lin BB (2011) Resilience in agriculture through crop diversification: adaptive management for environmental change. Bioscience 61:183–193CrossRefGoogle Scholar
  41. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models. SAS Institute Inc., Cary, U.S.A.Google Scholar
  42. Magnusson M, Mata L, Wang N, Zhao J, de Nys R, Paul NA (2015) Manipulating antioxidant content in macroalgae in intensive land-based cultivation systems for functional food applications. Algal Res 8:153–160CrossRefGoogle Scholar
  43. Mata L, Magnusson M, Paul N, de Nys R (2016) The intensive land-based production of the green seaweeds Derbesia tenuissima and Ulva ohnoi: biomass and bioproducts. J Appl Phycol 28:365–375CrossRefGoogle Scholar
  44. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energy Rev 14:217–232CrossRefGoogle Scholar
  45. Meins F (1983) Heritable variation in plant cell culture. AnnuRev Plant Physiol 34:327–346CrossRefGoogle Scholar
  46. Meneses I, Santelices B (1999) Strain selection and genetic variation in Gracilaria chilensis (Gracilariales, Rhodophyta). J Appl Phycol 11:241–246CrossRefGoogle Scholar
  47. Moheimani N, Borowitzka M (2006) The long-term culture of the coccolithophore Pleurochrysis carterae (Haptophyta) in outdoor raceway ponds. J Appl Phycol 18:703–712CrossRefGoogle Scholar
  48. Monro K, Poore AG (2004) Selection in modular organisms: is intraclonal variation in macroalgae evolutionarily important? Am Nat 163:564–578CrossRefPubMedGoogle Scholar
  49. Monro K, Poore AG (2009) The potential for evolutionary responses to cell-lineage selection on growth form and its plasticity in a red seaweed. Am Nat 173:151–163CrossRefPubMedGoogle Scholar
  50. Mooney EH, McGraw JB (2009) Relationship between age, size, and reproduction in populations of American ginseng, Panax quinquefolius (Araliaceae), across a range of harvest pressures. Ecoscience 16:84–94CrossRefGoogle Scholar
  51. Neveux N, Magnusson M, Maschmeyer T, de Nys R, Paul NA (2014a) Comparing the potential production and value of high-energy liquid fuels and protein from marine and freshwater macroalgae. GCB Bioenergy. doi: 10.1111/gcbb.12171 Google Scholar
  52. Neveux N, Yuen A, Jazrawi C, Magnusson M, Haynes B, Masters A, Montoya A, Paul N, Maschmeyer T, de Nys R (2014b) Biocrude yield and productivity from the hydrothermal liquefaction of marine and freshwater green macroalgae. Bioresource Technol 155:334–341CrossRefGoogle Scholar
  53. Orive ME (2001) Somatic mutations in organisms with complex life histories. Theor Popul Biol 59:235–249CrossRefPubMedGoogle Scholar
  54. Park J, Craggs R (2011) Algal production in wastewater treatment high rate algal ponds for potential biofuel use. Water Sci Technol 63:2403–2410CrossRefPubMedGoogle Scholar
  55. Pereira R, Yarish C, Sousa-Pinto I (2006) The influence of stocking density, light and temperature on the growth, production and nutrient removal capacity of Porphyra dioica (Bangiales, Rhodophyta). Aquaculture 252:66–78CrossRefGoogle Scholar
  56. Picasso VD, Brummer EC, Liebman M, Dixon PM, Wilsey BJ (2008) Crop species diversity affects productivity and weed suppression in perennial polycultures under two management strategies. Crop Sci 48:331–342CrossRefGoogle Scholar
  57. Poore AGB, Fagerström T (2000) Intraclonal variation in macroalgae: causes and evolutionary consequences. Selection 1:123–134Google Scholar
  58. Proaktor G, Coulson T, Milner-Gulland EJ (2007) Evolutionary responses to harvesting in ungulates. J Anim Ecol 76:669–678CrossRefPubMedGoogle Scholar
