Species-specific defense strategies of vegetative versus reproductive blades of the Pacific kelps Lessonia nigrescens and Macrocystis integrifolia

Marine Biology

Volumn 155, Issue 1, 2008, Pages 51-62

  Pansch, Christian ^a   Gómez, Ivan ^b   Rothäusler, Eva ^a   Veliz, Karina ^b   Thiel, Martin ^c,d  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c UNIVERSIDAD CATÓLICA DEL NORTE   (Chile)

^d CENTRO DE ESTUDIOS AVANZADOS EN ZONAS ÁRIDAS CEAZA   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPOD; BROWN ALGA; CHEMICAL DEFENSE; DEFENSE MECHANISM; GRAZING; HERBIVORY; KELP FOREST; ONTOGENY;

PACIFIC OCEAN; PACIFIC OCEAN (SOUTHEAST);

ALGAE; LAMINARIALES; LESSONIA NIGRESCENS; MACROCYSTIS; MACROCYSTIS INTEGRIFOLIA; PARHYALELLA; PHAEOPHYCEAE; ULVA;

EID: 46649102017     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-008-1006-z     Document Type: Article

References (76)

1. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1-91. doi: 10.1016/S0065-2296(05) 43001-3
2. Arnold TM, Targett NM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406-408. doi: 10.1034/j.1600-0706.2003. 11680.x
3. Brawley SH, Johnson LE (1992) Gametogenesis, gametes and zygotes: an ecological perspective on sexual reproduction in the algae. Br Phycol J 27:233-252. doi: 10.1080/00071619200650241
4. Brawley SH, Johnson LE, Pearson GA (1999) Gamete release at low tide in fucoid algae: maladaptive or advantageous? Am Zool 39:218-229
5. Buschmann A, Santelices B (1987) Micrograzers and spore release in Iridaea laminarioides Bory (Rhodophyta: Gigartinales). J Exp Mar Biol Ecol 108:171-179. doi: 10.1016/S0022-0981(87) 80021-7
6. Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345-363. doi: 10.2307/1942551
7. Cronin G (2001) Resource allocation in seaweed and marine invertebrates: chemical defense patterns in relation to defense theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 325-353
8. Cronin G, Hay ME (1996) Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105:361-368. doi: 10.1007/BF00328739
9. Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201-219
10. Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483-506. doi: 10.1890/0012-9615(2003) 073[0483:PNQIWC]2.0.CO;2
11. Duffy JE, Hay ME (1990) Seaweed adaptation to herbivory. Bioscience 40:368-375. doi: 10.2307/1311214
12. Duffy JE, Paul VJ (1992) Prey nutritional quality and effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333-339. doi: 10.1007/BF00317689
13. Edding M, Fonck E, Macchiavello J (1994) Lessonia. In: Akatsuka I (ed) Biology of economic algae. Academic Publishing, The Hague Netherlands, pp 407-446
14. Edgar GJ (ed) (2000) Australian marine life: the plants and animals of temperate waters. Reed New Holland, Sydney
15. Fagerström T (1989) Anti-herbivore chemical defense in plants: a note on the concept of cost. Am Nat 133:281-287. doi: 10.1086/284918
16. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005a) Within-thallus variation in chemical and physical defenses in two species of ecologically dominant brown macroalgae from the Antarctic Peninsula. J Exp Mar Biol Ecol 322:1-12. doi: 10.1016/j.jembe.2005.01.010
17. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005b) Variation in phlorotannin content within two species of brown macroalgae (Desmarestia anceps and D. menziesii) from the Western Antarctic Peninsula. Polar Biol 28:680-686. doi: 10.1007/s00300-005-0735-4
18. Gómez I, Orostegui M, Huovinen P (2007) Morpho-functional patterns of photosynthesis in the south Pacific kelp Lessonia nigrescens: Effects of UV radiation on 14C fixation and primary photochemical reactions. J Phycol 43:55-64. doi: 10.1111/j.1529-8817.2006.00301.x
19. Harper MK, Bubni TS, Copp BR, James RD, Lindsay BS, Richardson AD et al (2001) Introduction to the chemical ecology of marine natural products. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 3-69
20. Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111-145. doi: 10.1146/annurev.es.19. 110188.000551
21. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:285-335. doi: 10.1086/417659
