Non-native marine invertebrates are more tolerant towards environmental stress than taxonomically related native species: Results from a globally replicated study

Environmental Research

Volumn 111, Issue 7, 2011, Pages 943-952

  Lenz, Mark ^a   da Gama, Bernardo A P ^b   Gerner, Nadine V ^c   Gobin, Judith ^d   Gröner, Frederike ^e   Harry, Anil ^d   Jenkins, Stuart R ^f   Kraufvelin, Patrik ^g,j   Mummelthei, Corinna ^h   Sareyka, Jörg ⁱ   Xavier, Eduardo A ^b   Wahl, Martin ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^c GOETHE UNIVERSITY   (Germany)

^d UNIVERSITY OF THE WEST INDIES   (Trinidad and Tobago)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f BANGOR UNIVERSITY   (United Kingdom)

^g ÅBO AKADEMI UNIVERSITY   (Finland)

^h UNIVERSITY OF FREIBURG   (Germany)

ⁱ RUHR UNIVERSITY BOCHUM   (Germany)

^j NOVIA UNIVERSITY OF APPLIED SCIENCES   (Finland)

more..

Author keywords

Native species; Non native species; Respiration; Stress tolerance; Survival

Indexed keywords

ADAPTATION; BIVALVE; CRUSTACEAN; EMPIRICAL ANALYSIS; ENVIRONMENTAL STRESS; FUTURE PROSPECT; GLOBAL CHANGE; INVASIVENESS; NATIVE SPECIES; OXYGEN; RESPIRATION; RISK ASSESSMENT; SEA SURFACE SALINITY; SEA SURFACE TEMPERATURE; SURVIVAL; TAXONOMY;

ANIMAL EXPERIMENT; ARTICLE; ASCIDIACEA; BIVALVE; BRACHIDONTES EXUSTUS; CONTROLLED STUDY; CRASSOSTREA GIGAS; DIDEMNUM VEXILLUM; DIPLOSOMA LISTERIANUM; ENVIRONMENTAL STRESS; GAMMARUS; GAMMARUS TIGRINUS; GAMMARUS ZADDACHI; HEAT STRESS; HYPOOSMOTIC STRESS; HYPOXIA; INVERTEBRATE; ISOGNOMON BICOLOR; MARINE SPECIES; NATIVE SPECIES; NONHUMAN; PERNA PERNA; PERNA VIRIDIS; PRIORITY JOURNAL; SACCOSTREA GLOMERATA; SIMULATION; SPECIES COMPARISON; SURVIVAL RATE;

ACCLIMATIZATION; ANIMALS; BIVALVIA; CRUSTACEA; ECOSYSTEM; INTRODUCED SPECIES; OXYGEN CONSUMPTION; POPULATION DYNAMICS; SALINITY; STRESS, PHYSIOLOGICAL; TEMPERATURE; UROCHORDATA;

ASCIDIACEA; BIVALVIA; CRASSOSTREA GIGAS; CRUSTACEA; DIDEMNUM; DIPLOSOMA LISTERIANUM; GAMMARUS ZADDACHI; HORMOMYA EXUSTUS; INVERTEBRATA; ISOGNOMON BICOLOR; PERNA VIRIDIS; SACCOSTREA GLOMERATA; VEXILLUM;

EID: 80052033297     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2011.05.001     Document Type: Article

References (72)

