Importance of plasticity and local adaptation for coping with changing salinity in coastal areas: A test case with barnacles in the Baltic Sea

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Wrange, Anna Lisa ^a   André, Carl ^a   Lundh, Torbjörn ^b   Lind, Ulrika ^a   Blomberg, Anders ^a   Jonsson, Per J ^a   Havenhand, Jon N ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Balanus (Amphibalanus) improvisus; Baltic Sea; Common garden experiment; Crustacea; Evolutionary change; Gompertz growth model; Phenotypic plasticity

Indexed keywords

COASTAL ZONE; CRUSTACEAN; ENVIRONMENTAL CONDITIONS; GROWTH RATE; LOCAL ADAPTATION; MORTALITY; PHENOTYPIC PLASTICITY; PREDATION; SALINITY; SHELL;

ATLANTIC OCEAN; BALTIC SEA; KATTEGAT; NORTH SEA; SKAGERRAK;

BALANUS IMPROVISUS; CRUSTACEA; THORACICA;

SEA WATER;

ACCLIMATIZATION; ADAPTATION; ANIMAL; ANIMAL SHELL; ARTICLE; BARNACLE; CHEMISTRY; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY; REPRODUCTION; SALINITY; SEA;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANIMAL SHELLS; ANIMALS; ECOSYSTEM; OCEANS AND SEAS; PHENOTYPE; REPRODUCTION; SALINITY; SEAWATER; THORACICA;

EID: 84906513709     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-156     Document Type: Article

References (107)

