Advertisement

Marine Biology

, Volume 152, Issue 3, pp 677–686 | Cite as

Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the Northern Hemisphere after exposure to simulated El Niño stress

  • Lydia B. Ladah
  • José A. Zertuche-González
Research Article

Abstract

Many organisms survive stressful conditions through a tolerant life history stage. The life history known as the alternation of generations is typical of temperate kelps, producing diploid macroscopic stages, and both haploid and diploid microscopic stages, with the haploid stages thought to be stress tolerant. The survival of microscopic stages of the giant kelp Macrocystispyrifera during El Niño has been suggested, yet has never been tested. This mechanism could be critical for population persistence, particularly at the southern limit of the range in the Northern Hemisphere, which is greatly impacted by El Niño conditions. The purpose of this study was to determine if microscopic stages of giant kelp could survive and recover from El Niño-type conditions and whether those from a population near its southern limit were more tolerant than a population at the center of its range. Microscopic stages were exposed to a laboratory simulation of potential El Niño conditions (high temperature, with and without light and nitrate) for 8 weeks and then allowed to recover at optimal conditions (low temperature and high nitrate) for 8 weeks, while controls were left at optimal conditions the entire 16 weeks test period. Haploid developmental stages from both populations survived and recovered from stressful conditions with no population level effect, suggesting haploid stress-tolerance may be widespread. The more advanced the developmental stage, and the presence of nitrate, resulted in significantly greater recovery for haploids. Yet, none of these stages were able to go on to produce sporophytes, whereas all controls did. There was a large population-level effect for diploids, however, with only microscopic diploid stages (embryonic sporophytes) from the southern-limit population recovering from El Niño simulated stress, suggesting ecotypic adaptation for microscopic sporophytes. Diploid recovery was significantly greater with light. We propose that the diploid stage is the most likely to survive and recover after El Niño conditions, as it would avoid obligate egg and sperm encounters after the stress period. The survivorship of the microscopic diploid in a seed bank analogue may be how the isolated southern-limit populations are able to recover after mass disappearance during El Niño.

Keywords

Stress Exposure Life History Stage Microscopic Stage Southern Limit Kelp Forest 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The companies of Productos del Pacifico and Abulones Cultivados, the Fishing Cooperative in Bahia Tortugas, and the Fishing Cooperative Estaban Cantu assisted with field research logistics and permits. Diving would not have been possible without assistance from J. Guzman and R. Bermudez. Marco Aurelio provided laboratory assistance. The authors acknowledge funding and support from the UABC (4078-22) and SIMACCONACYT (970106007) grants to J.A.Z., and UC MEXUSCONACYT awards, IAI-EPCOR (CRN-062), AMELIS-CONACYT (J37689/V), and SEP-CONACYT (J50046) research grants to L.B.L. Special thanks to Dr. C. Barilloti, Dr. A. Cabello, and P. Chagoya.