  59. Pujol B, David P, McKey D (2005) Microevolution in agricultural environments: how a traditional Amerindian farming practice favours heterozygosity in cassava (Manihot esculenta Crantz, Euphorbiaceae). Ecol Lett 8:138–147CrossRefGoogle Scholar
  60. Reznick DN, Ghalambor CK (2005) Can commercial fishing cause evolution? Answers from guppies (Poecilia reticulata). Can J Fish Aquat Sci 62:791–801CrossRefGoogle Scholar
  61. Roberts DA, de Nys R, Paul NA (2013) The effect of CO2 on algal growth in industrial waste water for bioenergy and bioremediation applications. PLoS One 8(11):e81631CrossRefPubMedPubMedCentralGoogle Scholar
  62. Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotech Bioeng 102:100–112CrossRefGoogle Scholar
  63. Salo T, Gustafsson C, Boström C (2009) Effects of plant diversity on primary production and species interactions in brackish water angiosperm communities. Mar Ecol Prog Ser 396:261–272CrossRefGoogle Scholar
  64. Samocha TM, Fricker J, Ali AM, Shpigel M, Neori A (2015) Growth and nutrient uptake of the macroalga Gracilaria tikvahiae cultured with the shrimp Litopenaeus vannamei in an integrated multi-trophic aquaculture (IMTA) system. Aquaculture 446:263–271CrossRefGoogle Scholar
  65. Schwaegerle KE, McIntyre H, Swingley C (2000) Quantitative genetics and the persistence of environmental effects in clonally propagated organisms. Evolution 54:452–461CrossRefPubMedGoogle Scholar
  66. Snapp SS, Gentry LE, Harwood R (2010) Management intensity—not biodiversity—the driver of ecosystem services in a long-term row crop experiment. Agricult Ecosyst Environ 138:242–248CrossRefGoogle Scholar
  67. Stachowicz JJ, Best RJ, Bracken MES, Graham MH (2008a) Complementarity in marine biodiversity manipulations: reconciling divergent evidence from field and mesocosm experiments. Proc Nat Acad Sci 105:18842–18847CrossRefPubMedPubMedCentralGoogle Scholar
  68. Stachowicz JJ, Bruno JF, Duffy JE (2007) Understanding the effects of marine biodiversity on communities and ecosystems. Annu Rev Ecol Evol Systemat 38:739–766CrossRefGoogle Scholar
  69. Stachowicz JJ, Graham M, Bracken MES, Szoboszlai AI (2008b) Diversity enhances cover and stability of seaweed assemblages: the role of heterogeneity and time. Ecology 89:3008–3019CrossRefGoogle Scholar
  70. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845CrossRefPubMedGoogle Scholar
  71. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632CrossRefPubMedGoogle Scholar
  72. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720CrossRefGoogle Scholar
  73. Walsh MR, Munch SB, Chiba S, Conover DO (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecol Lett 9:142–148CrossRefPubMedGoogle Scholar
  74. Woertz I, Feffer A, Lundquist T, Nelson Y (2009) Algae grown on dairy and municipal wastewater for simultaneous nutrient removal and lipid production for biofuel feedstock. J Envi Eng 135:1115–1122CrossRefGoogle Scholar
  75. Xin L, Hong-ying H, Ke G, Ying-xue S (2010) Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresource Technol 101:5494–5500CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Rebecca J Lawton
    • 1
    • 2
  • Nicholas A Paul
    • 1
    • 3
  • Dustin J. Marshall
    • 4
  • Keyne Monro
    • 4
  1. 1.MACRO—the Centre for Macroalgal Resources and Biotechnology and College of Science and EngineeringJames Cook UniversityTownsville CityAustralia
  2. 2.Bay of Plenty Regional CouncilMount MaunganuiNew Zealand
  3. 3.Faculty of Science, Health, Education and EngineeringUniversity of the Sunshine CoastMaroochydoreAustralia
  4. 4.Centre for Geometric Biology and School of Biological SciencesMonash UniversityClaytonAustralia

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