Skip to main content

Advertisement

Log in

Northward establishment of the mediterranean mussel Mytilus galloprovincialis limited by changing climate

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Throughout Europe the blue mussel Mytilus edulis is dominant in the north while the Mediterranean mussel Mytilus galloprovincialis prevails in the south. Studies from the 1970s to the late 2000′s documented the northward range expansion of M. galloprovincialis in Europe and predicted this trend to continue with climate change. The objectives of this study were to sample predominantly wild mussels (n = 1459) at twenty-four Irish intertidal sites over a seven year period and at three Welsh sites to investigate (a) the abundance and distribution of Mytilus spp., identified molecularly by polymerase chain reaction (PCR), and (b) compare with historical observations, at Irish sites where M. galloprovincialis was observed to be more abundant than M. edulis. Mussels were sampled more than once at certain sites to investigate if there was a temporal effect. The findings of this study indicated that M. edulis was consistently the most abundant species, followed by hybrids and M. galloprovincialis. At certain sites, hybrids were detected while M. galloprovincialis was absent. This finding may indicate transient M. galloprovinicialis populations or input from individuals subtidally. One factor that may be of importance was the anomalous cold winter “polar snaps” (2010 and 2011) that occurred during this study. In addition, heavy precipitation events and subsequent increased freshwater loading in bays and estuaries also occurred during this time period. Future warming climate scenarios have been predicted to facilitate the northwards establishment of M. galloprovincialis, however, nearshore meteorological extremes may have an impact in its larval settlement, establishment and subsequent reproductive output.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

modified from Noone et al. (2015)

Similar content being viewed by others

References

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672–675

    CAS  PubMed  Google Scholar 

  • Barton NH (1979) The dynamics of hybrid zones. Heredity 43:341–359

    Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148

    Google Scholar 

  • Barton NH, Hewitt GM (1989) Adaptation, speciation and hybrid zones. Nature 431:497–503

    Google Scholar 

  • Bayne BL (1964) Primary and secondary settlement in Mytilus edulis L. (Mollusca). J Animal Ecol 33:513–523

    Google Scholar 

  • Beukema JJ (1985) Zoobenthos survival during severe winters on high and low tidal flats in the Dutch Wadden Sea. In: Gray JS, Christiansen ME (eds) Marine biology of polar regions and effects of stress on marine organisms. Wiley, Chichester, pp 351–361

    Google Scholar 

  • Blegvad H (1929) Mortality among animals of the littoral region in ice winters. Rep Dan Biol Stn 35:49–62

    Google Scholar 

  • Braby CE, Somero GN (2006) Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J Exp Biol 209:2554–2566

    PubMed  Google Scholar 

  • Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215

    Google Scholar 

  • Brown J, Carrillo L, Fernand L, Horsburgh KJ, Hill AE, Young EF, Medler KJ (2003) Observations of the physical structure and seasonal jet-like circulation of the Celtic Sea and St. George's Channel of the Irish Sea. Cont Shelf Res 23:33–561

    Google Scholar 

  • Canning-Clode J, Fowler AE, Byers JE, Carlton JT, Ruiz GM (2011) 'Caribbean Creep' chills out: climate change and marine invasive species. PLoS ONE 6(12):e29657

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canning-Clode J, Carlton JT (2017) Refining and expanding global climate change scenarios in the sea: poleward creep complexities, range termini, and setbacks and surges. Divers Distrib 23:463–473

    Google Scholar 

  • Casal G, Lavendar SJ (2017) Spatio-temporal variability of sea surface temperature in Irish waters (1982–2015) using AVHRR sensor. J Sea Res 129:89–104

    Google Scholar 

  • Christiansen BO (1965) Notes of the littoral fauna of Bear Island. Astarte 26:1–15

    Google Scholar 

  • Comensañsa AS, Sanjuan A (1997) Microgeographic allozyme differentiation in the hybrid zone of Mytilus galloprovincialis and M. edulis on the continental European coast. Helg Meeresunters 51:107–124

    Google Scholar 

  • Crisp DJ (1964) The effects of the severe winter of 1962–63 on marine life in Britain. J Anim Ecol 33:165–210

    Google Scholar 

  • Dailianis S (2010) Environmental impact of anthropogenic activities: the use of mussels as a reliable tool for monitoring marine pollution. In: McGevin LE (ed) Mussels: anatomy, habitat and environmental impact. Nova Science Publishers Inc, New York, pp 43–72

    Google Scholar 

  • Dias PJ, Dordor A, Tulett D, Piertney S, Davies IM, Snow M (2009) Survey of mussel (Mytilus) species at Scottish shellfish farms. Aqua Res 40:1715–1722

    Google Scholar 

  • FAO (2017) Cultured aquatic species information programme: Mytilus edulis. www.fao.org/fishery/culturedspecies/Mytilus_edulis/en Accessed 16 Mar 2020