1. Agard J.B.R., Kishore R., Bayne B. Perna viridis (Linnaeus, 1758): first record of the indo-pacific green mussel (Mollusc: Bivalvia) in the Caribbean. Caribb. Mar. Stud. 1992, 3:59-60.
2. Anestis A., Pörtner H.O., Michaelidis B. Anaerobic metabolic patterns related to stress responses in Mytilus galloprovincialis. J. Exp. Mar. Biol. Ecol. 2010, 94:123-133.
3. Bakhmet I.N., Berger V., Ja Khalaman V.V. The effect of salinity change on the heart rate of Mytilus edulis specimens from different ecological zones. J. Exp. Mar. Biol. Ecol. 2005, (318):121-126.
4. Barber B.J., Fajans J.S., Baker S.M., Baker P. Gametogenesis in the non-native green mussel, Perna viridis, and the native scorched mussel, Brachidontes exustus, in Tampa Bay, Florida. J. Shellfish Res. 2005, 24:1087-1095.
5. Bayne B.L. A physiological comparison between Pacific oysters Crassostrea gigas and Sydney Rock oysters Saccostrea glomerata: food, feeding and growth in a shared estuarine habitat. Mar. Ecol. Prog. Ser. 2002, 232:163-178.
6. Berrill N.J. The Tunicata with an Account of the British Species 1950, Ray Society, London.
7. Bousfield E.L. Freshwater amphipod crustaceans of glaciated North America. Can. Field Nat. 1958, 72:55-113.
8. Braby C., Somero G. Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J. Exp. Biol. 2006, 209:2554-2566.
9. Bullard S.G., Sedlack B., Reinhardt J.F., Litty C., Gareau K., Whitlatch R.B. Fragmentation of colonial ascidians: differences in reattachment capability among species. J. Exp. Mar. Biol. Ecol. 2007, 342:166-168.
10. Brunetti R., Bressan M., Marin M., Libralato M. On the ecology and biology of Diplosoma listerianum (Milne-Edwards, 1841) (Ascidiacea, Didemnidae). Vie Milieu 1988, 38:123-131.
11. Chapman D., Ranelletti M., Kaushik S. Invasive marine algae: an ecological perspective. Bot. Rev. 2006, 72:153-178.
12. Coles S.L., Jokiel P.L. Effects of salinity on coral reefs. Pollution in Tropical Aquatic Systems 1992, 147-166. CRC Press, Boca Raton. D.W. Connell, D.W. Hawker (Eds.).
13. David E., Tanguy A., Pichavant K., Moraga D. Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 2005, 272:5635-5652.
14. de Vooys C.G.N. Anaerobic metabolism in sublittoral living Mytilus galloprovincialis in the Mediterranean IV: role of amino acids in adaptation to low salinities during anaerobiosis and aerobiosis. J. Comp. Biochem. Physiol 1991, 100A:423-432.
15. de Zwaan A., Mathieu M. Cellular biochemistry and endocrinology. The Mussel Mytilus: Ecology, Physiology, Genetics and Culture 1991, 223-307. Elsevier, New York. E. Gosling (Ed.).
16. DeFur P.L., Mangum C.P. The effects of environmental variables on the heart rates of invertebrates. J. Comp. Biochem. Physiol, 1979, 62A:283-294.
17. Domaneschi O., Martins C.M. Isognomon bicolor (C.B. Adams) (Bivalvia, Isognomonidae): Primeiro registro para o Brasil, redescrição da 50 espécie e consideraçes sobre a ocorrĉncia e distribuição de Isognomon na costa brasileria. Rev. Bras. Zool. 2002, 19:601-610.
18. Epelbaum A., Therriault T.W., Paulson A., Pearce C.M. Botryllid tunicates: culture technique and experimental procedures. Aquat. Invasions 2009, 4:111-120.
19. Ekau W., Auel H., Pörtner H.-O., Gilbert D. Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 2010, 7:1669-1699.
20. Facon B., Genton B.J., Shykoff J., Jarne P., Estoup A., David P. A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol. Evol. 2006, 21:130-135.
21. Farrar, J.F., Vaze, P., (Eds.), 2000. Wales: Changing Climate, Challenging Choices-A Scoping Study of Climate Change Impacts in Wales. University of Wales, Bangor, ECOTEC Research & Consulting, Institute of Terrestrial Ecology, Bangor, University of East Anglia.
22. Ganning B. On the ecology of Heterocypris salinus, H. incongruens and Cypridopsis aculeata (Crustacea: Ostracoda) from Baltic brackish-water rockpools. Mar. Biol. 1971, 8:271-279.
