Advertisement

Marine Biology

, 163:91 | Cite as

When warming hits harder: survival, cellular stress and thermal limits of Sparus aurata larvae under global change

  • Diana Madeira
  • Pedro M. Costa
  • Catarina Vinagre
  • Mário S. Diniz
Original Paper

Abstract

Understanding physiological and molecular compensation mechanisms that shape thermotolerance is crucial for estimating the effects of ocean warming on fish stocks, especially during early life stages, whose tolerance determines recruitment success and population viability. The aims of this study were to assess the sensitivity of fish larvae toward ocean warming and heat wave events in the commercial species, Sparus aurata, whose habitat is likely to be affected by rising water temperatures. We (1) estimated its critical thermal maximum (CTmax) and relative mortality upon warming, (2) quantified stress biomarkers: heat shock protein 70 kDa, total ubiquitin, antioxidant enzymes (superoxide dismutase, catalase, glutathione-S-transferase), lipid peroxidation and protein carbonylation, and (3) analyzed histopathological changes as a result of thermal stress. Larvae showed increasing levels of lethargy with increasing temperature, attaining a cumulative CTmax value of 30 °C. Relative mortality increased upon warming, reaching 80 % at 30 °C. Oxidative damage was higher at moderate temperatures and decreased at 24 °C probably due to a significant increase in superoxide dismutase’s (SODs) activity. Hsp70 chaperone levels also increased at 26 °C, but unfolding persisted at higher temperatures as shown by the increase in total ubiquitin at 26 and 28 °C, indicating protein damage. Skeletal muscle showed disorganization of muscle fibers from 24 °C onwards. Overall, protein denaturation seems to be the major cause of larval mortality, potentially compromising recruitment’s success from 22 °C onwards, since larvae migrate into nursery grounds by spring and summer (i.e., high temperatures), thus hindering the viability of local fish stocks. These data demonstrate that the biochemical homeostasis of fish can be disturbed within an ecologically realistic thermal range and emphasize the risks of rising global temperatures for larval fishes.

Graphical Abstract

Keywords

Heat Wave Protein Carbonylation Coastal Lagoon Fish Stock Relative Mortality 
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

Acknowledgments

The authors would like to thank Marta Martins, Ana Patrícia and Carolina Madeira for the help given in the maintenance of experimental systems and feeding of the organisms. Authors would like to thank MARESA for providing not only S. aurata larvae but also microalgae, rotifers and Artemia salina nauplii.

Funding

This study had the support of the Portuguese Fundação para a Ciência e a Tecnologia (FCT) (individual grants: senior researcher position to CV, SFRH/BPD/72564/2010 to PMC, SFRH/BD/80613/2011 to DM; Project Grants PTDC/MAR/119068/2010 and PTDC/MAR-EST/2141/2012; strategic Project Grants UID/Multi/04378/2013 and UID/MAR/04292/2013).

Compliance with ethical standards

Conflict of interest

We have no competing interests.