  • Fuentes J, López JL, Mosquera E, Vázquez J, Villalba A, Alvarez G (2002) Growth, mortality, pathological conditions and protein expression of Mytilus edulis and M. galloprovincialis crosses cultured in the Ría de Arousa (NW of Spain). Aquaculture 213:233–251

    Google Scholar 

  • Gardner JPA (1994) The structure and dynamics of naturally occurring hybrid Mytilus edulis Linnaeus, 1758 and Mytilus galloprovincialis Lamarck, 1819 (Bivalvia: Mollusca) populations: review and interpretation. Arch Hydrobiol Suppl 99:37–71

    Google Scholar 

  • Gardner JPA (1997) Hybridization in the sea. Adv Mar Biol 31:1–65

    Google Scholar 

  • Geller JB (1999) Decline of a native mussel masked by sibling species invasion. Conserv Biol 13:661–664

    Google Scholar 

  • GISD (Global Invasive Species Database). 2017. Species profile: Mytilus galloprovincialis. Downloaded from https://www.iucngisd.org/gisd/species.php?sc=102. Accessed 16 Mar 2020

  • Gosling EM, Wilkins NP (1981) Ecological genetics of the mussels Mytilus edulis and M. galloprovincialis on Irish Coasts. Mar Ecol Prog Ser 4:221–227

    Google Scholar 

  • Gosling EM, Wilkins NP (1977) Phosphoglucoisomerase allele frequency data in Mytilus edulis from Irish coastal sites: its ecological significance. In: Keegan BF, O’Ceidigh P, Boaden PJS (eds) Biology of benthic organisms. Pergamon Press, London, pp 297–309

    Google Scholar 

  • Gosling EM (1992) Systematics and geographic distribution of Mytilus. In: Gosling E (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 1–20

    Google Scholar 

  • Gosling E (2004) Bivalve molluscs: biology, ecology and culture. Blackwell Publishing, New Jersey

    Google Scholar 

  • Gosling E, Doherty S, Howley N (2008) Genetic characterization of hybrid mussel (Mytilus) populations on Irish coasts. J Mar Biol Assoc UK 88:341–346

    CAS  Google Scholar 

  • Hepper BT (1957) Notes on Mytilus galloprovincialis Lamarck in Great Britain. J Mar Biol Assoc UK 36:33–40

    Google Scholar 

  • Howard DJ (1986) A zone of overlap and hybridisation between two ground cricket species. Evolution 40:34–43

    PubMed  Google Scholar 

  • Hughes RN, Hughes DJ, Smith IP, Dale AC (2015) Oceanography and marine biology: an annual review. CRC Press, Florida

    Google Scholar 

  • Inoue K, Waite HJ, Matsuoka M, Odo S, Harayama S (1995) Interspecific variations in adhesive proteion sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biol Bull 189:370–375

    CAS  PubMed  Google Scholar 

  • Jansen JM, Bonga SW, Hummel H (2007) Differential coldshock resistance among acclimated European mussel populations. Mar Freshw Behav Physiol 40:233–245

    Google Scholar 

  • Jones PD, Osborn TJ, Briffa KR (2001) The evolution of climate over the last millennium. Science 292:662–667

    CAS  PubMed  Google Scholar 

  • Kristensen I (1957) Differences in density and growth in a cockle population in the Dutch Wadden Sea. Arch Neerl Zool 12:351–453

    Google Scholar 

  • Lenz M, Ahmed Y et al (2018) Heat challenges can enhance population tolerance to thermal stress in mussels: a potential mechanism by which ship transport can increase species invasiveness. Biol Invasions 20(11):3107–3122

    Google Scholar 

  • Lewis J, Seed R (1969) Morphological variations in Mytilus from southwest England in relation to the occurrence of M. galloprovincialis. Cah Bio Mar 10:231–253

  • Lima FP, Ribeiro PA, Queiroz N, Hawkins SJ, Santos AM (2007) Do distributional shifts of northern and southern species of algae match the warming pattern? Global Change Biol 13:2592–2604

    Google Scholar 

  • Loomis SH (1995) Freezing tolerance of marine invertebrates. Oceanogr Mar Biol Annu Rev 33:337–350

    Google Scholar 

  • Mayr E (1963) Animal species and evolution cambridge. Harvard University Press, Cambridge

    Google Scholar 

  • Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–277

    Google Scholar 

  • Noone S, Murphy C, Coll J, Matthews T, Mullan M, Wilby RL, Walsh S (2015) Homogenisation and analysis of an expanded long-term monthly rainfall network for the Island of Ireland (1850–2010). Int J Climatol 36:2837–2853

    Google Scholar 

  • Ozer A, Guneydag S (2014) First report of some parasites from Mediterranean mussel, Mytilus galloprovincialis Lamarck, 1819, collected from the Black Sea coast at Sinop. Turk J Zool 38:486–490