22. Hoffmann A, Santelices B (eds) (1997) Flora marina de Chile central: marine flora at central Chile. Universidad Católica de Chile, Santiago
23. Honkanen T, Jormalainen V, Hemmi A, Mäkinen A, Heikkilä N (2002) Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 9:332-338
24. Jormalainen V, Honkanen T (2008) Macroalgal chemical defenses and their roles in structuring temperate marine communities. In: Amsler CD (ed) Algal chemical ecology. Springer, Heidelberg, pp 57-89
25. Jormalainen V, Honkanen T, Koivikko R, Eränen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640-650. doi: 10.1034/j.1600-0706.2003.12635.x
26. Jormalainen V, Honkanen T, Vesakoski O, Koivikko R (2005) Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas). J Exp Mar Biol Ecol 317:143-157. doi: 10.1016/j.jembe.2004.11.021
27. Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195-212. doi: 10.1007/s10886-005-0984-2
28. Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25-44. doi: 10.1086/283610
29. Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu Rev Ecol Syst 12:405-437. doi: 10.1146/annurev.es.12.110181.002201
30. Lüder UH, Clayton MN (2004) Induction of phlorotannins in the brown macroalga Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory-the first microscopic study. Planta 218:928-937. doi: 10.1007/s00425-003-1176-3
31. Macaya EC, Thiel M (2008) In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast. J Exp Mar Biol Ecol 354:28-38. doi: 10.1016/j.jembe.2007.10.005
32. Macaya EC, Rothäusler E, Thiel M, Molis M, Wahl M (2005) Induction of defenses and within-alga variation of palatability in two brown algae from the northern-central coast of Chile: effects of mesograzers and UV radiation. J Exp Mar Biol Ecol 325:214-227. doi: 10.1016/j.jembe.2005.05.004
33. Martinez EA (1996) Micropopulation differentiation in phenol content and susceptibility to herbivory in the Chilean kelp Lessonia nigrescens (Phaeophyta, Laminariales). Hydrobiologia 326/327:205-211. doi: 10.1007/BF00047808
34. Maschek JA, Baker BJ (2008) The chemistry of algal secondary metabolism. In: Amsler CD (ed) Algal chemical ecology. Springer, Heidelberg, pp 1-24
35. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119-161. doi: 10.1146/annurev.es.11.110180.001003
36. Medeiros HE, da Gama BAP, Gallerani G (2007) Antifouling activity of seaweed extracts from Guarujá, Sao Paulo, Brazil. Braz J Oceanogr 55:257-264. doi: 10.1590/S1679-87592007000400003
37. Neushul M (1963) Studies on the giant kelp, Macrocystis. II. Reproduction. Am J Bot 50:354-359. doi: 10.2307/2440152
38. Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157-169. doi: 10.3354/meps034157
39. Pavia H, Toth GB (2008) Macroalgal models in testing and extending defense theories. In: Amsler CD (ed) Algal chemical ecology. Springer, Heidelberg, pp 147-172
40. Pavia H, Cervin G, Lindgren A, Aberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139-146. doi: 10.3354/meps157139
41. Pavia H, Toth GB, Aberg P (2002) Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891-897
42. Peckol P, Krane JM, Yates JL (1996) Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar Ecol Prog Ser 138:209-217. doi: 10.3354/meps138209
43. Pérez-Schultheiss J, Crespo JE (2008) A new species of Parhyalella Kunkel, 1910 (Amphipoda, Talitroidea, Dogielinotidae) from the coast of Chile. Zootaxa 1724:61-68
44. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82-86. doi: 10.1007/BF00789935
45. Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332-1334. doi: 10.1126/science.192.4246.1332
46. Raven JA (2003) Long-distance transport in non-vascular plants. Plant Cell Environ 26:73-85. doi: 10.1046/j.1365-3040.2003.00920.x
47. Reed D, Ebeling A, Anderson T, Anghera M (1996) Differential reproductive responses to fluctuating resources in two seaweeds with different reproductive strategies. Ecology 77:300-316. doi: 10.2307/2265679
48. Rothäusler E, Thiel M (2006) Effect of detachment on the palatability of two kelp species. J Appl Phycol 18:423-435. doi: 10.1007/s10811-006-9053-7
49. Rothäusler E, Macaya EC, Molis M, Wahl M, Thiel M (2005) Laboratory experiments examining inducible defense show variable responses of temperate brown and red macroalgae. Rev Chil Hist Nat 78:603-614
