Present and future invasion perspectives of an alien shrimp in South Atlantic coastal waters: an experimental assessment of functional biomarkers and thermal tolerance

  • Carolina MadeiraEmail author
  • Vanessa Mendonça
  • Miguel C. Leal
  • Mário S. Diniz
  • Henrique N. Cabral
  • Augusto A. V. Flores
  • Catarina Vinagre
Original Paper


Climate change, particularly ocean warming, is thought to benefit the spread of invasive species due to their increased tolerance to temperature fluctuations as compared to native species. The physiological tolerance of invasive species as a potential mechanism driving invasion success is therefore a subject that merits further study. Specifically, we need to adequately evaluate the potential of species invasions under changing environmental conditions, so that adequate preventive measures can be taken to minimize any impacts on coastal ecosystems. Here, we experimentally evaluated the physiological responses of a recent invader in the Southern Atlantic, the shrimp Lysmata lipkei, under a warming ocean scenario. Adult shrimps were collected from rocky shores in southeastern Brazil and subjected to experimental trials under a control and a + 3 °C scenario. Molecular biomarkers (in gills and muscle), upper thermal limits, acclimation response ratios, thermal safety margins, mortality rates, estimates of body condition and energy reserves were measured over 1 month. Results suggest that higher temperatures elicit physiological adjustments at the molecular level, underpinning a high thermal tolerance. In addition, results indicated substantial acclimation capacity, with no evidence of decreased performance under an ocean-warming scenario. Thermal safety margins were low for shrimp from intertidal rock pools but high for shrimp from subtidal habitats. We conclude that the thermal tolerance of this shrimp species may favor its ongoing invasion along the Southwestern Atlantic Ocean, mainly in subtidal habitats, both under present and future thermal conditions.

Graphical abstract


Tropical shrimp Invasive species Warming oceans Rocky reefs Thermal biology Stress physiology 



The present research was financially supported by the Portuguese Foundation for Science and Technology (FCT) through the WarmingWebs Project (PTDC/MAR-EST/2141/2012), the “Investigador FCT” position granted to C.V. and the strategic Projects UID/MAR/04292/2013 granted to MARE and UID/Multi/04378/2013 granted to UCIBIO. Authors C.M. and V.M. acknowledge Ph.D. Grants (SFRH/BD/92975/2013 and SFRH/BD/109618/2015, respectively), and M.C.L. acknowledges a post-doc Grant (SFRH/BPD/115298/2016), all Granted by FCT. The funding institution had no influence in the study design, collection and analysis of datasets or in the decision to publish the work. Authors would like to thank everyone who helped during field work and experimental trials, and to a Megan Walters for proofreading.

Compliance with ethical standards

Research involving animals

The authors declare that animal experiments followed legal guidelines for laboratory animal science and were authorized by competent authorities, as stated in the materials and methods subsection “Ethical guidelines”.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2019_1921_MOESM1_ESM.pdf (631 kb)
Supplementary material 1 (PDF 630 kb)