23. Gittenberger A. Recent population expansions of non-native ascidians in The Netherlands. J. Exp. Mar. Biol. Ecol. 2007, 342:122-126.
24. Global Invasive Species Database, 2011. Perna perna. Available from: 〈〉 (Accessed 19 April 2011). http://www.issg.org/database/species/ecology.asp?si=742&fr=1&sts=sss&lang=EN.
25. Goodbody I. Mass mortality of a marine fauna following tropical rains. Ecology 1961, 42:150-155.
26. Griffith K., Mowat S., Holt R.H.F., Ramsay K., Bishop J.D.D., Lambert G., Jenkins S.R. First records in Great Britain of the invasive colonial ascidian Didemnum vexillum Kott, 2002. Aquat. Invasions 2009, 4:581-590.
27. Hansson, H.G., 1989. NEAT (North East Atlantic Taxa): South Scandinavian marine Chordata check-list. Internet pdf Ed., August 1998. 〈〉. http://www.tmbl.gu.se.
28. Hicks D., Tunnell J., McMahon R. Population dynamics of the nonindigenous brown mussel Perna perna in the Gulf of Mexico compared to other world-wide populations. Mar. Ecol. Prog. Ser. 2001, 211:181-192.
29. IUCN, 2010. Invasive Species Specialist Group. 〈〉. 15 October 2010. http://www.issg.org/.
30. Jeschke J.M., Strayer D.L. Determinants of vertebrate invasion success in Europe and North America. Global Change Biol. 2006, 12:1608-1619.
31. Jewett E.B., Hines A.H., Ruiz G.M. Epifaunal disturbance by periodic low levels of dissolved oxygen: native vs. invasive species response. Mar. Ecol. Prog. Ser. 2005, 304:31-44.
32. Kelly D.W., Muirhead J.R., Heath D.D., Macisaac H.J. Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol. Ecol. 2006, 15:3641-3653.
33. van Kleunen M., Dawson W., Schlaepfer D., Jeschke J., Fischer M. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol. Lett. 2010, 13:937-946.
34. van Kleunen M., Weber E., Fischer M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 2010, 13:235-245.
35. Kolar C.S., Lodge D.M. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 2001, 16:199-204.
36. Korpinen S., Westerbom M. Microhabitat segregation of the amphipod genus Gammarus (Crustacea: Amphipoda) in the Northern Baltic Sea. Mar. Biol. 2010, 157:361-370.
37. Krassoi F.R., Brown K.R., Bishop M.J., Kelaher B.P., Summerhayes S. Condition-specific competition allows coexistence of competitively superior exotic oysters with native oysters. J. Anim. Ecol. 2008, 77:5-15.
38. Kraufvelin P., Salovius S. Animal diversity in Baltic rocky shore macroalgae: can Cladophora glomerata compensate for lost Fucus vesiculosus? Estuar. Coast Shelf Sci. 2004, 61:369-378.
39. Lambert G. Ecology and natural history of the protochordates. Can. J. Zool. 2005, 83:34-50.
40. Lambert G. Adventures of a sea squirt sleuth: unravelling the identity of Didemnum vexillum, a global ascidian invader. Aquat. Invasions 2009, 4:5-28.
41. Lee C. Evolutionary genetics of invasive species. Trends Ecol. Evol. 2002, 17:386-391.
42. Leppäkoski E., Olenin S. Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biol. Invasions 2000, 2:151-163.
43. Leppäkoski E., Gollasch S., Gruszka P., Ojaveer H., Olenin S., Panov V. The Baltic-a sea of invaders. Can. J. Fish. Aquat. Sci. 2002, 59:1175-1188.
44. Lockwood J.L., Cassey P., Blackburn T. The role of propagule pressure in explaining species invasions. Trends Ecol. Evol. 2005, 20:223-228.
45. Lockwood J.L., Hoopes M.F., Marchetti M.P. Invasion Ecology 2007, Blackwell Publishing, Oxford.
46. Marshall D.J., Keough M.J. Offspring size effects in the marine environment: a field test for a colonial invertebrate. Aust. Ecol. 2005, 30:275-280.
47. Nicholson S. Ecophysiological aspects of cardiac activity in the subtropical mussel Perna viridis (L.) (Bivalvia: Mytilidae). J. Exp. Mar. Biol. Ecol. 2002, 267:207-222.
48. Norkko A., Bonsdorff E. Rapid zoobenthic community responses to accumulations of drifting algae. Mar. Ecol. Prog. Ser. 1996, 131:143-157.