1. Steric sea level variations during 1957-1994: Importance of salinity. Antonov JI, Levitus S, Boyer TP, J Geophysl Res C 2002 107 8013
2. Linear trends in salinity for the world ocean, 1955-1998. Boyer TP, Levitus S, Antonov JI, Locarnini RA, Garcia HE, Geophys Res Lett 2005 32 01604
3. Comparing reconstructed past variations and future projections of the Baltic Sea ecosystem-first results from multi-model ensemble simulations. Meier HEM, Andersson HC, Arheimer B, Blenckner T, Chubarenko B, Donnelly C, Eilola K, Gustafsson BG, Hansson A, Havenhand J, Höglund A, Kuznetsov I, MacKenzie BR, Müller-Karulis B, Neumann T, Niiranen S, Piwowarczyk J, Raudsepp U, Reckermann M, Ruoho-Airola T, Savchuk OP, Schenk F, Schimanke S, Väli G, Weslawski J-M, Zorita E, Environ Res Lett 2012 7 034005
4. Impacts of Ocean Warming and Ocean Acidification on Marine Invertebrate Life History Stages: Vulnerabilities and Potential For Persistence in a Changing Ocean. Byrne M, Oceanography and Marine Biology: An Annual Review, Volume 49 Boca Raton: Crc Press-Taylor & Francis Group, Gibson RN, Atkinson RJA, Gordon JDM, 2011 1 42
5. Ocean acidification: the other CO2 problem. Doney SC, Fabry VJ, Feely RA, Kleypas JA, Ann Rev Mar Sci 2009 1 169 192
6. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP, Glob Chang Biol 2013 19 1884 1896
7. Increased freshwater discharge shifts the trophic balance in the coastal zone of the northern Baltic Sea. Wikner J, Andersson A, Glob Chang Biol 2012 18 2509 2519
8. The role of organic osmolytes in osmoregulation: From bacteria to mammals. Kinne RKH, J Exp Zool 1993 265 346 355
9. Physiological responses to salinity changes of the isopod Idotea chelipes from the Baltic brackish waters. Lapucki T, Nonnant M, Comp Biochem Physiol A-Mol Integr Physiol 2008 149 299 305
10. Does scope for growth change as a result of salinity stress in the amphipod Gammarus oceanicus? Normant M, Lamprecht I, J Exp Mar Biol Ecol 2006 334 158 163
11. Tolerance of the barnacle Balanus amphitrite amphitrite (Darwin) to salinity and temperature stress: effects of previous experience. Qiu JW, Qian PY, Mar Ecol-Prog Ser 1999 188 123 132
12. Growth, tolerance to low salinity, and osmoregulation in decapod crustacean larvae. Torres G, Gimenez L, Anger K, Aquat Biol 2011 12 249 260
13. Zoobenthic diversity-gradients in the Baltic Sea: Continuous post-glacial succession in a stressed ecosystem. Bonsdorff E, J Exp Mar Biol Ecol 2006 330 383 391
14. Status of biodiversity in the Baltic Sea. Ojaveer H, Jaanus A, MacKenzie BR, Martin G, Olenin S, Radziejewska T, Telesh I, Zettler ML, Zaiko A, PLoS One 2010 5 12467
15. A review of the history of the Baltic Sea, 13.0-8.0 KA BP. Björck S, Quat Int 1995 27 19 40
16. Past occurrences of hypoxia in the Baltic Sea and the role of climate variability, environmental change and human impact. Zillén L, Conley DJ, Andren T, Andren E, Björck S, Earth Sci Rev 2008 91 77 92
17. Non-native species and rates of spread: Lessons from the brackish Baltic Sea. Leppäkoski E, Olenin S, Biol Invas 2000 2 151 163
18. Leppäranta M, Myrberg K, Physical Oceanography of the Baltic Sea Chichester, UK: Springer Praxis Publishing Ltd 2009
19. Modeling the variations of salinity and temperature in the large Gulfs of the Baltic Sea. Omstedt A, Axell LB, Cont Shelf Res 2003 23 265 294
20. Local adaptation of Ceramium tenuicorne (Ceramiales, Rhodophyta) within the Baltic Sea. Bergström L, Kautsky L, J Phycol 2006 42 36 42
21. Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Johannesson K, André C, Mol Ecol 2006 15 2013 2029
22. The future of Baltic Sea populations: local extinction or evolutionary rescue? Johannesson K, Smolarz K, Grahn M, Andre C, Ambio 2011 40 179 190
23. Estimating uncertainties of projected Baltic Sea salinity in the late 21st century. Meier HEM, Kjellstrom E, Graham LP, Geophys Res Lett 2006 33 15705
24. Pigliucci M, Phenotypic Plasticity-Beyond Nature and Nurture Baltimore: The John Hopkins University Press 2001
25. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Reusch TBH, Evol Appl 2014 7 104 122
26. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. Crispo E, J Evol Biol 2008 21 1460 1469
27. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Ghalambor CK, McKay JK, Carroll SP, Reznick DN, Funct Ecol 2007 21 394 407
28. Genetic assimilation of an acquired character. Waddington CH, Evolution 1953 7 118 126
29. Climate change and evolution: disentangling environmental and genetic responses. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J, Mol Ecol 2008 17 167 178
30. Costs and limits of phenotypic plasticity. DeWitt TJ, Sih A, Wilson DS, Trends Ecol Evol 1998 13 77 81
31. Costs of phenotypic plasticity. Releya RA, Am Nat 2002 159 272 282
32. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Lande R, J Evol Biol 2009 22 1435 1446
33. Phenotypic plasticity and evolution by genetic assimilation. Pigliucci M, Murren CJ, Schlichting CD, J Exp Biol 2006 209 2362 2367
34. Adaptive phenotypic plasticity-target or by-product of selection in a variable environment. Via S, Am Nat 1993 142 352 365
35. Natural selection, larval dispersal, and the geography of phenotype in the sea. Sotka EE, Integr Comp Biol 2012 52 538 545
36. Variable salinity tolerance in ascidian larvae is primarily a plastic response to the parental environment. Renborg E, Johannesson K, Havenhand J, Evol Ecol 2014 28 561 572
37. Barnacle Ecology and Adaptation. Foster BA, Barnacle Biology Rotterdam: Balkema, Southward AJ, 1987 [Schram FR (Series Editor): Crustacean Issues]
38. Darwin C, A Monograph on the Sub-Class Cirripedia: The Balanidae (or sessile cirrepedes); the Verrucidae London: The Ray Society 1854
39. Potential for high-latitude marine invasions along western North America. De Rivera CE, Steves BP, Fofonoff PW, Hines AH, Ruiz GM, Divers Distrib 2011 17 1198 1209
40. Balanus improvisus Darwin on the west coast of Sweden. Blom S-E, Zoologiska Bidrag fra˚n Uppsala 1965 37 59 76
41. Holeuryhalinity and its mechanisms in a cirriped crustacean, Balanus improvisus. Fyhn HJ, Comp Biochem Physiol A Physiol 1976 53 19 30
42. Being young in a changing world: how temperature and salinity changes interactively modify the performance of larval stages of the barnacle Amphibalanus improvisus. Nasrolahi A, Pansch C, Lenz M, Wahl M, Mar Biol 2012 159 331 340
43. The reaction of the Black Sea Balanus improvisus (Darwin) to reduced salinities. Turpayeva YP, Simkina RG, T Inst Oceanogr 1961 XLIX 205 223
44. +ATPase from the euryhaline barnacle Balanus improvisus reveals multiple genes and differential expression of alternative splice variants. Lind U, Rosenblad MA, Wrange AL, Sundell KS, Jonsson PR, Andre C, Havenhand J, Blomberg A, PLoS One 2013 8 77069
45. A comparative study of the behaviour of some balanomorph barnacles exposed to fluctuating sea water concentrations. Davenport J, J Mar Biol Ass U K 1976 56 889 907
46. Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: patterns of microfouling and antimicrobial protection. Wahl M, Shahnaz L, Dobretsov S, Saha M, Symanowski F, David K, Lachnit T, Vasel M, Weinberger F, Mar Ecol Progr Ser 2010 411 33 U61
47. Temporal and spatial patterns in recruitment and succession of a temperate marine fouling assemblage: A comparison of static panels and boat hulls during the boating season. Berntsson KM, Jonsson PR, Biofouling 2003 19 187 195
48. Influence of temperature and salinity on larval development of Balanus amphitrite-implications in fouling ecology. Anil AC, Chiba K, Okamoto K, Kurokura H, Mar Ecol Prog Ser 1995 118 159 166
49. Analysis of behavioural rejection of micro-textured surfaces and implications for recruitment by the barnacle Balanus improvisus. Berntsson KM, Jonsson PR, Lejhall M, Gatenholm P, J Exp Mar Biol Ecol 2000 251 59 83
50. Larval development of the barnacle Amphibalanus improvisus responds variably but robustly to near-future ocean acidification. Pansch C, Schlegel P, Havenhand J, ICES J Mar Sci: Journal du Conseil 2013 70 805 811
51. Quinn G, Keough M, Experimental Design and Data Analysis for Biologists Cambridge, UK: Cambridge University Press 2002
52. Standard procedure for the determination of chlorophyll a by spectroscopic methods. Aminot A, Rey F, ICES: Techniques in Marine Environmental Sciences 2002 28 1 15
