Life cycle and early development of the thecosomatous pteropod Limacina retroversa in the Gulf of Maine, including the effect of elevated CO2 levels

Thabet, Ali A.; Maas, Amy E.; Lawson, Gareth L.; Tarrant, Ann M.

doi:10.1007/s00227-015-2754-1

Cited by 41 publications

(76 citation statements)

References 55 publications

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“…were corroborated in the GoM by observations of egg laying in the lab after seasonal sampling479 Thabet et al, 2015), which documented egg production in all seasons but noted that it was 480 particularly high in April and October.…”

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confidence: 73%

“…Understanding these cycles is important because they can reveal periods that could 123 serve as population "bottlenecks" under future anthropogenically acidified conditions. One 124 potential bottleneck is the life stage when initial biomineralization occurs, as it has been 125 demonstrated to be one of the most sensitive for both pteropods and other molluscan groups 126 (Thabet et al, 2015;Waldbusser et al, 2013;Waldbusser et al, 2015;White et al, 2013). It 127 remains mostly unclear when, and due to what physical factors, L. retroversa spawns in the 128 North Atlantic.…”

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confidence: 99%

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Seasonal variation in physiology and shell condition of the pteropodLimacina retroversain the Gulf of Maine relative to life cycle and carbonate chemistry

Maas

Lawson

Bergan

et al. 2020

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17Natural cycles in the seawater partial pressure of carbon dioxide (CO2) in the Gulf of Maine, 18 which vary from ~250-550 µatm seasonally, provide an opportunity to observe how the life cycle 19 and phenology of the shelled pteropod Limacina retroversa responds to changing food, 20 temperature and carbonate chemistry conditions. Distributional, hydrographic, and physiological 21 sampling suggest that pteropod populations are located in the upper portion of the water column 22 (0-150 m) with a maximum abundance above 50 m, allowing them to generally avoid aragonite 23 undersaturation. Gene expression and shell condition measurements show, however, that the 24 population already experiences biomineralization stress in the winter months even when 25 aragonite is slightly oversaturated, reinforcing the usefulness of this organism as a bio-indicator 26 for pelagic ecosystem response to ocean acidification. There appear to be two reproductive 27 events per year with one pulse timed to coincide with the spring bloom, the period with highest 28 respiration rate, fluorescence, and pH, and a second more extended pulse in the late summer and 29 fall. During the fall there is evidence of lipid storage for overwintering, allowing the second 30 generation to survive the period of low food and aragonite saturation state. Based on these 31 observations we predict that in the future pteropods will likely be most vulnerable to changing 32 CO2 regionally during the fall reproductive event when CO2 concentration already naturally rises 33 and there is the added stress of generating lipid stores. 34 73 patchy high abundances of small individuals appearing in the fall that persisted through the 74 spring. Redfield noted a correlation between the seasonal progression of the location of L. 75 retroversa patches and major surface currents, and based on the bimodal and non-linear growth 76 of their size frequency distributions he suggested that the population is maintained by pulses of 77 lateral advection from an open ocean source. The species has been reported to feed on detritus, 78 diatoms and dinoflagellates (Lalli & Gilmer, 1989; Morton, 1954) with the capacity to ingest 79 large quantities of phytoplankton (~4000 ng of chl a pigment individual -1 day -1 , Bernard & 80 Froneman, 2009). Limacina retroversa is eaten by a variety of fish (Bigelow, 1924; Lebour, 81 1932; Suca et al., 2018) and can become such a prevalent component of the diet of mackerel and 82herring that they can act as a vector for toxins and non-palatable compounds, negatively 83 affecting fisheries (Ackman et al., 1972;Foster et al., 2012;White, 1977). They also appear to 84 play a role in modifying the alkalinity budget and carbonate chemistry in deep basins in the Gulf 85 of Maine (Wang et al., 2017b). 86 The local ecological importance of L. retroversa, its natural seasonal exposure to strong variation 87 in CO2 levels, and the fact that it is widely distributed in temperate portions of the Atlantic open 88 ocean position the species as a valuable mod...

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confidence: 73%

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confidence: 99%

Seasonal variation in physiology and shell condition of the pteropodLimacina retroversain the Gulf of Maine relative to life cycle and carbonate chemistry

Maas

Lawson

Bergan

et al. 2020

Preprint

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“…Larval growth impairment showed a significant difference in the magnitude of response in comparison with adults and was one of the most sensitive to ar . Of those studies measuring ar growth impacts, data could only be obtained for the study by Manno et al (2012) but not from Thabet et al (2015) and Comeau et al (2010b) because LOE could not be extracted, or the uncertainty was too great, yet both studies demonstrated a significant decrease in larval growth and developmental delay. The derived LOE based on Manno et al (2012) was ar = 1.15 for 7 days.…”