  1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. Garland Science, New YorkGoogle Scholar
  2. Allan EL, Froneman PW, Hodgson AN (2006) Effects of temperature and salinity on the standard metabolic rate (SMR) of the caridean shrimp Palaemon peringueyi. J Exp Mar Bio Ecol 337:103–108. CrossRefGoogle Scholar
  3. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509. CrossRefGoogle Scholar
  4. Angilletta MJ, Bennett AF, Guderley H et al (2006) Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79:282–294. CrossRefGoogle Scholar
  5. Assis CRD, Linhares AG, Oliveira VM et al (2012) Comparative effect of pesticides on brain acetylcholinesterase in tropical fish. Sci Total Environ 441:141–150. CrossRefGoogle Scholar
  6. Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. Google Scholar
  7. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. CrossRefGoogle Scholar
  9. Buckley BA, Place SP, Hofmann GE (2004) Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii. J Exp Biol 207:3649–3656. CrossRefGoogle Scholar
  10. Burgiel SW, Muir AA (2010) Invasive species, climate change and ecosystem-based adaptation: addressing multiple drivers of global change. Global Invasive Species Programme (GISP), Washington, DC, US and Nairobi, KenyaGoogle Scholar
  11. Clark MS, Fraser KPP, Burns G, Peck LS (2008) The HSP70 heat shock response in the Antarctic fish Harpagifer antarcticus. Polar Biol 31:171–180. CrossRefGoogle Scholar
  12. Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782. CrossRefGoogle Scholar
  13. Claussen D (1977) Thermal acclimation in ambystomatid salamanders. Comp Biochem Physiol Mol Integr Physiol 58:333–340CrossRefGoogle Scholar
  14. Coles SL, Brown BE (2003) Coral bleaching—capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223. CrossRefGoogle Scholar
  15. Cortes PA, Puschel H, Acuña P et al (2016) Thermal ecological physiology of native and invasive frog species: do invaders perform better? Conserv Physiol 4:cow056. CrossRefGoogle Scholar
  16. Cuculescu M, Hyde D, Bowler K (1998) Thermal tolerance of two species of marine crab, Cancer pagurus and Carcinus maenas. J Therm Biol 23:107–110CrossRefGoogle Scholar
  17. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. CrossRefGoogle Scholar
  18. Farcy É, Voiseux C, Lebel JM, Fiévet B (2009) Transcriptional expression levels of cell stress marker genes in the pacific oyster Crassostrea gigas exposed to acute thermal stress. Cell Stress Chaperones 14:371–380. CrossRefGoogle Scholar
  19. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. CrossRefGoogle Scholar
  20. Festing MFW, Altman DG (2002) Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J 43:244–258. CrossRefGoogle Scholar
  21. González-Ortegón E, Pascual E, Drake P (2013) Respiratory responses to salinity, temperature and hypoxia of six caridean shrimps from different aquatic habitats. J Exp Mar Bio Ecol 445:108–115. CrossRefGoogle Scholar
  22. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S transferases. The first enzymatic step in mercapturic acid formation. Biol Chem 249:7130–7139Google Scholar
  23. Halpin PM, Sorte CJ, Hofmann GE, Menge BA (2002) Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Integr Comp Biol 42:815–824. CrossRefGoogle Scholar
  24. Hau J, Schapiro SJ (2010) Handbook of laboratory animal science: essential principles and practices, vol I, 3rd edn. CRC Press, Boca RatonGoogle Scholar
  25. Hillyer KE, Dias DA, Lutz A et al (2017) Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs 36:105–118. CrossRefGoogle Scholar
  26. Hoefnagel KN, Verberk WCEP (2016) Long-term and acute effects of temperature and oxygen on metabolism, food intake, growth and heat tolerance in a freshwater gastropod. J Therm Biol 68:1–12. Google Scholar
  27. Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255. CrossRefGoogle Scholar
  28. Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518Google Scholar
  29. Imbs AB, Yakovleva IM (2012) Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 31:41–53. CrossRefGoogle Scholar
  30. IPCC (2013) Atlas of Global and Regional Climate Projections. In: Climate change 2013: the physical science basis. contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change Annexe I, pp 1311–1394.
  31. Johansson LH, Borg LA (1988) A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem 174:331–336. CrossRefGoogle Scholar
  32. Kaspari M, Clay NA, Lucas J et al (2015) Thermal adaptation generates a diversity of thermal limits in a rainforest ant community. Glob Chang Biol 21:1092–1102. CrossRefGoogle Scholar