References

  1. Alamdari DH, Kostidou E, Paletas K, Sarigianni M, Konstas AGP, Karapiperidou A, Koliakos G (2005) High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein. Free Radic Biol Med 39:1362–1367CrossRefGoogle Scholar
  2. Alami-Durante H, Rouel M, Kentouri M (2006) New insights into temperature-induced white muscle growth plasticity during Dicentrarchus labrax early life: a developmental and allometric study. Mar Biol 149:1551–1565CrossRefGoogle Scholar
  3. Andrades JA, Becerra J, Fernández-Llebrez P (1996) Skeletal deformities in larval, juvenile and adult stages of cultures gilthead seabream (S. aurata L.). Aquaculture 141:1–11CrossRefGoogle Scholar
  4. Arabaci M, Yilmaz Y, Ceyhun SB et al (2010) A review on population characteristics of gilthead seabream (S. aurata). J Anim Vet Adv 9:976–981CrossRefGoogle Scholar
  5. Bartolini F, Barausse A, Pörtner H-O, Giomi F (2013) Climate change reduces offspring fitness in littoral spawners: a study integrating organismic response and long-term time-series. Glob Chang Biol 19:373–386CrossRefGoogle Scholar
  6. Basu N, Todgham AE, Ackerman PA et al (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183CrossRefGoogle Scholar
  7. Blaxter JHS (1992) The effect of temperature on larval fishes. Neth J Zool 42:336–357CrossRefGoogle Scholar
  8. Bodinier C, Sucré E, Lecurieux-Belfond L, Blondeau-Bidet E, Charmantier G (2010) Ontogeny of osmoregulation and salinity tolerance in the gilthead sea bream S. aurata. Comp Biochem Physiol A 157:220–228CrossRefGoogle Scholar
  9. Cabral HN, Costa MJ, Salgado JP (2001) Does the Tagus estuary fish community reflect environmental changes? Clim Res 18:119–126CrossRefGoogle Scholar
  10. Chícharo L, Teodósio MA (1991) Contribuição para o estudo do ictioplâncton do estuário do Guadiana. Rev Biol Univ Aveiro 4:277–286Google Scholar
  11. Damianides P, Chintiroglou CC (2000) Structure and functions of polychaetofauna living in Mytilus galloprovincialis assemblages in Thermaikos Gulf (north Aegean sea). Oceanol Acta 23:323–337CrossRefGoogle Scholar
  12. Dimitriou E, Katselis G, Moutopoulos DK, Akovitiotis C, Koutsikopoulos C (2007) Possible influence of reared gilthead sea bream (S. aurata, L.) on wild stocks in the area of the Messolonghi lagoon (Ionian Sea, Greece). Aquac Res 38:398–408CrossRefGoogle Scholar
  13. Dionísio G, Campos C, Valente LMP, Conceição LEC, Cancela ML, Gavaia PJ (2012) Effect of egg incubation temperature on the occurrence of skeletal deformities in Solea senegalensis. J Appl Ichthyol 28:471–476CrossRefGoogle Scholar
  14. Donelson JM, Munday PL, McCormick MI, Pitcher CR (2011) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32CrossRefGoogle Scholar
  15. Dunphy BJ, Ragg NLC, Collings MG (2013) Latitudinal comparison of thermotolerance and Hsp70 production in F2 larvae of the greenshell mussel (Perna canaliculus). J Exp Biol 216:1202–1209CrossRefGoogle Scholar
  16. FAO (2015) Cultured Aquatic Species Information Programme. Sparus aurata. In: Colloca F, Cerasi S (eds) Fisheries and Aquaculture Department, Rome. http://www.fao.org/fishery/culturedspecies/Sparus_aurata/en. Accessed 6 Apr 2015
  17. Faria AM, Chícharo MA, Gonçalves EJ (2011) Effects of starvation on swimming performance and body condition of pre-settlement S. aurata larvae. Aquat Biol 12:281–289CrossRefGoogle Scholar
  18. Feidantsis K, Pörtner H-O, Lazou A, Kostoglou B, Michaelidis B (2009) Metabolic and molecular stress responses of the gilthead seabream S. aurata during long-term exposure to increasing temperatures. Mar Biol 156:797–809CrossRefGoogle Scholar
  19. Feidantsis K, Antonopoulou E, Lazou A, Pörtner H-O, Michaelidis B (2013) Seasonal variations of cellular stress response of the gilthead sea bream (S. aurata). J Comp Physiol B 183:625–639CrossRefGoogle Scholar
  20. Fischer EM, Schär C (2010) Consistent geographical patterns of changes in high-impact European heatwaves. Nat Geosci 3(6):398–403CrossRefGoogle Scholar
  21. Fisher R, Wilson SK (2004) Maximum sustainable swimming speeds of late-stage larvae of nine species of reef fishes. J Exp Mar Biol Ecol 312:171–186CrossRefGoogle Scholar
  22. Froese R, Pauly D (eds) (2006) Fish base. World Wide Web electronic publication. http://www.fishbase.org
