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Biomineralization plasticity and environmental heterogeneity predict geographical resilience patterns of foundation species to future change

Biomineralization plasticity and environmental heterogeneity predict geographical resilience patterns of foundation species to future change
Biomineralization plasticity and environmental heterogeneity predict geographical resilience patterns of foundation species to future change

Although geographical patterns of species' sensitivity to environmental changes are defined by interacting multiple stressors, little is known about compensatory processes shaping regional differences in organismal vulnerability. Here, we examine large-scale spatial variations in biomineralization under heterogeneous environmental gradients of temperature, salinity and food availability across a 30° latitudinal range (3,334 km), to test whether plasticity in calcareous shell production and composition, from juveniles to large adults, mediates geographical patterns of resilience to climate change in critical foundation species, the mussels Mytilus edulis and M. trossulus. We find shell calcification decreased towards high latitude, with mussels producing thinner shells with a higher organic content in polar than temperate regions. Salinity was the best predictor of within-region differences in mussel shell deposition, mineral and organic composition. In polar, subpolar, and Baltic low-salinity environments, mussels produced thin shells with a thicker external organic layer (periostracum), and an increased proportion of calcite (prismatic layer, as opposed to aragonite) and organic matrix, providing potentially higher resistance against dissolution in more corrosive waters. Conversely, in temperate, higher salinity regimes, thicker, more calcified shells with a higher aragonite (nacreous layer) proportion were deposited, which suggests enhanced protection under increased predation pressure. Interacting effects of salinity and food availability on mussel shell composition predict the deposition of a thicker periostracum and organic-enriched prismatic layer under forecasted future environmental conditions, suggesting a capacity for increased protection of high-latitude populations from ocean acidification. These findings support biomineralization plasticity as a potentially advantageous compensatory mechanism conferring Mytilus species a protective capacity for quantitative and qualitative trade-offs in shell deposition as a response to regional alterations of abiotic and biotic conditions in future environments. Our work illustrates that compensatory mechanisms, driving plastic responses to the spatial structure of multiple stressors, can define geographical patterns of unanticipated species resilience to global environmental change.

Animal Shells, Animals, Biomineralization, Hydrogen-Ion Concentration, Mytilus edulis, Seawater
1354-1013
4179-4193
Telesca, Luca
ece9af91-8459-4151-b9f8-fdff453142ce
Peck, Lloyd S
097d27ed-4644-4bc1-a855-045029ace2df
Sanders, Trystan
4f3b5742-82bb-48d6-bcaa-0489c0880628
Thyrring, Jakob
b58291aa-f416-4930-b88e-e80ca7e0ea22
Sejr, Mikael K
98aa827d-fd72-4750-9aee-d3c4b61ce887
Harper, Elizabeth M
a365be7f-8523-43e2-a102-720eaed6c856
Telesca, Luca
ece9af91-8459-4151-b9f8-fdff453142ce
Peck, Lloyd S
097d27ed-4644-4bc1-a855-045029ace2df
Sanders, Trystan
4f3b5742-82bb-48d6-bcaa-0489c0880628
Thyrring, Jakob
b58291aa-f416-4930-b88e-e80ca7e0ea22
Sejr, Mikael K
98aa827d-fd72-4750-9aee-d3c4b61ce887
Harper, Elizabeth M
a365be7f-8523-43e2-a102-720eaed6c856

Telesca, Luca, Peck, Lloyd S, Sanders, Trystan, Thyrring, Jakob, Sejr, Mikael K and Harper, Elizabeth M (2019) Biomineralization plasticity and environmental heterogeneity predict geographical resilience patterns of foundation species to future change. Global Change Biology, 25 (12), 4179-4193. (doi:10.1111/gcb.14758).

Record type: Article

Abstract

Although geographical patterns of species' sensitivity to environmental changes are defined by interacting multiple stressors, little is known about compensatory processes shaping regional differences in organismal vulnerability. Here, we examine large-scale spatial variations in biomineralization under heterogeneous environmental gradients of temperature, salinity and food availability across a 30° latitudinal range (3,334 km), to test whether plasticity in calcareous shell production and composition, from juveniles to large adults, mediates geographical patterns of resilience to climate change in critical foundation species, the mussels Mytilus edulis and M. trossulus. We find shell calcification decreased towards high latitude, with mussels producing thinner shells with a higher organic content in polar than temperate regions. Salinity was the best predictor of within-region differences in mussel shell deposition, mineral and organic composition. In polar, subpolar, and Baltic low-salinity environments, mussels produced thin shells with a thicker external organic layer (periostracum), and an increased proportion of calcite (prismatic layer, as opposed to aragonite) and organic matrix, providing potentially higher resistance against dissolution in more corrosive waters. Conversely, in temperate, higher salinity regimes, thicker, more calcified shells with a higher aragonite (nacreous layer) proportion were deposited, which suggests enhanced protection under increased predation pressure. Interacting effects of salinity and food availability on mussel shell composition predict the deposition of a thicker periostracum and organic-enriched prismatic layer under forecasted future environmental conditions, suggesting a capacity for increased protection of high-latitude populations from ocean acidification. These findings support biomineralization plasticity as a potentially advantageous compensatory mechanism conferring Mytilus species a protective capacity for quantitative and qualitative trade-offs in shell deposition as a response to regional alterations of abiotic and biotic conditions in future environments. Our work illustrates that compensatory mechanisms, driving plastic responses to the spatial structure of multiple stressors, can define geographical patterns of unanticipated species resilience to global environmental change.

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More information

e-pub ahead of print date: 20 August 2019
Published date: December 2019
Keywords: Animal Shells, Animals, Biomineralization, Hydrogen-Ion Concentration, Mytilus edulis, Seawater

Identifiers

Local EPrints ID: 448355
URI: http://eprints.soton.ac.uk/id/eprint/448355
ISSN: 1354-1013
PURE UUID: f50549e4-b721-42a3-ab98-d30c377b0edc
ORCID for Trystan Sanders: ORCID iD orcid.org/0000-0002-7605-0747

Catalogue record

Date deposited: 21 Apr 2021 16:30
Last modified: 16 Mar 2024 11:56

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Contributors

Author: Luca Telesca
Author: Lloyd S Peck
Author: Trystan Sanders ORCID iD
Author: Jakob Thyrring
Author: Mikael K Sejr
Author: Elizabeth M Harper

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