References

  1. Bernstein H, Byerly H, Hopf F, Michod R (1985) Genetic damage, mutation, and the evolution of sex. Science 229:1277–1281CrossRefGoogle Scholar
  2. Bolton J, Luning K (1982) Optimal growth and maximal survival temperatures of Atlantic Laminaria species in culture. Mar Biol 87:131–135CrossRefGoogle Scholar
  3. Chapman ARO (1984) Reproduction, recruitment, and mortality of two species of Laminaria in southwest Nova Scotia. J Exp Mar Biol Ecol 78:99–109CrossRefGoogle Scholar
  4. Clarke A (2003). Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581CrossRefGoogle Scholar
  5. Clayton M (1987) Isogamy and a fucalean type of life history in the antarctic brown algae, Ascoseira mirabilis. Botanica Marina 30:447–54CrossRefGoogle Scholar
  6. Clayton M (1990) The adaptive significance of life history characters in selected orders of marine brown macroalgae. Aust J Ecol 15:439–452CrossRefGoogle Scholar
  7. Cohen CS, Strathman R (1996) Embryos at the edge of tolerance: effects of environmental and structure of egg masses on supply of oxygen to embryos. Biol Bull 190:8–15CrossRefGoogle Scholar
  8. Crow JF, Kimura M (1978) Evolution in sexual and asexual populations. Am Nat 909:439–450Google Scholar
  9. Dawson Y (1951) A further study of upwelling and associated vegetation along Pacific Baja California, Mexico. J Mar Res 10:39–58Google Scholar
  10. Dawson Y (1952) Circulation within Bahía Vizcaino, Baja California, and its effects on marine vegetation. Am J Bot 39:425–432CrossRefGoogle Scholar
  11. Dayton P (1973) Dispersion and persistence of the annual intertidal alga Postelsia palmaeformis. Ecology 54:433–438CrossRefGoogle Scholar
  12. Dayton P (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–45CrossRefGoogle Scholar
  13. Dayton P, Tegner M (1984) Catastrophic storms, El Niño, and patch stability in a southern California kelp community. Science 224:283–85CrossRefGoogle Scholar
  14. Dean T, Jacobsen FR (1984) Growth of juvenile Macrocystis pyrifera (Laminariales) in relation to environmental factors. Mar Biol 83:301–11CrossRefGoogle Scholar
  15. Devinny J, Volse L (1978) Effects of sediments on the development of Macrocystis pyrifera gametophytes. Mar Biol 48:343–348CrossRefGoogle Scholar
  16. Deysher L, Dean T (1986a). In situ recruitment of sporophytes of the giant kelp, Macrocystis pyrifera: effects of physical factors. J Exp Mar Biol Ecol 103:41–63CrossRefGoogle Scholar
  17. Deysher L, Dean T (1986b) Interactive effect of light and temperature on sporophyte production in the giant kelp, Macrocystis pyrifera. Mar Biol 93:17–20CrossRefGoogle Scholar
  18. Durazo R, Baumgartner T (2002) Evolution of oceanographic conditions off Baja California: 1997–1999. Prog Oceanogr 54:7–31CrossRefGoogle Scholar
  19. Edwards M (2004) Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia 138(3):436–447CrossRefGoogle Scholar
  20. Espinoza J, Chapman ARO (1983) Ecotypic differentiation of Laminaria longicruris in relation to seawater nitrate concentration. Mar Biol 74:213–218CrossRefGoogle Scholar
  21. Fields P, Graham J, Rosenblat H, Somero G (1993) Effects of expected global climate change on marine faunas. Trends Ecol Evol 8:361–3671CrossRefGoogle Scholar
  22. Foster M, Schiel D (1985) The ecology of giant kelp forests in California: a community profile. U.S. Fish and wildlife service, Biological Report 85(7.2)Google Scholar
  23. Gerard V (1984) Physiological effects of El Niño on giant kelp in southern California. Mar Biol Letts 5:317–322Google Scholar
  24. Gerard V (1988) Ecotypic differentiation in light related traits of the kelp Laminaria saccharina. Mar Biol 97:25–36CrossRefGoogle Scholar
  25. Gerard V (1990) Ecotypic differentiation in the kelp Laminaria saccharina:phase-specific adaptation in a complex life cycle. Mar Biol 107:519–28CrossRefGoogle Scholar
  26. Gerard V (1997) The role of nitrogen nutrition in high-temperature tolerance of the kelp Laminaria saccharina (Chromophyta). J Phycol 33:800–810CrossRefGoogle Scholar
  27. Gerard V, Dubois K (1988) Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina. Mar Biol 97:575–580CrossRefGoogle Scholar