  33. Kelley AL (2014) The role thermal physiology plays in species invasion. Conserv Physiol 2:1–14. CrossRefGoogle Scholar
  34. Klose MK, Robertson RM (2004) Stress-induced thermoprotection of neuromuscular transmission. Integr Comp Biol 44:14–20. CrossRefGoogle Scholar
  35. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204. CrossRefGoogle Scholar
  36. Kühnhold H, Kamyab E, Novais S et al (2016) Thermal stress effects on energy resource allocation and oxygen consumption rate in the juvenile sea cucumber, Holothuria scabra (Jaeger, 1833). Aquaculture 467:1–9. Google Scholar
  37. Lejeusne C, Latchere O, Petit N et al (2014) Do invaders always perform better? Comparing the response of native and invasive shrimps to temperature and salinity gradients in south-west Spain. Estuar Coast Shelf Sci 136:102–111. CrossRefGoogle Scholar
  38. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. CrossRefGoogle Scholar
  39. Loarie SR, Duffy PB, Hamilton H et al (2009) The velocity of climate change. Nature 462:1052–1055. CrossRefGoogle Scholar
  40. 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–R1383. CrossRefGoogle Scholar
  41. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. CrossRefGoogle Scholar
  42. Madeira D, Narciso L, Cabral HN et al (2012a) HSP70 production patterns in coastal and estuarine organisms facing increasing temperatures. J Sea Res 73:137–147. CrossRefGoogle Scholar
  43. Madeira D, Narciso L, Cabral HN, Vinagre C (2012b) Thermal tolerance and potential impacts of climate change on coastal and estuarine organisms. J Sea Res 70:32–41. CrossRefGoogle Scholar
  44. Madeira D, Narciso L, Cabral HN et al (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol Part A Mol Integr Physiol 166:237–243. CrossRefGoogle Scholar
  45. Madeira D, Vinagre C, Costa PM, Diniz MS (2014) Histopathological alterations, physiological limits, and molecular changes of juvenile Sparus aurata in response to thermal stress. Mar Ecol Prog Ser 505:253–266. CrossRefGoogle Scholar
  46. Madeira C, Madeira D, Vinagre C, Diniz M (2015a) Octocorals in a changing environment: seasonal response of stress biomarkers in natural populations of Veretillum cynomorium. J Sea Res 103:120–128CrossRefGoogle Scholar
  47. Madeira D, Mendonça V, Dias M et al (2015b) Physiological, cellular and biochemical thermal stress response of intertidal shrimps with different vertical distributions: Palaemon elegans and Palaemon serratus. Comp Biochem Physiol Part A Mol Integr Physiol 183:107–115. CrossRefGoogle Scholar
  48. Madeira C, Madeira D, Diniz MS et al (2016) Thermal acclimation in clownfish: An integrated biomarker response and multi-tissue experimental approach. Ecol Indic 5:4. Google Scholar
  49. Madeira C, Madeira D, Diniz MS et al (2017) Comparing biomarker responses during thermal acclimation: a lethal vs non-lethal approach in a tropical reef clownfish. Comp Biochem Physiol Part A Mol Integr Physiol 204:104–112. CrossRefGoogle Scholar
  50. Madeira C, Leal MC, Diniz MS et al (2018a) Thermal stress and energy metabolism in two circumtropical decapod crustaceans: Responses to acute temperature events. Mar Environ Res. Google Scholar
  51. Madeira C, Mendonça V, Flores AAV et al (2018b) High thermal tolerance does not protect from chronic warming—a multiple end-point approach using a tropical gastropod. Ecol Indic, Stramonita haemastoma. CrossRefGoogle Scholar
  52. Magozzi S, Calosi P (2015) Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Glob Chang Biol 21:181–194. CrossRefGoogle Scholar
  53. Marengo JA (2007) Mudanças Climáticas Globais e seus Efeitos sobre a Biodiversidade: caracterização do Clima Atual e Definição das Alterações Climáticas para o Território Brasileiro ao Longo do Século XXI. Série Biodiversidade 26:212. Google Scholar
  54. McMahon RF (2002) Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Can J Fish Aquat Sci 59:1235–1244. CrossRefGoogle Scholar
  55. Mendonça V, Madeira C, Dias M et al (2018) What’s in a tide pool? Just as much food web network complexity as in large open ecosystems. PLoS ONE. Google Scholar
  56. Niki E (2012) Do antioxidants impair signaling by reactive oxygen species and lipid oxidation products? FEBS Lett 586:3767–3770. CrossRefGoogle Scholar
  57. Ober GT, Thornber C, Grear J, Kolbe JJ (2016) Ecological differences influence the thermal sensitivity of swimming performance in two co-occurring mysid shrimp species with climate change implications. J Therm Biol 64:26–34. CrossRefGoogle Scholar
