Variation in the effects of ocean acidification on shell growth and strength in two intertidal gastropods

Barclay, Kristina M.; Gaylord, Brian; Jellison, Brittany M.; Shukla, Priya; Sanford, Eric; Leighton, Lindsey R.

doi:10.3354/meps13056

Cited by 32 publications

(14 citation statements)

References 47 publications

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“…This is also supported by the unchanged expression and methylation of key biomineralization genes such as carbonic anhydrases, tyrosinases (except one putative tyrosinase3) and alkaline phosphatases (Li, Liu, et al, 2016; Miyamoto et al, 1996, 2005; Zhang et al, 2006). Shell growth is often found to be affected under OA in molluscan species, to quote a few examples: clams Chamelea gallina (Bressan et al, 2014), snail Tegula funebralis (Barclay et al, 2019) and oysters C. gigas (De Wit et al, 2018). However, shell growth is not affected in all species by OA; some species have unaffected shell growth such as the mussel Mytilus galloprovincialis (Bressan et al, 2014), sea snail Nucella ostrina (Barclay et al, 2019), mussel Mytilus edulis , clam Arctica islandica (Hiebenthal et al, 2013) and abalone Concholepas concholepas (Manríquez et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Oyster biomineralization under ocean acidification: From genes to shell

Rajan

Yuan

et al. 2021

Global Change Biology

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Biomineralization is one of the key processes that is notably affected in marine calcifiers such as oysters under ocean acidification (OA). Understanding molecular changes in the biomineralization process under OA and its heritability, therefore, is key to developing conservation strategies for protecting ecologically and economically important oyster species. To do this, in this study, we have explicitly chosen the tissue involved in biomineralization (mantle) of an estuarine commercial oyster species, Crassostrea hongkongensis. The primary aim of this study is to understand the influence of DNA methylation over gene expression of mantle tissue under decreased ~pH 7.4, a proxy of OA, and to extrapolate if these molecular changes can be observed in the product of biomineralization—the shell. We grew early juvenile C. hongkongensis, under decreased ~pH 7.4 and control ~pH 8.0 over 4.5 months and studied OA‐induced DNA methylation and gene expression patterns along with shell properties such as microstructure, crystal orientation and hardness. The population of oysters used in this study was found to be moderately resilient to OA at the end of the experiment. The expression of key biomineralization‐related genes such as carbonic anhydrase and alkaline phosphatase remained unaffected; thus, the mechanical properties of the shell (shell growth rate, hardness and crystal orientation) were also maintained without any significant difference between control and OA conditions with signs of severe dissolution. In addition, this study makes three major conclusions: (1) higher expression of Ca2+ binding/signalling‐related genes in the mantle plays a key role in maintaining biomineralization under OA; (2) DNA methylation changes occur in response to OA; however, these methylation changes do not directly control gene expression; and (3) OA would be more of a ‘dissolution problem’ rather than a ‘biomineralization problem’ for resilient species that maintain calcification rate with normal shell growth and mechanical properties.

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Section: Discussionmentioning

confidence: 99%

Oyster biomineralization under ocean acidification: From genes to shell

Rajan

Yuan

et al. 2021

Global Change Biology

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“…Paired work on two common gastropods found in intertidal habitats along the US west coast highlights disparate responses amongst taxa. In a long-term exposure of the herbivorous gastropod, Tegula funebralis (the black turban snail), and a predatory counterpart, Nucella ostrina (the striped dogwhelk), to OA, Barclay et al. (2019) demonstrate both notably different changes between these two taxa in how shell properties shifted under altered seawater chemistry, as well as cryptic changes that were not obvious by eye.…”

Section: Interspecific Variation In Biomechanical Responsesmentioning

confidence: 96%

“…The black-dotted line at 200 N indicates conservative crushing forces exerted by adult crabs of C. productus (Taylor, 2000). Modified from Barclay et al. (2019).…”