  28. Hernández-Carmona G, Rodríguez-Montesinos Y, Casas-Valdez M, Vilchis M, Sanchez-Rodríguez I (1991) Evaluation of the beds of Macrocystis pyrifera in the Baja California Peninsula, Mexico III. Summer 1986 and seasonal variation. Ciencias Marinas 17:121–145CrossRefGoogle Scholar
  29. Hoffman A, Santelices B (1991) Banks of algal microscopic forms: hypotheses on their functioning and comparisons with seed banks. Mar Ecol Prog Ser 79:185–194CrossRefGoogle Scholar
  30. Hummel H, Amiard-Triquet C, Bachelet G, Desprez M, Marchand J, Sylvand B, Amiard J, Rybarczyk R, Boogards H, Sinke J, de Wolf L (1996) Sensitivity to stress of the estuarine bivalve Macoma balthica from areas between the Netherlands and its southern limits. J Sea Res 35:315–321CrossRefGoogle Scholar
  31. Huyer A, Smith RL (1985) The signature of El Niño off Oregon in 1982–83. J Geophys Res 90:7133–7142CrossRefGoogle Scholar
  32. Jackson GA (1977) Nutrients and production of giant kelp, Macrocystis pyrifera, off southern California. Limnol Oceanogr 22:979–995CrossRefGoogle Scholar
  33. John D (1994) Alternation of generation in algae: its complexity, maintenance and evolution. Biol Rev 69:275–91CrossRefGoogle Scholar
  34. Kahru M, Mitchell G (2000) Influence of the 1997–98 El Niño on the surface chlorophyll in the California current. J Geophys Lett 26:2937–2940CrossRefGoogle Scholar
  35. Kinlan B, Graham M, Sala E, Dayton P (2003) Arrested development of giant kelp (Macrocystis pyrifera, Phaeophyceae) embryonic sporophytes: a mechanism for delayed recruitment in perennial kelps. J Phycol 39:47–57CrossRefGoogle Scholar
  36. Kopczak C, Zimmerman R, Kremer J (1991) Variation in nitrogen physiology and growth among geographically isolated populations of the giant kelp Macrocystis pyrifera (Phaeophyta). J Phycol 27:149–158CrossRefGoogle Scholar
  37. Ladah L (2003) The shoaling of nutrient-enriched subsurface waters as a mechanism to sustain primary productivity off Central Baja California during El Niño winters. J Mar Systems 42:145–152CrossRefGoogle Scholar
  38. Ladah L, Zertuche-Gonzalez JA (2004) Giant kelp (Macrocystis pyrifera) survival in deep water (25–40 m) during El Niño of 1997–1998 in Baja California, Mexico. Botanica Marina 47:367–372CrossRefGoogle Scholar
  39. Ladah L, Zertuche-Gonzalez JA, Hernandez-Carmona G (1999) Rapid recovery giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997–1998. J Phycol 35:1106–1112CrossRefGoogle Scholar
  40. Lee JA, Brinkuis BH (1986) Reproductive phenology of Laminaria saccharina (L.) Lamour (Phaeophyta) at the southern limit of its distribution in the northwestern Atlantic Ocean. J Phycol 22:276–285CrossRefGoogle Scholar
  41. Lewis WM (1985) Nutrient scarcity as an evolutionary cause of haploidy. Am Nat 125:692–701CrossRefGoogle Scholar
  42. Lubchenco J, Cubit J (1980) Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology 64:1116–23CrossRefGoogle Scholar
  43. Lynn R, Simpson J (1987) The California current system: the seasonal variability of its physical characteristics. J Geophys Res 92:12947–966CrossRefGoogle Scholar
  44. Martinez E (1999) Latitudinal differences in thermal tolerance among microscopic sporophytes of the kelp Lessonia nigrescens (Phaeophyta: Laminariales). Pac Sci 53(1):74–81Google Scholar
  45. Martinez E, Santelices B (1998) Selective mortality on haploid and diploid microscopic stages of Lessonia nigrescens Bory (Phaeophyta, Laminariales). J Exp Mar Biol Ecol 229:219–239CrossRefGoogle Scholar
  46. Maynard-Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, pp 222Google Scholar
  47. McGowan J, Cayan D, Dorman L (1998) Climate–ocean variability and ecosystem response in the Northeast Pacific. Science 281:210–217CrossRefGoogle Scholar
  48. Miller A, Schneider N (2000) Interdecadal climate regime dynamics in the North Pacific Ocean: theories, observations and ecosystem impacts. Prog Oceanogr 47:355–379CrossRefGoogle Scholar
  49. North W (1994) Review of Macrocystis biology. In: Akatsuka I (ed) Biology of economic algae. Academic Publishing, Netherlands, pp 447–527Google Scholar