    Google Scholar 

  • Page HM, Hubbard DM (1987) Temporal and spatial patterns of growth in mussels Mytilus edulis on an offshore platform: relationships to water temperature and food availability. J Exp Mar Biol Ecol 111:159–179

    Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915

    CAS  PubMed  Google Scholar 

  • Rawson PD, Hilbish TJ (1998) Asymmetric introgression of mitochondrial DNA among European populations of blue mussels (Mytilus spp.). Evolution 52:100–108

    PubMed  Google Scholar 

  • Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400

    CAS  PubMed  Google Scholar 

  • Saavedra C, Donald TS, Stanwood RR, Zouros E (1996) Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize. Genetics 143:1359–1367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanjuan A, Zapata C, Alvarez G (1994) Mytilus galloprovincialis and M. edulis on the coasts of the Iberian Peninsula. Mar Ecol Prog Ser 113:131–146

    Google Scholar 

  • Sagarin RD, Barry JP, Gilman SE, Baxter CH (1999) Climate related change in an intertidal community over short and long time scales. Ecol Monogr 69:465–490

    Google Scholar 

  • Sarver SK, Foltz DW (1993) Genetic population-structure of a species complex of blue mussels (Mytilus spp.). Mar Biol 117:105–112

    Google Scholar 

  • Schneider KR (2008) Heat stress in the intertidal: comparing survival and growth of an invasive and native mussel under a variety of thermal conditions. Biol Bull 215:253–264

    PubMed  Google Scholar 

  • Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores I breeding and settlement. Oecologia 3:277–316

    CAS  PubMed  Google Scholar 

  • Seed R (1974) Morphological variations in Mytilus from the Irish Coasts in relation to the occurrence and distribution of M. galloprovincialis Lmk. Cah Biol Mar 15:1–25

  • Seed R, Suchanek TH (1992) Population and community ecology of Mytilus. In: Gosling EM (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 87–169

    Google Scholar 

  • Shurova N (2001) Influence of salinity on the structure and the state of bivalve Mytilus galloprovincialis populations. Russ J Mar Biol 27:151–155

    Google Scholar 

  • Skibinski DOF, Beardmore JA, Cross TF (1983) Aspects of the population genetics of Mytilus (Mytilidae; Mollusca) in the British Isles. Biol J Linn Soc 19:137–183

    Google Scholar 

  • Smidt ELB (1944) The effects of ice winters on marine littoral faunas. Folia Geogr Dan 2:1–36

    Google Scholar 

  • Steele CJ, Dorling SR, von Glasow R, Bacon J (2013) Idealized WRF model sensitivity simulations of sea breeze types and their effects on offshore windfields. Atmos Chem Phys 13:443–461

    CAS  Google Scholar 

  • Suchanek TH, Geller J, Kreiser B, Mitton J (1997) Zoogeographic distributions of the sibling species Mytilus galloprovincialis and M. trossulus (Bivalvia: Mytilidae) and their hybrids in the north Pacific. Biol Bull 193:187–194

    CAS  PubMed  Google Scholar 

  • Tang Q, Zhang X, Yang X, Francis JA (2013) Cold winter extremes in northern continents linked to Arctic sea ice loss. Environ Res Lett 8:014036

    Google Scholar 

  • Toro JE, Thompson RJ, Innes DJ (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland. Mar Biol 141:897–909

    Google Scholar 

  • Tyler-Walters H, Seed R (2006) "The Marine Life Information Network" (On-line). at https://www.marlin.ac.uk/species/detail/1421 Accessed 16 Mar 2020

  • Van Erkom SC, Griffiths CL (1992) Physiological energetics of four South African mussel species in relation to size, ration and temperature. Comp Biochem Physiol 101:779–789

    Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Williams RJ (1970) Freezing tolerance in Mytilus edulis. Comp Biochem Physiol 35:145–161

    Google Scholar 

  • Zagata C, Young C, Sountis J, Kuehl M (2008) ``Mytilus edulis`` (Online), Animal diversity web. https://animaldiversity.org/accounts/Mytilus_edulis/ Accessed 16 Mar 2020

Download references

Acknowledgements

This study was part-funded by the SUSFISH (Grant Agreement No. 244132) and BlueFish (Grant Agreement No. 80991) Projects under the European Regional Development Fund (ERDF) through the EU Ireland/Wales Interregional (INTERREG) Programme. A cross-border programme investing in the overall economic, environmental and social well-being of Ireland and Wales. The authors would like to thank the reviewers for their positive response to this study and for providing interesting comments, thoughts and very relevant references.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. A. Lynch.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lynch, S.A., Coghlan, A., Leary, B.O. et al. Northward establishment of the mediterranean mussel Mytilus galloprovincialis limited by changing climate. Biol Invasions 22, 2725–2736 (2020). https://doi.org/10.1007/s10530-020-02294-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02294-6

Keywords

Navigation