Tolerance to hypometabolism and arousal induced by hibernation in the apple snail Pomacea canaliculata (Caenogastropoda, Ampullariidae)

Giraud-Billoud, Maximiliano; Castro-Vázquez, Alfredo; Campoy-Diaz, Alejandra D.; Giuffrida, Pablo M.; Vega, Israel A.

doi:10.1016/j.cbpb.2017.12.015

Cited by 23 publications

(25 citation statements)

References 53 publications

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“…The identified enzyme list included Cu-Zn SOD and catalase-and peroxidase-like molecules, which may contribute to the maintenance of redox equilibrium. This is in line with observations that correlate the ampulla with the oxidative stress response during environmentally driven challenges [39,99]. The presence of immune-related proteins as well as of enzymes committed to the maintenance of redox equilibrium would suggest that the ampulla is potentially involved in facing oxidative stress in different occasions, e.g., during aestivation/hibernation arousal [38,39] or as a consequence of an immune challenge.…”

Section: Discussionsupporting

confidence: 89%

“…The hypothesis that the ampulla might serve as a haemocytic reservoir [14] remained unproven. Biochemical and ultrastructural evidence also suggested the involvement of the ampulla, together with other organs, in the anti-oxidant stress response associated with the aestivation/hibernation processes [38,39]. In these respects, the oxidative stress observed in the apple snail mimics to some extent the oxidative burst that is associated with ischemia-reperfusion injury [40], and this capacity of resisting a systemic oxidative burst could also represent a resource in case of other stressors, e.g., exposure to a biocide or an immune challenge.…”

Section: Introductionmentioning

confidence: 99%

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Pomacea canaliculata Ampullar Proteome: A Nematode-Based Bio-Pesticide Induces Changes in Metabolic and Stress-Related Pathways

Boraldi

Lofaro

Bergamini

et al. 2021

Biology

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Pomacea canaliculata is a freshwater gastropod known for being both a highly invasive species and one of the possible intermediate hosts of the mammalian parasite Angiostrongylus cantonensis. With the aim of providing new information concerning P. canaliculata biology and adaptability, the first proteome of the ampulla, i.e., a small organ associated with the circulatory system and known as a reservoir of nitrogen-containing compounds, was obtained. The ampullar proteome was derived from ampullae of control snails or after exposure to a nematode-based molluscicide, known for killing snails in a dose- and temperature-dependent fashion. Proteome analysis revealed that the composition of connective ampulla walls, cell metabolism and oxidative stress response were affected by the bio-pesticide. Ultrastructural investigations have highlighted the presence of rhogocytes within the ampullar walls, as it has been reported for other organs containing nitrogen storage tissue. Collected data suggested that the ampulla may belong to a network of organs involved in controlling and facing oxidative stress in different situations. The response against the nematode-based molluscicide recalled the response set up during early arousal after aestivation and hibernation, thus encouraging the hypothesis that metabolic pathways and antioxidant defences promoting amphibiousness could also prove useful in facing other challenges stimulating an oxidative stress response, e.g., immune challenges or biocide exposure. Targeting the oxidative stress resistance of P. canaliculata may prove helpful for increasing its susceptibility to bio-pesticides and may help the sustainable control of this pest’s diffusion.

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Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Pomacea canaliculata Ampullar Proteome: A Nematode-Based Bio-Pesticide Induces Changes in Metabolic and Stress-Related Pathways

Boraldi

Lofaro

Bergamini

et al. 2021

Biology

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“…The close association of rhogocytes with storage cells has been intriguing to us, because we have occasionally observed rhogocytes in other tissues too, such as the aortic ampulla and the perivascular tissue of the digestive gland, and all of these organs also contain storage cells (Giraud-Billoud et al, 2008). In P. canaliculata, there is substantial evidence for a role of the accumulated uric acid in counteracting the oxidative burst that accompanies the arousal from estivation and hibernation (Giraud-Billoud et al, 2011;Giraud-Billoud et al, 2018;Giraud-Billoud et al, 2013), while Mueck, Deaton & Lee (2020a) have proposed a role of the calcareous crystalloids in buffering the lowering of pH that occurs during estivation in P. maculata.…”

Section: The Respiratory Lamina: How It Can Be Both Thin and Strongmentioning

confidence: 93%

“…Only the first one may have a functional role in respiration, because its contraction or relaxation may affect the volume of the lung cavity. The second one has, at least in P. canaliculata, a role in the antioxidant protection during arousal from estivation (Giraud-Billoud et al, 2011;Giraud-Billoud et al, 2013) and hibernation (Giraud-Billoud et al, 2018).…”

Section: The Respiratory Lamina: How It Can Be Both Thin and Strongmentioning

confidence: 99%

Morphological grounds for the obligate aerial respiration of an aquatic snail: functional and evolutionary perspectives