Section: Interspecific Variation In Biomechanical Responsesmentioning

confidence: 99%

“…Still, because mineralogical responses to shifts in temperature or OA may not be visually obvious, and yet have the capacity to affect shell integrity (and therefore resistance to predation), explicit examinations of shell and skeletal structural properties remain important. Indeed, had Barclay et al. (2019) not included a mechanical test of shell strength, one might have assumed that Nucella ’s anti-predator defenses were unaffected by OA, given that its macroscopic patterns of growth did not change in low-pH seawater.…”

Section: Interspecific Variation In Biomechanical Responsesmentioning

confidence: 99%

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Ocean change within shoreline communities: from biomechanics to behaviour and beyond

Gaylord

Barclay

Jellison

et al. 2019

Conservation Physiology

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Humans are changing the physical properties of Earth. In marine systems, elevated carbon dioxide concentrations are driving notable shifts in temperature and seawater chemistry. Here, we consider consequences of such perturbations for organism biomechanics and linkages amongst species within communities. In particular, we examine case examples of altered morphologies and material properties, disrupted consumer–prey behaviours, and the potential for modulated positive (i.e. facilitative) interactions amongst taxa, as incurred through increasing ocean acidity and rising temperatures. We focus on intertidal rocky shores of temperate seas as model systems, acknowledging the longstanding role of these communities in deciphering ecological principles. Our survey illustrates the broad capacity for biomechanical and behavioural shifts in organisms to influence the ecology of a transforming world.

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“…However, shell growth of some other species such as Nassarius festivus in Hong Kong was not significantly affected by reduced pH (950 and 1250 µatm for 31 days) (Zhang et al, 2016), thus indicating that sensitivity to ocean acidification is species-specific and needs to be explored in fine detail (Doney et al, 2020). Similarly, shell growth of Nucella ostrina was not affected when pH was reduced by 0.5 units for a period of 6 months, although its shell became 10% weaker under predation cues (Barclay et al, 2019). Temperature as a factor alone has been also proven to affect the formation of mollusc shells, such as in Chamelea gallina that formed lighter, thinner and more porous shells at higher temperatures resulting in reduced shell fracture load (Gizzi et al, 2016).…”

Section: Introductionmentioning

confidence: 96%

Morphological Properties of Gastropod Shells in a Warmer and More Acidic Future Ocean Using 3D Micro-Computed Tomography

2021

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The increased absorption of atmospheric CO2 by the ocean reduces pH and affects the carbonate chemistry of seawater, thus interfering with the shell formation processes of marine calcifiers. The present study aims to examine the effects of ocean acidification and warming on the shell morphological properties of two intertidal gastropod species, Nassarius nitidus and Columbella rustica. The experimental treatments lasted for 3 months and combined a temperature increase of 3°C and a pH reduction of 0.3 units. The selected treatments reflected the high emissions (RCP 8.5) “business as usual” scenario of the Intergovernmental Panel on Climate Change models for eastern Mediterranean. The morphological and architectural properties of the shell, such as density, thickness and porosity were examined using 3D micro-computed tomography, which is a technique giving the advantage of calculating values for the total shell (not only at specific points) and at the same time leaving the shells intact. Nassarius nitidus had a lower shell density and thickness and a higher porosity when the pH was reduced at ambient temperature, but the combination of reduced pH and increased temperature did not have a noticeable effect in comparison to the control. The shell of Columbella rustica was less dense, thinner and more porous under acidic and warm conditions, but when the temperature was increased under ambient pH the shells were thicker and denser than the control. Under low pH and ambient temperature, shells showed no differences compared to the control. The vulnerability of calcareous shells to ocean acidification and warming appears to be variable among species. Plasticity of shell building organisms as an acclimation action toward a continuously changing marine environment needs to be further investigated focusing on species or shell region specific adaptation mechanisms.

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Variation in the effects of ocean acidification on shell growth and strength in two intertidal gastropods

Cited by 32 publications

References 47 publications

Oyster biomineralization under ocean acidification: From genes to shell

Oyster biomineralization under ocean acidification: From genes to shell

Ocean change within shoreline communities: from biomechanics to behaviour and beyond

Morphological Properties of Gastropod Shells in a Warmer and More Acidic Future Ocean Using 3D Micro-Computed Tomography

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