  58. Okuno J, Fiedler C (2010) Lysmata lipkei: a new species of Peppermint Shrimp (Decapoda, Hippolytidae) from warm temperate and subtropical waters of Japan. In: Fransen C, de Grave S, Ng P (eds) Studies of malacostraca: Lipke Bijdeley Holthuis Memorial Volume—Crustaceana Monographs. Koninklijke Brill, Leiden, pp 597–610Google Scholar
  59. Pachelle PPG, Anker A, Mendes CB, Bezerra LEA (2016) Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa 4131:1–63. CrossRefGoogle Scholar
  60. Pannunzio TM, Storey KB (1998) Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. J Exp Mar Bio Ecol 221:277–292. CrossRefGoogle Scholar
  61. Payne NL, Smith JA, van der Meulen DE et al (2016) Temperature dependence of fish performance in the wild: Links with species biogeography and physiological thermal tolerance. Funct Ecol. Google Scholar
  62. PBMC, 2014: Base científica das mudanças climáticas. Contribuição do Grupo de Trabalho 1 do Painel Brasileiro de Mudanças Climáticas ao Primeiro Relatório da Avaliação Nacional sobre Mudanças Climáticas [Ambrizzi, T., Araujo, M. (eds.)]. COPPE. Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrasilGoogle Scholar
  63. Pérez-Casanova JC, Rise ML, Dixon B et al (2008) The immune and stress responses of Atlantic cod to long-term increases in water temperature. Fish Shellfish Immunol 24:600–609. CrossRefGoogle Scholar
  64. Pörtner HO, Farrell A (2008) Physiology and climate change. Science 322:690–692. CrossRefGoogle Scholar
  65. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97. CrossRefGoogle Scholar
  66. Qian Z, Liu X, Wang L et al (2012) Gene expression profiles of four heat shock proteins in response to different acute stresses in shrimp, Litopenaeus vannamei. Comp Biochem Physiol C Toxicol Pharmacol 156:211–220. CrossRefGoogle Scholar
  67. Rahlff J, Peters J, Moyano M et al (2017) Short-term molecular and physiological responses to heat stress in neritic copepods Acartia tonsa and Eurytemora affinis. Comp Biochem Physiol Part A Mol Integr Physiol 203:348–358. CrossRefGoogle Scholar
  68. Ravaux J, Léger N, Rabet N et al (2016) Plasticity and acquisition of the thermal tolerance (upper thermal limit and heat shock response) in the intertidal species Palaemon elegans. J Exp Mar Bio Ecol 484:39–45. CrossRefGoogle Scholar
  69. Reiser S, Herrmann JP, Temming A (2014) Thermal preference of the common brown shrimp (Crangon crangon, L.) determined by the acute and gravitational method. J Exp Mar Bio Ecol 461:250–256. CrossRefGoogle Scholar
  70. Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bull Fish Res Board Can 191:1–382Google Scholar
  71. Rodríguez-Fuentes G, Murúa-Castillo M, Díaz F et al (2017) Ecophysiological biomarkers defining the thermal biology of the Caribbean lobster Panulirus argus. Ecol Indic 78:192–204. CrossRefGoogle Scholar
  72. Rushworth KJW, Smith SDA, Cowden KL, Purcell SW (2011) Optimal temperature for growth and condition of an endemic subtropical anemonefish. Aquaculture 318:479–482. CrossRefGoogle Scholar
  73. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702. CrossRefGoogle Scholar
  74. Shabtay A, Arad Z (2005) Ectothermy and endothermy: evolutionary perspectives of thermoprotection by HSPs. J Exp Biol 208:2773–2781. CrossRefGoogle Scholar
  75. Singh A, Jaiswal SK, Sharma B (2013) Effect of low temperature stress on acetylcholinesterase activity and its kinetics in 5th instar larvae of Philosamia ricini. J Biochem Res 1:17–25Google Scholar
  76. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits and costs of living. Integr Comp Biol 42:780–789. CrossRefGoogle Scholar
  77. Sorte CJB, Ibáñez I, Blumenthal DM et al (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270. CrossRefGoogle Scholar
  78. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  79. Stillman JH (2004) A comparative analysis of plasticity of thermal limits in porcelain crabs across latitudinal and intertidal zone clines. Int Congr Ser 1275:267–274. CrossRefGoogle 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. Tang C-H, Leu M-Y, Shao K et al (2014) Short-term effects of thermal stress on the responses of branchial protein quality control and osmoregulation in a reef-associated fish, Chromis viridis. Zool Stud 53:21. CrossRefGoogle Scholar
  82. Tavares-Sánchez OL, Gómez-Anduro GA, Felipe-Ortega X et al (2004) Catalase from the white shrimp Penaeus (Litopenaeus) vannamei: molecular cloning and protein detection. Comp Biochem Physiol B Biochem Mol Biol 138:331–337. CrossRefGoogle Scholar
