Brooding strategy in fluctuating salinity environments: oxygen availability in the pallial cavity and metabolic stress in females and offspring in the Chilean oyster Ostrea chilensis

Abstract

Organisms that encounter stressful situations in nature often cope using behavioral (e.g., avoidance) or physiological tactics. In sessile mollusks, the only available behavioral option in dealing with salinity stress is to "clam up", isolating their tissues from the environment. Though effective in the short term, prolonged isolation can have detrimental physiological consequences, particularly for females brooding embryos in a mantle cavity that is isolated from the external environment. In the Quempillén estuary, the Chilean oyster, Ostrea chilensis, spent nearly one-third of its brooding season at salinities low enough to cause female isolation. When females thus isolated themselves, the dissolved oxygen in their mantle cavity fluid dropped to hypoxic levels within 10 min. In females that were brooding embryos, this depletion of oxygen was not uniform: oxygen was depleted more quickly in the palp region (where embryos accumulate) than in the inhalant region. Additionally, oxygen was reduced even more quickly in the palp region when females were brooding late-stage embryos, which consumed oxygen significantly more quickly than embryos in earlier developmental stages. Finally, O. chilensis used anaerobic metabolism to cope with the hypoxia induced by isolation, as lactate accumulated in the tissues of both females (brooding > non-brooding) and embryos (late stage > early stage). Our findings demonstrate the trade-off between an adaptive avoidance behavior (clamming up) and the potentially detrimental consequences brought on by such a behavior (hypoxia). Cycling of embryos throughout the mantle cavity by deliberate female pumping keeps them from accumulating in the area between the palps, forestalling the creation of hypoxic conditions there. In addition, the capacity for anaerobic metabolism by both females and their embryos should help them tolerate the low oxygen levels that do eventually arise when the pallial cavity is isolated from the surrounding environment during long periods of reduced ambient salinity.

Slow shell building, a possible trait for resistance to the effects of acute ocean acidification

“…Recent experiments and analyses indicate that brooding in calcifiers and non‐calcifying species appears to convey some fitness to ocean acidification (Noisette et al ; Lucey et al ); therefore slower calcification may only be one trait of several that provides brooded oyster larvae resistance to acute OA effects during PDI development. Conversely, brooding may also create adverse conditions for larvae; for example, extended shell closure due to stress in the oyster Ostrea chilensis during brooding can generate low pH after several hours (Chaparro et al ; Segura et al ). During normal ventilation, however, seawater is rapidly flushed through the brood chamber suggesting there is little time for respiratory carbon dioxide accumulation (Chaparro et al ; Mardones‐Toledo et al ) and salinity events that cause O. chilensis to “clam up,” in Chile are uncommon during the brooding period (Segura et al ).…”

Life History Traits Conferring Larval Resistance against Ocean Acidification: The Case of Brooding Oysters of the Genus Ostrea

“…to have little to no direct effect of the brood chamber pH, oxygen, or ammonium concentration (Chaparro et al 2008, Chaparro et al 2009a, 2009b. More recently, Segura et al (2015) demonstrated that as larvae mature and their oxygen demand increases, late-stage larvae can greatly reduce the oxygen availability within the brood chamber, contributing to brood chamber acidification. Similar relationships between chamber oxygen depletion and development of brooded young have been observed among other marine invertebrate species (see review by Pechenick 1999).…”

“…It has been hypothesized that circulation of brooded larvae by means of the female countercurrent increases the access of larvae to oxygenated areas of the brood chamber (i.e., posterior, inhalant opening) (Chaparro et al 1993, Mardones-Toledo et al 2015. Indeed, older larvae may rapidly deplete the maternal palps of oxygen when mothers isolate their brood chamber (Segura et al 2015); therefore, circulation and other maternal care behaviors may be increasingly important as larva develop. Although mothers do not increase feeding or pumping rate to compensate for the growing demands of broods as they develop (Chaparro & Thompson 1998), these and other parental behaviors (e.g., mucus coating and larval circulation) require further exploration to better understand maternal care under OA stress.…”

Growing Safe: Acute Size Escape from Desiccation in Juvenile Crepipatella peruviana (Mollusca: Gastropoda)

“…However, this isolation response also restricts access to oxygen by cutting off exposure to air. Thus, when clamped, molluscs first deplete the oxygen stored in their mantle cavity water and then must either switch to anaerobic respiration (Segura et al, 2015(Segura et al, , 2016 or periodically open their shells to exchange oxygen and carbon dioxide via aerobic res-piration, despite the water loss that accompanies such behavior .…”