  23. Fulda S, Gorman AM, Hori O, Samali A (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010:23. doi: 10.1155/2010/214074
  24. Garrabou J, Coma R, Bensoussan N et al (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103CrossRefGoogle Scholar
  25. Georgakopoulou E, Katharios P, Divanach P, Koumoundouros G (2010) Effect of temperature on the development of skeletal deformities in Gilthead seabream (S. aurata Linnaeus, 1758). Aquaculture 308(1–2):13–19CrossRefGoogle Scholar
  26. Godbold JA, Calosi P (2013) Ocean acidification and climate change: advances in ecology and evolution. Philos Trans R Soc B 368(1627):20120448CrossRefGoogle Scholar
  27. Green BS, Fisher R (2004) Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. J Exp Mar Biol Ecol 299:115–132CrossRefGoogle Scholar
  28. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturicacid formation. J Biol Chem 246:7130–7139Google Scholar
  29. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci 103(39):14288–14293CrossRefGoogle Scholar
  30. Houde ED (1989) Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495Google Scholar
  31. Houde ED (2008) Emerging from Hjort’s shadow. J Northwest Atl Fish Sci 41:53–70CrossRefGoogle Scholar
  32. Ibarra-Zatarain Z, Duncan N (2015) Mating behaviour and gamete release in gilthead seabream (S. aurata, Linnaeus 1758) held in captivity. Span J Agric Res 13(1):e04-001CrossRefGoogle Scholar
  33. IPCC (2001) Third assessment report of the working group I. In: Houghton JT et al (eds) The science of climate change. Cambridge University Press, CambridgeGoogle Scholar
  34. IPCC (2007) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, chap 3. Observations: surface and atmospheric climate change (section 3.8 Changes in extreme events). In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
  35. IPCC (2013) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
  36. IPCC (2014) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. In: Pachauri RK, Meyer LA (eds) Climate change 2014: synthesis report. IPCC, GenevaGoogle Scholar
  37. Johansson LH, Borg LAH (1988) A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem 174:331–336CrossRefGoogle Scholar
  38. José R (2012) Sparus aurata larvae production in mesocosm: evaluation of abiotic and biotic parameters. Dissertation, University of Porto, PortugalGoogle Scholar
  39. Kissil GW, Lupatsch I, Elizur A, Zohar Y (2001) Long photoperiod delayed spawning and increased somatic growth in gilthead seabream (S. aurata). Aquaculture 200:363–379CrossRefGoogle Scholar
  40. Koumoundouros G, Ashton C, Xenikoudakis G, Giopanou I, Georgakopoulou E, Stickland N (2009) Ontogenetic differentiation of swimming performance in Gilthead seabream (S. aurata, Linnaeus 1758) during metamorphosis. J Exp Mar Biol Ecol 370:75–81CrossRefGoogle Scholar
  41. Kristiansen T, Stock C, Drinkwater KF, Curchitser EN (2014) Mechanistic insights into the effects of climate change on larval cod. Glob Chang Biol 20:1559–1584CrossRefGoogle Scholar
  42. Landsman SJ, Gingerich AJ, Philipp DP, Suski CD (2011) The effects of temperature change on the hatching success and larval survival of largemouth bass Micropterus salmoides and smallmouth bass Micropterus dolomieu. J Fish Biol 78:1200–1212CrossRefGoogle Scholar
  43. Leis J, McCormick M (2002) The biology, behaviour, and ecology of the pelagic, larval stage of coral reef fishes. In: Sale P (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 171–200CrossRefGoogle Scholar
  44. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278CrossRefGoogle Scholar
  45. Linares-Casenave J, Werner I, Van Eenennaam JP, Doroshov SI (2013) Temperature stress induces notochord abnormalities and heat shock proteins expression in larval green sturgeon (Acipenser medirostris Ayres 1854). J Appl Ichthyol 29:958–967CrossRefGoogle Scholar
  46. Logan CA, Somero GN (2011) Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol Regul Integr Comp Physiol 300:R1373–R1383CrossRefGoogle Scholar
  47. Madeira D, Narciso L, Cabral HN, Vinagre C (2012a) Thermal tolerance and potential impacts of climate change on coastal and estuarine organisms. J Sea Res 70:32–41CrossRefGoogle Scholar