  83. Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979. CrossRefGoogle Scholar
  84. Tomanek L, Somero GN (2002) Interspecific- and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. J Exp Biol 205:677–685Google Scholar
  85. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278. CrossRefGoogle Scholar
  86. Valenzuela IMP, Akaaboune M (2007) Acetylcholinesterase mobility and stability at the neuromuscular junction of living mice. Mol Biol Cell 18:2904–2911. CrossRefGoogle Scholar
  87. Varela R, Lima FP, Seabra R et al (2018) Coastal warming and wind-driven upwelling: a global analysis. Sci Total Environ 639:1501–1511. CrossRefGoogle Scholar
  88. Verberk WCEP, Overgaard J, Ern R et al (2016) Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comp Biochem Physiol Part A Mol Integr Physiol 192:64–78. CrossRefGoogle Scholar
  89. Verlecar XN, Jena KB, Chainy GBN (2008) Seasonal variation of oxidative biomarkers in gills and digestive gland of green-lipped mussel Perna viridis from Arabian Sea. Estuar Coast Shelf Sci 76:745–752. CrossRefGoogle Scholar
  90. Viant MR, Werner I, Rosenblum ES et al (2003) Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol Biochem 29:159–171. CrossRefGoogle Scholar
  91. Vinagre C, Madeira D, Narciso L et al (2012) Impact of climate change on coastal versus estuarine nursery areas: cellular and whole-animal indicators in juvenile seabass Dicentrarchus labrax. Mar Ecol Prog Ser 464:237–243. CrossRefGoogle Scholar
  92. Vinagre C, Dias M, Roma J et al (2013) Critical thermal maxima of common rocky intertidal fish and shrimps—a preliminary assessment. J Sea Res 81:10–12. CrossRefGoogle Scholar
  93. Vinagre C, Madeira D, Mendonça V et al (2014) Effect of temperature in multiple biomarkers of oxidative stress in coastal shrimp. J Therm Biol 41:38–42. CrossRefGoogle Scholar
  94. Vinagre C, Leal I, Mendonça V, Flores AAV (2015) Effect of warming rate on the critical thermal maxima of crabs, shrimp and fish. J Therm Biol 47:19–25. CrossRefGoogle Scholar
  95. Vinagre C, Leal I, Mendonça V et al (2016) Vulnerability to climate warming and acclimation capacity of tropical and temperate coastal organisms. Ecol Indic 62:317–327. CrossRefGoogle Scholar
  96. Vollenweider R (1985) Elemental and biochemical composition of plankton biomass: some comments and explorations. Arch fur Hydrobiol 105:11–29Google Scholar
  97. Whitehead A, Crawford DL (2005) Variation in tissue-specific gene expression among natural populations. Genome Biol 6:R13. CrossRefGoogle Scholar
  98. Whitley D, Goldberg SP, Jordan WD (1999) Heat shock proteins: a review of the molecular chaperones. J Vasc Surg 29:748–751. CrossRefGoogle Scholar
  99. Yamashita M, Yabu T, Ojima N (2010) Stress Protein HSP70 in Fish. Aqua BioSci Monogr 3:111–141. CrossRefGoogle Scholar
  100. Ye L, Yang S-Y, Zhu X-M et al (2011) Effects of temperature on survival, development, growth and feeding of larvae of Yellowtail clownfish Amphiprion clarkii (Pisces: perciformes). Acta Ecol Sin 31:241–245. CrossRefGoogle Scholar
  101. Yuan X, Yang H, Wang L et al (2009) Bioenergetic responses of sub-adult sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea) to temperature with special discussion regarding its southernmost distribution limit in China. J Therm Biol 34:315–319. CrossRefGoogle Scholar
  102. Yuan X, Yang H, Meng L et al (2013) Impacts of temperature on the scavenging efficiency by the deposit-feeding holothurian Apostichopus japonicus on a simulated organic pollutant in the bivalve-macroalage polyculture from the perspective of nutrient budgets. Aquaculture 406–407:97–104. CrossRefGoogle Scholar
  103. Zerebecki RA, Sorte CJB (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS ONE 5:4. Google Scholar

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Authors and Affiliations

  1. 1.Faculdade de Ciências da Universidade de LisboaMARE - Marine and Environmental Sciences CentreLisbonPortugal
  2. 2.UCIBIO, REQUIMTE, Departamento de Química, Faculdade de Ciências e TecnologiaUniversidade NOVA de LisboaCaparicaPortugal
  3. 3.Department of Fish Ecology and Evolution, Centre for Ecology, Evolution and BiogeochemistrySwiss Federal Institute of Aquatic Science and Technology (Eawag)KastanienbaumSwitzerland
  4. 4.IrsteaUR EABXCestasFrance
  5. 5.Cebimar - Centro de Biologia MarinhaUniversidade de São PauloSão SebastiãoBrazil

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