Rodriguez

Prieto

Vega

et al. 2021

PeerJ

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The freshwater caenogastropod family Ampullariidae is emerging as a model for a variety of studies, among them, the evolution of terrestriality. A common character of the family is that all its members bear a lung while retaining the ancestral gill. This ensures that many ampullariids are able to inhabit poorly oxygenated waters, to bury in the mud during estivation, and to temporarily leave the water, in some species for oviposition. To these characters Pomacea canaliculata (Caenogastropoda, Ampullariidae) adds that is an obligate air-breather. In a recent paper, we showed the gill epithelium of P. canaliculata has a set of characteristics that suggest its role for oxygen uptake may be less significant than its role in ionic/osmotic regulation and immunity. We complement here our morphological investigation on the respiratory organs of P. canaliculata by studying the lung of this species at the anatomical (3D reconstructions of the blood system and nerve supply), histological and ultrastructural levels. The circulation of the gill and the lung are interconnected so that the effluence of blood from the gill goes to the lung where it completes oxygenation. Besides that, we found the lung cavity is lined by a pavement epithelium that encloses an anastomosing network of small blood spaces resting over a fibromuscular layer, which altogether form the respiratory lamina. The pavement cells form a blood-gas barrier that is 80–150 nm thick and thus fulfils the requirements for an efficient gas exchanger. Tufts of ciliary cells, together with some microvillar and secretory cells, are interspersed in the respiratory lamina. Rhogocytes, which have been proposed to partake in metal depuration and in the synthesis of hemocyanin in other gastropods, were found below the respiratory lamina, in close association with the storage cell tissue. In light of these findings, we discuss the functional role of the lung in P. canaliculata and compare it with that of other gastropods. Finally, we point to some similarities in the pattern of the evolution of air dependence in this family.

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“…The gill helps to generate the water current across the mantle cavity and, in Pomacea canaliculata , may have an important role in ionic/osmotic and acid–base regulation and immune defense ( Taylor & Andrews, 1987 ; Rodriguez et al, 2019 ). The lung is used as a flotation device ( Bavay, 1873 ; Ramanan, 1903 ; Hylton Scott, 1957 ; McClary, 1965 ; Burky & Burky, 1977 ; Berthold, 1991 ) and, in P. canaliculata , it is involved in immune defense ( Rodriguez et al, 2018 ), hematopoiesis ( Rodriguez et al, 2020 ; Rodriguez et al, 2021 ), and storage of urates ( Giraud-Billoud et al, 2008 ), which are key components in the antioxidant-defense mechanism during arousal after estivation ( Giraud-Billoud et al, 2013 ) and hibernation ( Giraud-Billoud et al, 2018 ). It has been reported that the lung of Pomacea maculata accumulates calcium carbonate that may buffer the lowering of pH during estivation ( Mueck, Deaton & Lee, 2020b ).…”

Section: Introductionmentioning

confidence: 99%

Caution ahead: reassessing the functional morphology of the respiratory organs in amphibious snails

Prieto

2021

PeerJ

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After a long hiatus, interest in the morphology of the respiratory organs in apple snails (Ampullariidae, Caenogastropoda) and its functional and evolutionary bearings is making a comeback. The variability in the morphology of the gill and lung and its link to different lifestyles and patterns of air dependency within the Ampullariidae make research on the morphology of the respiratory organs particularly suitable for approaching the evolution of terrestriality in animals. Additionally, morphology is a valuable source of hypotheses regarding the several functions the ampullariid respiratory organs have besides respiration. However, this is an underexplored field that only recently has incorporated ultrastructural and three-dimension visualization tools and in which more research is much needed, particularly, comparisons between species representing the diversity within the Ampullariidae. In this paper, I examine Mueck, Deaton & Lee’s (2020a) assessment of the morphology of the gill and lung of Pomacea maculata and compare it with earlier and contemporary studies on other ampullariid species. I show that Mueck, Deaton & Lee’s paper combines significant morphological misinterpretations, conceptual and terminological mistakes, and crucial literature omissions. I also reinterpret their results and point to the similarities and differences between them and available data on other ampullariids.

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Tolerance to hypometabolism and arousal induced by hibernation in the apple snail Pomacea canaliculata (Caenogastropoda, Ampullariidae)

Cited by 23 publications

References 53 publications

Pomacea canaliculata Ampullar Proteome: A Nematode-Based Bio-Pesticide Induces Changes in Metabolic and Stress-Related Pathways

Pomacea canaliculata Ampullar Proteome: A Nematode-Based Bio-Pesticide Induces Changes in Metabolic and Stress-Related Pathways

Morphological grounds for the obligate aerial respiration of an aquatic snail: functional and evolutionary perspectives

Caution ahead: reassessing the functional morphology of the respiratory organs in amphibious snails

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