49. Osman R.W., Whitlatch R.B. Variation in the ability of Didemnum sp. to invade established communities. J. Exp. Mar. Biol. Ecol. 2007, 342:40-53.
50. Osovitz C.J., Hofmann G.E. Marine macrophysiology: studying physiological variations across large spatial scales in marine systems. Comp. Biochem. Physiol. A 2007, 147:821-827.
51. Paavola M., Laine A.O., Helavuori M., Kraufvelin P. Profiling four brackish water harbours: zoobenthic composition and invasion status. Bor. Environ. Res. 2008, 13:159-175.
52. Pienimäki M., Helavuori M., Leppäkoski E. First finding of the North American amphipod Gammarus tigrinus Sexton, 1939 along the Finnish coast. Memoranda Soc. Fauna Flora Fennica 2004, 80:17-19.
53. Piola R.F., Johnston E.L. Comparing differential tolerance of native and non-indigenous marine species to metal pollution using novel assay techniques. Environ. Pollut. 2009, 157:2853-2864.
54. Powell A.W. New Zealand Mollusca. Marine, Land and Freshwater Shells 1979, Collins, Auckland.
55. Ricciardi A., Rasmussen J.B. Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can. J. Fish. Aquat. Sci. 1998, 55:1759-1765.
56. Richards C.L., Bossdorf O., Muth N.Z., Gurevitch J., Pigliucci M. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol. Lett. 2006, 9:981-991.
57. Richardson D.M., Pysek P. Fifty years of invasion ecology-the legacy of Charles Elton. Diversity Distributions 2008, 14:161-168.
58. Roman J. Diluting the founder effect: cyptic invasions expand a marine invader's range. Proc. R. Soc. B 2006, 273:2453-2459.
59. Ruiz G.M., Fofonoff P.W., Carlton J.T., Wonham M.J., Hines A.H. Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu. Rev. Ecol. Syst. 2000, 31:481-531.
60. Sadok S., Uglow R.F., Haswell S.J. Haemolymph and mantle fluid ammonia and ninhydrin positive substances variations in salinity-challenged mussels (Mytilus edulis L.). J. Exp. Mar. Biol. Ecol. 1997, 212:195-212.
61. Salovius S., Kraufvelin P. Filamentous green alga Cladophora glomerata as a habitat for littoral macrofauna in the Northern Baltic Sea. Ophelia 2004, 58:65-78.
62. Sareyka, J., Kraufvelin, P., Lenz, M., Lindström, M., Tollrian, R., Wahl, M., 2011. Differences in stress tolerance and brood size between a non-indigenous and an indigenous gammarid in the northern Balti Sea. Mar. Biol., in press. doi:10.1007/s00227-011-1708-5.
63. Schneider K.R. Heat stress in the intertidal: comparing survival and growth of an invasive and native mussel under a variety of thermal conditions. Biol. Bull. 2008, 215:253-264.
64. Souza R.C.C.L., Fernandes F.C., Silva E.P. A study on the occurrence of the brown mussel Perna perna on the sambaquis of the Brazilian coast. Rev. Mus. Arqueol. Etnol. 2003, 13:3-24.
65. Stickle W.B., Sabourin T.D. Effects of salinity on the respiration and heart rate of the common mussel, Mytilus edulis L., and the black chiton, Katherina tunicata (Wood). J. Exp. Mar. Biol. Ecol. 1979, 41:257-268.
66. Valentine P.C., Carman M.R., Blackwood D.S., Heffron E.J. Ecological observations on the colonial ascidian Didemnum sp. in a New England tide pool habitat. J. Exp. Mar. Biol. Ecol. 2007, 342:109-121.
67. Velazquez J.M., Lindquist S. Hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 1984, 36:652-662.
68. Williamson M. Invasions. Ecography 1999, 22:5-12.
69. Williamson M.H., Fitter A. The characters of successful invaders. Biol. Conserv. 1996, 78:163-170.
70. Vance T., Lauterbach L., Lenz M., Wahl W., Sanderson R.A., Thomason J.C. Rapid invasion and ecological interactions of Diplosoma listerianum in the North Sea, UK. Mar. Biodiversity Rec. 2008, 2:e59. 10.1017/S1755267209000815.
71. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science 1982, 217:1214-1222.
72. Zardi G.I., Nicastro K.R., McQuaid C.D., Erlandsson J. Sand and wave induced mortality in invasive (Mytilus galloprovincialis) and indigenous (Perna perna) mussels. Mar. Biol. 2008, 153:853-858.