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Who is taking the heat? Accounting for multiple levels of biodiversity under contemporary climatic change

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Cheating the locals: invasive mussels steal and benefit from the cooling effect of indigenous mussels
Publication . Lathlean, Justin A.; Seuront, Laurent; McQuaid, Christopher D.; Ng, Terence P. T.; Zardi, Gerardo I.; Nicastro, Katy R
The indigenous South African mussel Perna perna gapes during periods of aerial exposure to maintain aerobic respiration. This behaviour has no effect on the body temperatures of isolated individuals, but when surrounded by conspecifics, beneficial cooling effects of gaping emerge. It is uncertain, however, whether the presence of the invasive mussel Mytilus galloprovincialis limits the ability of P. perna for collective thermoregulation. We investigated whether varying densities of P. perna and M. galloprovincialis influences the thermal properties of both natural and artificial mussel beds during periods of emersion. Using infrared thermography, body temperatures of P. perna within mixed artificial beds were shown to increase faster and reach higher temperatures than individuals in conspecific beds, indicating that the presence of M. galloprovincialis limits the group cooling effects of gaping. In contrast, body temperatures of M. galloprovincialis within mixed artificial mussel beds increased slower and exhibited lower temperatures than for individuals in beds comprised entirely of M. galloprovincialis. Interestingly, differences in bed temperatures and heating rates were largely dependent on the size of mussels, with beds comprised of larger individuals experiencing less thermal stress irrespective of species composition. The small-scale patterns of thermal stress detected within manipulated beds were not observed within naturally occurring mixed mussel beds. We propose that small-scale differences in topography, size-structure, mussel bed size and the presence of organisms encrusting the mussel shells mask the effects of gaping behaviour within natural mussel beds. Nevertheless, the results from our manipulative experiment indicate that the invasive species M. galloprovincialis steals thermal properties as well as resources from the indigenous mussel P. perna. This may have significant implications for predicting how the co-existence of these two species may change as global temperatures continue to rise.
Enemies with benefits: parasitic endoliths protect mussels against heat stress
Publication . Zardi, Gerardo I.; Nicastro, Katy R; McQuaid, C. D.; Ng, T. P. T.; Lathlean, J.; Seuront, L.
Positive and negative aspects of species interactions can be context dependant and strongly affected by environmental conditions. We tested the hypothesis that, during periods of intense heat stress, parasitic phototrophic endoliths that fatally degrade mollusc shells can benefit their mussel hosts. Endolithic infestation significantly reduced body temperatures of sun-exposed mussels and, during unusually extreme heat stress, parasitised individuals suffered lower mortality rates than nonparasitised hosts. This beneficial effect was related to the white discolouration caused by the excavation activity of endoliths. Under climate warming, species relationships may be drastically realigned and conditional benefits of phototrophic endolithic parasites may become more important than the costs of infestation.
Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga
Publication . Lourenço, Carla R.; Zardi, Gerardo I.; McQuaid, Christopher D.; Serrão, Ester; Pearson, Gareth; Jacinto, Rita; Nicastro, Katy R
AimGlobal climate change has profound and diverse effects on biological diversity. Identifying present-day climate refugia is an increasingly recognized strategy for the management of biodiversity loss. Such refugia are potential safe havens that enhance environmental diversity by buffering the effects of large scale change, facilitating species persistence at regional scales and conserving unique genetic diversity. Although their ecological effects are well studied, the potential of upwelling centres to act as refugia in a scenario of climate warming remains largely unexplored. Here, we investigate whether upwelled waters act as refugia in a region heavily affected by recent climatic changes.LocationShores of south-western Iberia and north-western Africa.MethodsWe compared changes in distribution of the canopy-forming macroalga Fucus guiryi with sea surface temperature patterns in five upwelling areas and adjacent warmer regions. Population diversity and structure was inferred from genotypic analyses using nine microsatellite loci.ResultsFucus guiryi has disappeared from large expanses of non-upwelling shores, currently persisting in areas characterized by strong upwelling and reduced or non-significant rates of warming. Populations of F. guiryi were more abundant towards upwelling centres. Furthermore, the genetic characterization of populations revealed distinct genetic groups associated with each upwelling system.Main conclusionsWithin a large region of predominantly changing climate, we highlight the fundamental importance of upwelling areas as favourable, comparatively stable climates where F. guiryi has retreated and persists, preserving unique portions of the species' genetic pool.
Biogeographical patterns of endolithic infestation in an invasive and an indigenous intertidal marine ecosystem engineer
Publication . Ndhlovu, Aldwin; McQuaid, Christopher D.; Nicastro, Katy; Marquet, Nathalie; Gektidis, Marcos; Monaco, Cristián J.; Zardi, Gerardo
By altering the phenotypic properties of their hosts, endolithic parasites can modulate the engineering processes of marine ecosystem engineers. Here, we assessed the biogeographical patterns of species assemblages, prevalence and impact of endolithic parasitism in two mussel species that act as important ecosystem engineers in the southern African intertidal habitat, Perna perna and Mytilus galloprovincialis. We conducted large-scale surveys across three biogeographic regions along the South African coast: the subtropical east coast, dominated by the indigenous mussel, P. perna, the warm temperate south coast, where this species coexists with the invasive Mediterranean mussel, M. galloprovincialis, and the cool temperate west coast dominated by M. galloprovincialis. Infestation increased with mussel size, and in the case of M. galloprovincialis we found a significantly higher infestation in the cool temperate bioregion than the warm temperate region. For P. perna, the prevalence of infestation was higher on the warm temperate than the subtropical region, though the difference was marginally non-significant. On the south coast, there was no significant difference in infestation prevalence between species. Endolith-induced mortality rates through shell collapse mirrored the patterns for prevalence. For P. perna, endolith species assemblages revealed clear grouping by bioregions. Our findings indicate that biogeography affects cyanobacteria species composition, but differences between biogeographic regions in their effects are driven by environmental conditions.
Taking the heat: distinct vulnerability to thermal stress of central and threatened peripheral lineages of a marine macroalga
Publication . Saada, Gabriel; Nicastro, Katy R; Jacinto, Rita; McQuaid, Christopher D.; Serrão, Ester; Pearson, G. A.; Zardi, Gerardo I.
Aim Although many studies have reported the effects of climate change on species' distributions, most of them consider each species as a physiologically homogenous unit. However, different lineages or populations inhabiting distinct bioregions within a species' distributional range can retain unique genetic diversity that could result in distinct adaptive capacities. A recent, large, climate-correlated distributional range contraction occurred at the southern edge of the intertidal macroalga Fucus vesiculosus, causing loss of genetic diversity unique to the southern clade. We tested for differential selective constraints and signs of local adaptation to thermal stress in the two genetic lineages.Location Iberian Atlantic shores.Methods We performed a series of common garden experiments and a field reciprocal transplant.Results In the laboratory, southern F. vesiculosus showed higher resilience to heat stress than northern individuals. On the southwest coast of Portugal, local individuals grew more than those transplanted from the northern range; in the north of Portugal, growth rates did not differ significantly between lineages.Conclusions We present evidence for unique adaptive traits at the retreating edge of the species' distribution that could be lost if warming trends persist. The loss of the distinct southern genetic heritage could end potential ongoing diversification or speciation processes and impoverishes the adaptive potential of the species as a whole.

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Funding agency

Fundação para a Ciência e a Tecnologia

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Investigador FCT

Funding Award Number

IF/01413/2014/CP1217/CT0004

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