  50. North W, Zimmerman R (1984) Influences of macronutrients and water temperatures on summertime survival of Macrocystis canopies. Hydrobiología 116/117:419–24CrossRefGoogle Scholar
  51. Ott F (1965) Synthetic media and techniques for the xenic culture of marine algae and flagellates. VA J Sci (N.S.)Google Scholar
  52. Palacios-Hernandez E, Argote-Espinosa M, Amador-Buenrostro A, Mancilla-Peraza M (1996) Simulación de la circulación barotropica inducida por viento en Bahía Sebastián Vizcaíno, B.C. Atmosfera 9:171–188Google Scholar
  53. Perrot V, Richerd S, Valero M (1991) Transition from haploidy to diploidy. Nature 351:315–317CrossRefGoogle Scholar
  54. Portner H (2002) Climate variations and the physiological basis of temperature dependant biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A Mol Integr Physiol 133:303–321CrossRefGoogle Scholar
  55. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, A. Hattori (eds) Cultures and collections of algae. Proc US–Japan Conf. Hakone. Sept 1966. Japanese Society of Plant Physiology 63–75Google Scholar
  56. Reed D, Neushul M, Ebeling A (1991) Role of density on gametophyte growth and reproduction in the kelps Macrocystis pyrifera and Pterygophora californica. J Phycol 27:361–366CrossRefGoogle Scholar
  57. Reed D, Anderson T, Ebeling A, Anghera M (1997) The role of reproductive synchrony in the colonization potential of kelp. Ecology 78(8):2443–2457CrossRefGoogle Scholar
  58. Sagarin R, Barry J, Gilman S, Baxter C (1999) Climate-related change in an intertidal community over short and long time scales. Ecol Monogr 69:465–490CrossRefGoogle Scholar
  59. Santelices B (1990) Patterns of reproduction, dispersal, and recruitment in seaweeds. Oceanogr Mar Biol Annu Rev 28:177–276Google Scholar
  60. Santelices B, Hoffman A, Aedo D, Bobadilla M, Otaiza R (1995) A bank of microscopic forms on disturbed boulders and stones in tide pools. Mar Ecol Prog Ser 129:215–228CrossRefGoogle Scholar
  61. Scagel R, Bandoni R, Maze J, Rouse R, Scholfield G, Stein J (1982) Nonvascular plants. An evolutionary survey. Wadsworth publishing Company, BelmontGoogle Scholar
  62. Seymour R, Tegner M, Dayton P, Parnell P (1989) Storm wave induced mortality of giant kelp, Macrocystis pyrifera, in southern California. Estuar Coast Shelf Sci 28:277–292CrossRefGoogle Scholar
  63. Tegner M, Dayton P (1987) El Niño effects on southern California kelp communities. Adv Ecol Res 17:243–279CrossRefGoogle Scholar
  64. Tegner M, Dayton P (1991) Sea urchins, El Niño’s, and long term stability of southern California kelp forest communities. Mar Ecol Prog Ser 77:49–63CrossRefGoogle Scholar
  65. Tegner M, Dayton P, Edwards P, Riser K (1996) Is there evidence for long-term climatic change in Southern California kelp forests? Calcofi Reports 37:111–126Google Scholar
  66. tom Dieck I (1993) Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta): ecological and biogeographic implications. Mar Ecol Prog Ser 100:253–264CrossRefGoogle Scholar
  67. Trowbridge CD (1994) Life at the edge: population dynamics and salinity tolerance of a high intertidal, pool-dwelling ascoglossan opisthobranch on New Zealand rocky shores. J Exp Mar Biol Ecol 182:65–84CrossRefGoogle Scholar
  68. Vermeij GJ (1980) Biogeography and adaptation––patterns of marine life. Harvard University Press, Cambridge, p 332Google Scholar
  69. Zimmerman R, Kremer J (1984) Episodic nutrient supply to a kelp forest ecosystem in Southern California. J Mar Res 42:591–604CrossRefGoogle Scholar
  70. Zimmerman R, Robertson DL (1985) Effects of El Niño on local hydrography and growth of giant kelp Macrocystis pyrifera, at Santa Catalina Island, California. Limnol Oceanogr 30:1298–1302CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Lydia B. Ladah
    • 1
    • 2
  • José A. Zertuche-González
    • 3
  1. 1.Department of Biological OceanographyCICESEEnsenadaMexico
  2. 2.San DiegoUSA
  3. 3.Instituto de Investigaciones OceanológicasUniversidad Autónoma de Baja CaliforniaEnsenadaMexico

Personalised recommendations