  48. Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2012b) HSP70 production patterns in coastal and estuarine organisms facing increasing temperatures. J Sea Res 73:137–147CrossRefGoogle Scholar
  49. Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol A 166:237–243CrossRefGoogle Scholar
  50. Madeira D, Vinagre C, Costa PM, Diniz MS (2014) Histopathological alterations, physiological limits, and molecular changes of juvenile S. aurata in response to thermal stress. Mar Ecol Prog Ser 505:253–266CrossRefGoogle Scholar
  51. McLeod IM, Rummer JL, Clark TD, Jones GP, McCormick MI, Wenger AS, Munday PL (2013) Climate change and the performance of larval coral reef fishes: the interaction between temperature and food availability. Conserv Physiol 1(1):cot024CrossRefGoogle Scholar
  52. Meyer E, Aglyamova GV, Matz MV (2011) Profiling gene expression responses of coral larvae (Acropora milepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol 20(17):3599–3616Google Scholar
  53. Miranda PMA, Coelho FES, Tomé AR, Valente MA, Carvalho A, Pires C, Pires HO, Pires VC, Ramalho C (2002) 20th century portuguese climate and climate scenarios, in climate change in Portugal. In: Santos FD, Forbes K, Moita R (eds) Scenarios, impacts and adaptation measures—SIAM project. Gradiva, Lisboa, pp 23–83Google Scholar
  54. Mora C, Maya MF (2006) Effect of the rate of temperature increase of the dynamic method on the heat tolerance of fishes. J Therm Biol 31:337–341CrossRefGoogle Scholar
  55. Mora C, Ospina AF (2001) Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific). Mar Biol 139:765–769CrossRefGoogle Scholar
  56. Moretti A, Fernandez-Criado MP, Cittolin G, Guidastri R (1999) Manual on hatchery production of seabass and gilthead seabream, vol 1. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  57. Munday PL (2014) Transgenerational acclimation of fishes to climate change and ocean acidification. F1000 Prime Rep 6:99CrossRefGoogle Scholar
  58. Mylonas C, Zohar Y, Pankhurst N, Kagawa H (2011) Reproduction and broodstock management. In: Pavlidis MA, Mylonas CC (eds) Sparidae: biology and aquaculture of gilthead seabream and others species. Wiley, Oxford, pp 95–121CrossRefGoogle Scholar
  59. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Natl Acad Sci USA 104:1266–1271CrossRefGoogle Scholar
  60. Pearce AF, Feng M (2013) The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011. J Mar Syst 111–112:139–156CrossRefGoogle Scholar
  61. Peck MA, Huebert KB, Llopiz JK (2012) Intrinsic and extrinsic factors driving match–mismatch dynamics during the early life history of marine fishes. Adv Ecol Res 47:178–278Google Scholar
  62. Pepin P (1991) Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Can J Fish Aquat Sci 48(3):503–518CrossRefGoogle Scholar
  63. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefGoogle Scholar
  64. Pimentel M, Faleiro F, Dionísio G, Repolho T, Pousão-Ferreira P, Machado J, Rosa R (2014) Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean. J Exp Biol 217:2062–2070CrossRefGoogle Scholar
  65. Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A 131:41–50CrossRefGoogle Scholar
  66. Polo A, Yafera M, Pascual E (1991) Effects of temperature on egg and larval development of Spartus aurata L. Aquaculture 92:367–375CrossRefGoogle Scholar
  67. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692CrossRefGoogle Scholar
  68. Rhee JS, Kim BM, Kim RO, Seo JS, Kim IC, Lee YM, Lee JS (2013) Co-expression of antioxidant enzymes with expression of p53, DNA repair, and heat shock protein genes in the gamma ray-irradiated hermaphroditic fish Kryptolebias marmoratus larvae. Aquat Toxicol 140C–141C:58–67CrossRefGoogle Scholar
  69. Rosa R, Baptista M, Lopes VM, Pegado MR, Paula R, Trübenbach K, Leal MC, Calado R, Repolho T (2014) Early-life exposure to climate change impairs tropical shark survival. Proc R Soc B 281:1793CrossRefGoogle Scholar
  70. Rose TH, Smale DA, Botting G (2012) The 2011 marine heat wave in Cockburn Sound, southwest Australia. Ocean Sci 8:545–550CrossRefGoogle Scholar
  71. Salinas S, Munch SB (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163CrossRefGoogle Scholar
  72. Santos FD, Miranda P (eds) (2006) Climate change in Portugal: scenarios, impacts and adaptation measures—SIAM II project. Gradiva, LisboaGoogle Scholar
