Historical changes in the distributions of invasive and endemic marine invertebrates are contrary to global warming predictions: the effects of decadal climate oscillations

Abstract

Aim We tested whether a hybrid zone that has formed between an endemic and an invasive species of marine mussel has shifted poleward as expected under a general hypothesis of global warming or has responded instead to decadal climate oscillations.Location We sampled 15 locations on the coast of California, USA, that span the distributions of the two species of marine mussels and their hybrids.Methods Mussels were sampled in 2005-08 and analysed at three nuclear gene loci using methods identical to those used in a study a decade earlier in order to document the genetic architecture of this system. Change in the system was determined by comparing the frequency of species-specific alleles and multi-locus genotypes over the intervening decade. Climate variation over the same period was examined by comparing the Pacific Decadal Oscillation (PDO), El Niño/ Southern Oscillation (ENSO), upwelling indices and sea surface temperature (SST) during and prior to the study period.Results Contrary to the general expectations of global warming we show that the highly invasive warm-water mussel Mytilus galloprovincialis and the hybrid zone formed with the endemic species Mytilus trossulus has rapidly contracted southwards. Mytilus galloprovincialis declined in abundance over the northern third of its geographic range (c. 540 km) and has become rare or absent across the northern 200 km of the range it previously colonized during its initial invasion. The distribution of the native species M. trossulus has remained unchanged over the same time period. Main conclusionsThe large-scale range shift in the warm-water invasive species M. galloprovincialis and the hybrid zone it forms with M. trossulus has been exceptionally rapid and is in the opposite direction to that predicted by the global warming hypotheses. This shift, however, is consistent with decadal climate variation associated with the ENSO and the PDO. Since the biogeography of this system was first described in 1999, the PDO has shifted from a warm phase, dominated by frequent and large El Niño events, to a cold-phase period, with minimal ENSO activity. Thus recent decadal climate variation can oppose global trends in average temperature and this study illustrates the need to integrate the effects of climate change across multiple time-scales.

Physiology and Biogeography: The Response of European Mussels (Mytilusspp.) to Climate Change*

“…Blue mussels are physiologically quiescent during winter (Bayne 1976), and there are no major differences in the SFG of M. edulis and M. galloprovincialis at cold temperatures in other seasons that would explain the inability of M. galloprovincialis populations to persist where winter temperatures are below 9 °C (Fly and Hilbish 2013). This cold-water limitation has been noted previously for European M. galloprovincialis populations (Hilbish et al 2012), as well as populations on the west coast of the U.S. (Hilbish et al 2010). There are several hypotheses on the mechanism of this limitation that warrant further investigation, including tolerance to cold-shock and reproductive abilities.…”

“…This suggests that M. galloprovincialis might not have the same capability to recover from cumulative cold damage as M. edulis. Another possibility is that the reproductive capabilities of M. galloprovincialis are impeded at temperatures below 9 °C (Hilbish et al 2010, Fly and Hilbish (2013). SFG data were not collected for winter (A).…”

Three decades of high-resolution coastal sea surface temperatures reveal more than warming

“…5d). Temperatures on these coasts are largely dominated by decadal changes in circulation patterns such as the Pacific Decadal Oscillation and the El Niño/Southern Oscillation 33,34 , which frequently alternate between contrasting warm and cold phases. Large-scale temperature fluctuations are important drivers on the biogeographic patterns observed on the Eastern pacific coast 35 , and while several studies have reported population and poleward range shifts associated with episodes of abnormally high SST 36,37 , others show that during cold phases species distributions may be driven in equatorialwards 33 , or may not change at all 38 .…”

Proteomics of hyposaline stress in blue mussel congeners (genusMytilus): implications for biogeographic range limits in response to climate change

“…Although the range limits of these congeners are still in flux due to shorter climatic variations, e.g. the Pacific Decadal Oscillation, the main hybrid zone ranges roughly from Monterey Bay to San Francisco Bay, with small numbers of M. galloprovincialis hybrids found further north to Humboldt Bay (Braby and Somero, 2006a;Hilbish et al, 2010). Field surveys indicate that the distribution within the hybrid zone is determined by both temperature and salinity (Braby and Somero, 2006a;Schneider and Helmuth, 2007).…”