53. A quantitative theory of organic growth. von Bertalanffy L, Hum Biol 1938 10 181 213
54. The Gompertz curve as a growth equation. Winsor C, Proc Natl Acad Sci U S A 1932 18 1 8
55. Salinity effects on the growth, mortality and shell strength of Balanus amphitrite from the Salton Sea, California. Simpson E, Hurlbert S, Hydrobiologia 1998 381 179 190
56. Growth and reproductive performance in cultured nearshore rockfish (Sebastes spp.). Tsang WN, Chaillé PM, Collins PM, Aquaculture 2007 266 236 245
57. Sigmoidal growth in the brittle star Amphiura filiformis (Echinodermata: Ophiuroidea). Sköld M, Josefson AB, Loo LO, Mar Biol 2001 139 519 526
58. Trajectories and models of individual growth. Karkach AS, Demogr Res 2006 15 348 400
59. Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2. Pansch C, Nasrolahi A, Appelhans YS, Wahl M, Mar Biol 2013 160 2023 2035
60. Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: Variable responses to ocean acidification at local scales? Range P, Chicharo MA, Ben-Hamadou R, Pilo D, Matias D, Joaquim S, Oliveira AP, Chicharo L, J Exp Mar Biol Ecol 2011 396 177 184
61. The evolution of life histories in spatially heterogeneous environments-optimal reaction norms revisited. Kawecki TJ, Stearns SC, Evol Ecol 1993 7 155 174
62. CAP: A FORTRAN Computer Program for Canonical Analysis of Principal Coordinates. Anderson MJ, New Zealand: Department of Statistics, University of Auckland 2004
63. Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Anderson MJ, Willis TJ, Ecology 2003 84 511 525
64. Partialling out the spatial component of ecological variation: questions and propositions in the linear modelling framework. Meot A, Legendre P, Borcard D, Environ Ecol Stat 1998 5 1 27
65. Responses and acclimation to salinity in adults of some balanomorph barnacles. Foster BA, Philos Trans R Soc Lond Ser B-Biol Sci 1970 256 377 400
66. Effects of salinity and adult extract on settlement of the oligohaline barnacle Balanus subalbidus. Dineen JF, Hines AH, Mar Biol 1994 119 423 430
67. Larval settlement of the polyhaline barnacle Balanus eburneus (Gould): cue interactions and comparisons with two estuarine congeners. Dineen JF, Hines AH, J Exp Mar Biol Ecol 1994 179 223 234
68. Temperature and salinity interactively impact early juvenile development: a bottleneck in barnacle ontogeny. Nasrolahi A, Pansch C, Lenz M, Wahl M, Mar Biol 2013 160 1109 1117
69. Early post-settlement mortality of an intertidal barnacle: A critical period for survival. Gosselin LA, Qian PY, Mar Ecol-Progr Ser 1996 135 69 75
70. Effects of competition, predation by Thais lapillus, and other factors on natural populations of barnacle Balanus balanoides. Connell JH, Ecol Monogr 1961 31 61 104
71. Desiccation as a factor in intertidal zonation of barnacles. Foster BA, Mar Biol 1971 8 12 29
72. Juvenile mortality in benthic marine invertebrates. Gosselin LA, Qian PY, Mar Ecol Prog Ser 1997 146 265 282
73. The role of spatial and size refuges in the interaction between juvenile barnacles and grazing limpets. Miller KM, Carefoot TH, J Exp Mar Biol Ecol 1989 134 157 174
74. Effects of reduced salinities on development and bioenergetics of early larval shore crab, Carcinus maenas. Anger K, Spivak E, Luppi T, J Exp Mar Biol Ecol 1998 220 287 304
75. Cumulative effects of low salinity on larval growth and biochemical composition in an estuarine crab, Neohelice granulata. Torres G, Gimenez L, Anger K, Aquat Biol 2008 2 37 45
76. Temperature and salinity effects on calcification rate in Mytilus edulis and its paleoecological implications. Malone PG, Dodd JR, Limnol Oceanogr 1967 12 432 436
77. Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Lively CM, Evolution 1986 40 232 242
78. Reproduction of the intertidal barnacle Balanus glandula along an estuarine gradient. Berger MS, Mar Ecol 2009 30 346 353
79. Reproduction in three species of intertidal barnacles from central California. Hines AH, Biol Bull 1978 154 262 281
80. Egg numbers, metabolic efficiency of egg production and fecundity; Local and regional variations in a number of common cirripedes. Barnes H, Barnes M, J Exp Mar Biol Ecol 1968 2 135 153