50. Santelices B, Ugarte R (1987) Algal life-history strategies and resistance to digestion. Mar Ecol Prog Ser 35:267-275. doi: 10.3354/meps035267
51. Santelices B, Castilla JC, Cancino J, Schmiede P (1980) Comparative ecology of Lessonia nigrescens and Durvillaea antarctica (Phaeophyta) in Central Chile. Mar Biol (Berl) 59:119-132. doi: 10.1007/BF00405461
52. Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125-139
53. Schoenwaelder MEA, Clayton MN (1999) The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161-166
54. Shibata T, Kawaguchi S, Hama Y, Inagaki M, Yamaguchi K, Nakamura T (2004) Local and chemical distribution of phlorotannins in brown algae. J Appl Phycol 16:291-296. doi: 10.1023/B:JAPH.0000047781.24993.0a
55. Steinberg PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405-407. doi: 10.1126/science.223.4634.405
56. Steinberg PD (1985) Feeding preferences of Tegula funebralis and chemical defenses of marine brown algae. Ecol Monogr 53:333-349. doi: 10.2307/1942581
57. Steinberg PD, Van Altena IA (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189-222. doi: 10.2307/2937093
58. Stekoll MS, Else PV (1990) Cultivation of Macrocystis integrifolia (Laminariales, Phaeophyta) in southeastern Alaskan waters. Hydrobiologia 204/205:445-451. doi: 10.1007/BF00040269
59. Steneck RS, Watling LE (1982) Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar Biol (Berl) 68:299-319. doi: 10.1007/BF00409596
60. Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195-205. doi: 10.1046/j.1529-8817.1998.340195.x
61. Targett NM, Arnold TM (2001) Effects of secondary metabolites on digestion in marine herbivores. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 391-411
62. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68-76. doi: 10.1007/s00442-002-0944-2
63. Toth GB, Pavia H (2002a) Intraplant habitat and feeding preference of two gastropod herbivores inhabiting the kelp Laminaria hyperborea. J Mar Biol Assoc UK 82:1-5. doi: 10.1017/S0025315402005416
64. Toth GB, Pavia H (2002b) Lack of phlorotannin induction in the kelp Laminaria hyperborea in response to grazing by two gastropod herbivores. Mar Biol (Berl) 140:403-409. doi: 10.1007/s002270100707
65. Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425-434. doi: 10.1111/j.1365-2745.2007.01224.x
66. Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defences of valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612-618. doi: 10.1890/04-0484
67. Tugwell S, Branch GM (1989) Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defense theory. J Exp Mar Biol Ecol 129:219-230. doi: 10.1016/0022-0981(89) 90104-4
68. Tuomi J, Ilvessalo H, Niemelä P, Sirén S, Jormalainen V (1989) Within-plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus L. Bot Mar 32:505-509
69. Van Alstyne KL (1995) Comparison of three methods for quantifying brown algal polyphenolic compounds. J Chem Ecol 21:45-58. doi: 10.1007/BF02033661
70. Van Alstyne KL, Houser LT (2003) Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar Ecol Prog Ser 250:175-181. doi: 10.3354/meps250175
71. Van Alstyne KL, McCarthy JJ, Hustead CL, Kearns LJ (1999) Phlorotannin allocation among tissues of northeastern pacific kelps and rockweeds. J Phycol 35:483-492. doi: 10.1046/j.1529-8817.1999.3530483.x
72. Van Alstyne KL, Wolfe GV, Freidenburg TL, Neill A, Hicken C (2001) Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213:53-65. doi: 10.3354/meps213053
73. Vinueza LR, Branch GM, Branch LM, Bustamente RH (2006) Top-down herbivory and bottom-up El Nino effects on Galapagos rocky-shore communities. Ecol Monogr 76:111-131. doi: 10.1890/04-1957
74. Winter FC, Estes JA (1992) Experimental evidence for the effects of polyphenolic compounds from Dictyoneurum californicum (Phaeophyta; Laminariales) on feeding rate and growth in the red abalone (Haliotus rufescens). J Exp Mar Biol Ecol 155:263-277. doi: 10.1016/0022-0981(92) 90067-K
75. Wotton RS (2004) The ubiquity and many roles of exopolymers (EPS) in aquatic systems. Sci Mar 68:13-21
76. Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757-1766. doi: 10.2307/1939934