This could be due to multiple biological processes such as cellular and metabolic processes, biological regulation, and organization and biogenesis that must be fulfilled in this larval stage, as has been demonstrated at the transcriptomic level in early larvae of the mussel M.
Interestingly, ATP supplying efficiency by mitochondria as indicated by ETS:CS ratio decreased linearly with larval development, attaining the lowest level at the premetamorphic pediveliger stage, and increasing markedly in early juveniles. Altogether, all these data reveal that metabolic demand and metabolic capacity vary significantly throughout A. Herein, we evidence that veliger larvae compared with other developmental stages, are inefficient in terms of energy production vs.
Immune response is an energetically expensive process because it implies the recruitment and activity of specialized cells namely hemocytes in mollusks , and the production and action of specific molecules involved in sensing and opsonizing foreign particles as well as in antimicrobial functions.
These studies were, respectively, carried out in Chlamys farreri and A. The present study constitutes, to the knowledge of the authors, the first evaluation of the metabolic cost induced by the exposure of a pathogenic bacterium in the different stages of the early development of A. Respiration rates did not vary in the course of the first hours of bacterial exposure and followed the pattern of undisturbed larvae and early juveniles.
Therefore, independent of the bacterial challenge, D-veliger maintained the highest RR at individual and mass-specific levels , followed by veliger, pediveliger, and juveniles at mass-specific levels.
These responses are expected under stress conditions here a pathogen exposure , aiming to produce the energy required to fuel the necessary pathways to counteract the deleterious effects of such stresses Kadenbach These results suggest that both, trochophore and D-veliger would have the necessary energy to support immune response. These results suggest that both veliger and pediveliger to a lesser extent stages would have a limited energy supply to support immune responses.
These results suggest that early juveniles are a less energy-demanding stage at the basal level, are less perturbed by the presence of the bacteria, and would have a good capacity to energetically fuel the immune response.
The present findings are partially consistent with the expression pattern of immune genes observed in the same developmental stages of A. This previous study showed that early juveniles overexpress a Toll-like receptor ApTLR in response to bacterial challenge.
The latter also showed a similar overexpression of two antimicrobial effectors, a ferritin Apfer1 and a big defensin antimicrobial peptide ApBD1 in pediveliger and early juveniles.
However, trochophore and D-veliger, which appear to be better prepared to support immune response in terms of energy supply, did not overexpress immune genes after Vibrio exposure Rojas et al. Thus, the immune response would be likely limited by the level of maturation of the immune system in these early stages.
However, parental transfer of some immune effectors has been suggested to occur, acting as protection during these early stages Yue et al. It has been indeed suggested in the Mediterranean mussel M. Moreover, present results suggest that the lack of induction of immune molecules after pathogen exposure might be limited by a low capacity to supply the necessary energy.
This would potentially explain why pathogenic outbreaks occur or affect more often during the veliger larval stage Miranda et al. We thus suggest that a potential energetic compromise between the morpho-anatomical changes and the immune response capacity exists during this larval stage, but a more in-depth study would be necessary to elucidate this tradeoff.
The traditional farming methods of the scallop A. This point is especially relevant now that all evidence collected in the frame of the present study allows us to infer that the veliger stage would have lower energy efficiency along with the incapacity to express immune-related genes Rojas et al.
This would explain why this larval stage shows the highest mortality rates in commercial crops i. With these results, we propose that technical improvements in farming, that is, considering engineering or administration of immunomodulators, should aim to overpass this critical point aiming to improve the energy condition of the veliger larvae so that they may achieve a higher settlement index and a lower vulnerability to pathogen infections.
The raw data supporting the conclusions of this article will be made available by the authors upon request. IR: methodology, validation, investigation, visualization, data curation, formal analysis, writing the original draft, reviewing, and editing. GR-I: methodology, validation, investigation, visualization, resources, reviewing, and editing.
CC: software, reviewing and editing, project administration, and funding acquisition. KJ: investigation, visualization, reviewing, and editing. EF-O: resources, reviewing, and editing. PS: conceptualization, reviewing and editing, and funding acquisition. KB: conceptualization, methodology, investigation, supervision, resources, writing the original draft, reviewing, editing, project administration, and funding acquisition.
All authors contributed to the article and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers.
Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. The authors would like to thank Laboratorio Central de Cultivos Marinos of the UCN for providing the infrastructure for carrying out the experiments, especially German Lira and Daniel Gonzalez for animal maintenance. Balseiro, P.
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