81. The tolerance of developing cirripede embryos to salinity and temperature. Crisp DJ, Costlow JD, Oikos 1963 14 22 34
82. Effects of solar radiation on barnacle settlement, early post-settlement mortality and community development in the intertidal zone. Gosselin LA, Jones LA, Mar Ecol Progr Ser 2010 407 149 158
83. Southward AJ, Barnacle Biology Rotterdam: A.A. Balkema 1987
84. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. Dickinson GH, Ivanina AV, Matoo OB, Portner HO, Lannig G, Bock C, Beniash E, Sokolova IM, J Exp Biol 2012 215 29 43
85. The solubility of calcite and aragonite in seawater at various salinities, temperatures and one atmosphere total pressure. Mucci A, Am J Sci 1983 283 780 799
86. The effects of reduced salinity on the shell growth of small Mytilus edulis. Almada-Villela PC, J Mar Biol Assoc UK 1984 64 171 182
87. Genotypic and phenotypic differences between Baltic and North-Sea populations of Mytilus edulis evaluated through reciprocal transplantations. 1. Growth and morphology. Kautsky N, Johannesson K, Tedengren M, Mar Ecol Prog Ser 1990 59 203 210
88. Predator-inducible changes in blue mussels from the predator-free Baltic Sea. Reimer O, Harms-Ringdahl S, Mar Biol 2001 139 959 965
89. Persistence and space occupancy by subtidal blue mussel patches. Reusch TBH, Chapman ARO, Ecol Monogr 1997 67 65 87
90. The Ecological and Evolutionary Importance of Maternal Effects in the Sea. Marshall DJ, Allen RM, Crean AJ, Oceanography and Marine Biology: An Annual Review, Volume 46 Boca Raton: Crc Press-Taylor & Francis Group, Gibson RN, Atkinson RJA, Gordon JDM, 2008 203 250
91. Oceanographic connectivity and environmental correlates of genetic structuring in Atlantic herring in the Baltic Sea. Teacher AGF, Andre C, Jonsson PR, Merila J, Evol Appl 2013 6 549 567
92. From genes to geography-evolutionary perspectives on salinity tolerance in the brackish water barnacle Balanus improvisus. Wrange A-L, PhD thesis University of Gothenburg: Department of Biological and Environmental Sciences 2014
93. Om Balanus improvisus i Östersjön. Luther A, Fauna Flora 1950 45 155 160
94. Reconstructing routes of invasion using genetic data: why, how and so what? Estoup A, Guillemaud T, Mol Ecol 2010 19 4113 4130
95. A general eco-evolutionary framework for understanding bioinvasions. Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P, Trends Ecol Evol 2006 21 130 135
96. How interactions between ecology and evolution influence contemporary invasion dynamics. Lambrinos JG, Ecology 2004 85 2061 2070
97. Recruitment and the local dynamics of open marine populations. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA, Annu Rev Ecol Syst 1996 27 477 500
98. Conceptual issues in local adaptation. Kawecki TJ, Ebert D, Ecol Lett 2004 7 1225 1241
99. The risk of marine bioinvasion caused by global shipping. Seebens H, Gastner MT, Blasius B, Ecol Lett 2013 16 782 790
100. Twelve years of contemporary armor evolution in a threespine stickleback population. Bell MA, Aguirre WE, Buck NJ, Evolution 2004 58 814 824
101. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME, Science 2011 331 1322 1325
102. Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V, Heredity 2007 99 592 600
103. Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides. Schmidt PS, Bertness MD, Rand DM, Proc R Soc Lond Ser B-Biol Sci 2000 267 379 384
104. Evolution of physiological tolerance and performance during freshwater invasions. Lee CE, Remfert JL, Gelembiuk GW, Integr Comp Biol 2003 43 439 449
105. Predicting evolutionary responses to climate change in the sea. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ, Ecol Lett 2013 16 1488 1500
106. Feasting in fresh water: impacts of food concentration on freshwater tolerance and the evolution of food × salinity response during the expansion from saline into fresh water habitats. Lee CE, Moss WE, Olson N, Chau KF, Chang Y-M, Johnson KE, Evol Appl 2013 6 673 689
107. Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Todgham AE, Stillman JH, Integr Comp Biol 2013 53 539 544