Section: Growth Reductionmentioning

confidence: 99%

Systematic Review and Meta-Analysis Toward Synthesis of Thresholds of Ocean Acidification Impacts on Calcifying Pteropods and Interactions With Warming

et al. 2019

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Interpreting the vulnerability of pelagic calcifiers to ocean acidification (OA) is enhanced by an understanding of their critical thresholds and how these thresholds are modified by other climate change stressors (e.g., warming). To address this need, we undertook a three-part data synthesis for pteropods, one of the calcifying zooplankton group. We conducted the first meta-analysis and threshold analysis of literature characterizing pteropod responses to OA and warming by synthetizing dataset comprising of 2,097 datapoints. Meta-analysis revealed the extent to which responses among studies conducted on differing life stages and disparate geographies could be integrated into a common analysis. The results demonstrated reduced calcification, growth, development, and survival to OA with increased magnitude of sensitivity in the early life stages, under prolonged duration, and with the concurrent exposure of OA and warming, but not species-specific sensitivity. Second, breakpoint analyses identified OA thresholds for several endpoints: dissolution (mild and severe), calcification, egg development, shell growth, and survival. Finally, consensus by a panel of pteropod experts was used to verify thresholds and assign confidence scores for five endpoints with a sufficient signal: noise ratio to develop life-stage specific, duration-dependent thresholds. The range of aragonite saturation state from 1.5-0.9 provides a risk range from early warning to lethal impacts, thus providing a rigorous basis for vulnerability assessments to guide climate change management responses, including an evaluation of the efficacy of local pollution management. In addition, meta-analyses with OA, and warming shows increased vulnerability in two pteropod processes, i.e., shell dissolution and survival, and thus pointing toward increased threshold sensitivity under combined stressor effect.

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“…Examinations of seasonal changes in size distributions and gonad development have suggested L. retroversa spawning peaks in the GoME in May, but with active reproduction continuing into the fall [Hsiao, 1939]. A recent laboratory study of L. retroversa reproductive and developmental biology also found that this species is capable of spawning multiple times per year, and suggest that, in this region, individuals likely live 6 months [Thabet et al, 2015]. Abundances of small individuals were very high in May 2013 and April-June 2015, indicative of a strong springtime spawning event, presumably associated with the spring bloom.…”

Section: Pteropod Abundancementioning

confidence: 99%

“…Alternatively, it may represent an indirect association between pteropod abundance and Journal of Geophysical Research: Oceans 10.1002/2016JC012373 X-Ar mediated by synchrony between the pteropod life cycle and senescence after reproductive events with times of high productivity (i.e., spring and fall blooms) at which time enhanced DIC serves to decrease X-Ar. Related to this notion, it is possible that the life cycle of L. retroversa in the region is optimized such that large reproductive adults are most abundant during periods when their larvae have a better chance of passing the initial calcification bottleneck [Thabet et al, 2015;Waldbusser et al, 2013Waldbusser et al, , 2015, and this causes successful cohorts to appear in large numbers during periods when X-Ar is high (as well as food abundant). If so, it will become useful to consider how the predicted changes in saturation state might influence their future spawning success.…”

Section: Pteropod Abundancementioning

confidence: 99%

Seasonal controls of aragonite saturation states in the Gulf of Maine

et al. 2017

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The Gulf of Maine (GoME) is a shelf region especially vulnerable to ocean acidification (OA) due to natural conditions of low pH and aragonite saturation states (Ω‐Ar). This study is the first to assess the major oceanic processes controlling seasonal variability of the carbonate system and its linkages with pteropod abundance in Wilkinson Basin in the GoME. Two years of seasonal sampling cruises suggest that water‐column carbonate chemistry in the region undergoes a seasonal cycle, wherein the annual cycle of stratification‐overturn, primary production, respiration‐remineralization and mixing all play important roles, at distinct spatiotemporal scales. Surface production was tightly coupled with remineralization in the benthic nepheloid layer during high production seasons, which results in occasional aragonite undersaturation. From spring to summer, carbonate chemistry in the surface across Wilkinson Basin reflects a transition from a production‐respiration balanced system to a net autotropic system. Mean water‐column Ω‐Ar and abundance of large thecosomatous pteropods show some correlation, although patchiness and discrete cohort reproductive success likely also influence their abundance. Overall, photosynthesis‐respiration is the primary driving force controlling Ω‐Ar variability during the spring‐to‐summer transition as well as over the seasonal cycle. However, calcium carbonate (CaCO3) dissolution appears to occur near bottom in fall and winter when bottom water Ω‐Ar is generally low but slightly above 1. This is accompanied by a decrease in pteropod abundance that is consistent with previous CaCO3 flux trap measurements. The region might experience persistent subsurface aragonite undersaturation in 30–40 years under continued ocean acidification.

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Life cycle and early development of the thecosomatous pteropod Limacina retroversa in the Gulf of Maine, including the effect of elevated CO2 levels

Cited by 41 publications

References 55 publications

Seasonal variation in physiology and shell condition of the pteropodLimacina retroversain the Gulf of Maine relative to life cycle and carbonate chemistry

Seasonal variation in physiology and shell condition of the pteropodLimacina retroversain the Gulf of Maine relative to life cycle and carbonate chemistry

Systematic Review and Meta-Analysis Toward Synthesis of Thresholds of Ocean Acidification Impacts on Calcifying Pteropods and Interactions With Warming

Seasonal controls of aragonite saturation states in the Gulf of Maine

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