  73. Shama LNS, Strobel A, Mark FC, Wegner KM (2014) Transgenerational plasticity in marine sticklebacks: maternal effects mediate impacts of a warming ocean. Funct Ecol 28(6):1482–1493CrossRefGoogle Scholar
  74. Skjærven KH, Penglase S, Olsvik PA, Hamre K (2013) Redox regulation in Atlantic cod (Gadus morhua) embryos developing under normal and heat-stressed conditions. Free Radic Biol Med 57:29–38CrossRefGoogle Scholar
  75. Sola L, Moretti A, Crosetti D, Karaiskou N, Magoulas A, Rossi AR, Rye M, Triantafyllidis A, Tsigenopoulos CS (2007) Genetic effects of domestication, culture and breeding of fish and shellfish, and their impacts on wild populations: Gilthead seabream S. aurata. In: Svåsand T, Crosetti D, García-Vázquez E, Verspoor E (eds) Genetic impact of aquaculture activities on native populations, a European network (EU contract no. RICA-CT-2005-022802). Final scientific report, p 176. http://genimpact.imr.no/
  76. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920CrossRefGoogle Scholar
  77. Somero GN, Hofmann GE (1997) Temperature thresholds for protein adaptation: when does temperature change start to ‘hurt’? In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 1–24CrossRefGoogle Scholar
  78. Storch D, Fernández M, Navarrete SA, Pörtner HO (2001) Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus. Mar Ecol Prog Ser 429:157–167CrossRefGoogle Scholar
  79. Suau P, Lopez J (1976) Contribution to knowledge of biology of Gilt-Head (S. aurata L.). Investig Pesq 40:169–199Google Scholar
  80. Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500Google Scholar
  81. Sung YY, Pineda C, MacRae TH, Sorgeloos P, Bossier P (2008) Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii. Cell Stress Chaperones 13(1):59–66CrossRefGoogle Scholar
  82. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278CrossRefGoogle Scholar
  83. Valente LMP, Moutou KA, Conceição L, Engrola S, Fernandes JMO, Johnston IA (2013) What determines growth potential and juvenile quality of farmed fish species? Rev Aquac 5:1–26CrossRefGoogle Scholar
  84. Verdiell-Cubedo D, Oliva-Paterna FJ, Ruiz-Navarro A, Torralva M (2013) Assessing the nursery role for marine fish species in a hypersaline coastal lagoon (Mar Menor, Mediterranean Sea). Mar Biol Res 9:739–748CrossRefGoogle Scholar
  85. Vinagre C, Santos FD, Cabral HN, Costa MJ (2009) Impact of climate and hydrology on juvenile fish recruitment towards estuarine nursery grounds in the context of climate change. Estuar Coast Shelf Sci 85:479–486CrossRefGoogle Scholar
  86. Vinagre C, Narciso L, Pimentel M, Cabral HN, Costa MJ, Rosa R (2013) Contrasting impacts of climate change across seasons: effects on flatfish cohort. Reg Environ Chang 13:853–859CrossRefGoogle Scholar
  87. Vinagre C, Narciso L, Cabral HN, Costa MJ, Rosa R (2014) Thermal sensitivity of native and invasive seabreams. Mar Ecol 35:292–297CrossRefGoogle Scholar
  88. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  89. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Chang 3:78–82CrossRefGoogle Scholar
  90. Werner I, Linares-Casenave J, Van Eenennaam JP, Doroshov SI (2007) The effect of temperature stress on development and heat-shock protein expression in larval green sturgeon (Acipenser medirostris). Environ Biol Fish 79:191–200CrossRefGoogle Scholar
  91. Williams BR, van Heerwaarden B, Dowling DK, Sgrò CM (2012) A multivariate test of evolutionary constraints for thermal tolerance in Drosophila melanogaster. J Evol Biol 25:1415–1426CrossRefGoogle Scholar
  92. Woodin SA, Hilbish TJ, Helmuth B, Jones SJ, Wethey DS (2013) Climate change, species distribution models, and physiological performance metrics: predicting when biogeographic models are likely to fail. Ecol Evol 3(10):3334–3346Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.UCIBIO-REQUIMTE, Faculdade de Ciências e TecnologiaUniversidade Nova de LisboaCaparicaPortugal
  2. 2.Unit of Molecular Toxicology, Institute of Environmental Medicine (IMM)Karolinska InstitutetStockholmSweden
  3. 3.Marine and Environmental Sciences Centre (MARE), Faculdade de CiênciasUniversidade de LisboaLisbonPortugal

Personalised recommendations