Tolerant Larvae and Sensitive Juveniles: Integrating Metabolomics and Whole-Organism Responses to Define Life-Stage Specific Sensitivity to Ocean Acidification in the American Lobster.

Fanny Noisette,Kayla Menu-Courey,Piero Calosi,Dounia Daoud,Diana Madeira,Kumiko Azetsu-Scott,Mathilde Chemel,Helen Gurney-Smith,Sarah Piedalue

doi:10.3390/metabo11090584

Abstract

Bentho-pelagic life cycles are the dominant reproductive strategy in marine invertebrates, providing great dispersal ability, access to different resources, and the opportunity to settle in suitable habitats upon the trigger of environmental cues at key developmental moments. However, free-dispersing larvae can be highly sensitive to environmental changes. Among these, the magnitude and the occurrence of elevated carbon dioxide (CO2) concentrations in oceanic habitats is predicted to exacerbate over the next decades, particularly in coastal areas, reaching levels beyond those historically experienced by most marine organisms. Here, we aimed to determine the sensitivity to elevated pCO2 of successive life stages of a marine invertebrate species with a bentho-pelagic life cycle, exposed continuously during its early ontogeny, whilst providing in-depth insights on their metabolic responses. We selected, as an ideal study species, the American lobster Homarus americanus, and investigated life history traits, whole-organism physiology, and metabolomic fingerprints from larval stage I to juvenile stage V exposed to different pCO2 levels. Current and future ocean acidification scenarios were tested, as well as extreme high pCO2/low pH conditions that are predicted to occur in coastal benthic habitats and with leakages from underwater carbon capture storage (CCS) sites. Larvae demonstrated greater tolerance to elevated pCO2, showing no significant changes in survival, developmental time, morphology, and mineralisation, although they underwent intense metabolomic reprogramming. Conversely, juveniles showed the inverse pattern, with a reduction in survival and an increase in development time at the highest pCO2 levels tested, with no indication of metabolomic reprogramming. Metabolomic sensitivity to elevated pCO2 increased until metamorphosis (between larval and juvenile stages) and decreased afterward, suggesting this transition as a metabolic keystone for marine invertebrates with complex life cycles.

Highlights

Bentho-pelagic life cycles are the dominant reproductive strategy in the oceans, as they are found in more than 75% of known marine invertebrate species [1]
For body size, from stage I to stage V (i) mean body size increased progressively from 4.72 ± 0.05 to 9.38 ± 0.12 mm, (ii) mean cephalothorax length increased from 1.93 ± 0.03 to 4.57 ± 0.06 mm, and (iii) mean abdomen size increased from
Our study comprehensively integrates the investigation of life history, mineralisation, and metabolic and metabolomic responses to a broad seawater pressure of CO2 (pCO2) gradient across multiple early ontogenetic stages, in an ecological and economic important marine invertebrate species with a bentho-pelagic life cycle, the American lobster Homarus americanus

Summary

Introduction

Bentho-pelagic life cycles are the dominant reproductive strategy in the oceans, as they are found in more than 75% of known marine invertebrate species [1]. Complex life cycles are punctuated by critical junctures along the ontogenetic trajectory, beginning at hatching when larvae are released in the water column, continuing with metamorphosis when larvae transform into post-larvae and reach the juvenile stages when they return to the sea floor [2]. These junctures represent bottlenecks, or biological filters, that reduce recruitment to the adult population [3]. Homeostatic and regulatory functions develop throughout ontogeny and, as a consequence, early life stages are overall considered to be more sensitive to environmental changes when compared to later life stages [6,7,8]

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