Upwelling as a stressor event during embryonic development: Consequences for encapsulated and early juvenile stages of the marine gastropod Acanthina monodon.

Upwelling phenomena alter the physical and chemical parameters of the sea's subsurface waters, producing low levels of temperature, pH and dissolved oxygen, which can seriously impact the early developmental stages of marine organisms. To understand how upwelling can affect the encapsulated development of the gastropod Acanthina monodon, capsules containing embryos at different stages of development (initial, intermediate and advanced) were exposed to upwelling conditions (pH = 7.6; O2 = 3 mg L-1; T° = 9 °C) for a period of 7 days. Effects of treatment were determined by estimating parameters such as time to hatching, number of hatchlings per capsule, percentage of individuals with incomplete development, and shell parameters such as shell shape and size, shell strength, and the percentage of the organic/inorganic content. We found no significant impacts on hatching time, number of hatchlings per capsule, or percentage of incomplete development in either the presence or absence of upwelling, regardless of developmental stage. On the other hand, latent effects on encapsulated stages of A. monodon were detected in embryos that had been exposed to upwelling stress in the initial embryonic stage. The juveniles from this treatment hatched at smaller sizes and with higher organic content in their shells, resulting in a higher resistance to cracking 30 days after hatching, due to greater elasticity. Geometric morphometric analysis showed that exposure to upwelling condition induced a change in the morphology of shell growth in all post-hatching juveniles (0-30 days), regardless of embryonic developmental stage at the time of exposure. Thus, more elongated shells (siphonal canal and posterior region) and more globular shells were observed in newly hatched juveniles that had been exposed to the upwelling condition. The neutral or even positive upwelling exposure results suggests that exposure to upwelling events during the encapsulated embryonic phase of A. monodon development might not have major impacts on the future juvenile stages. However, this should be taken with caution in consideration of the increased frequency and intensity of upwelling events predicted for the coming decades.

Embryonic encapsulated development of the gastropod Acanthina monodon is impacted by future environmental changes of temperature and pCO2.

Egg capsules of the gastropod Acanthina monodon were maintained during the entire period of encapsulated development at three temperatures (10, 15, 20 °C) and two pCO2 levels (400, 1200 µatm). Embryos per capsule, size at hatching, time to hatching, embryonic metabolic rates, and the resistance of juveniles to shell breakage were quantified. No embryos maintained at 20 °C developed to hatching. The combination of temperature and pCO2 levels had synergistic effects on hatching time and developmental success, antagonistic effects on number of hatchlings per capsule, resistance to juvenile shell cracking and metabolism, and additive effect on hatching size. Juveniles hatched significantly sooner at 15 °C, independent of the pCO2 level that they had been exposed to, while individuals hatched at significantly smaller sizes if they had been held under 15 °C/1200 µatm rather than at 10 °C/low pCO2. Embryos held at the higher pCO2 had a significantly greater percentage of abnormalities. For capsules maintained at low pCO2 and 15 °C, emerging juveniles had less resistance to shell breakage. Embryonic metabolism was significantly higher at 15 °C than at 10 °C, independent of pCO2 level. The lower metabolism occurred in embryos maintained at the higher pCO2 level. Thus, in this study, temperature was the factor that had the greatest effect on the encapsulated development of A. monodon, increasing the metabolism of the embryos and consequently accelerating development, which was expressed in a shorter intracapsular development time, but with smaller individuals at hatching and a lower resistance of their shells to breakage. On the other hand, the high pCO2 level suppressed metabolism, prolonged intracapsular development, and promoted more incomplete development of the embryos. However, the combination of the two factors can mitigate--to some extent--the adverse effects of both incomplete development and lower resistance to shell breakage.

UV-R mitigation strategies in encapsulated embryos of the intertidal gastropod Acanthina monodon: A way to compensate for lack of parental care.

Intracapsular embryonic development in the intertidal zone exposes embryos to various stress sources characteristic of this environment, including UV-R. They require defensive mechanisms to mitigate its adverse effects. The presence of total carotenoids (TC), and mycosporine-like amino acids (MAAs) was studied in adults, in encapsulated embryos, and in the egg capsule walls of the intertidal gastropod Acanthina monodon. Oxygen consumption rates (OCR) were determined in encapsulated and excapsulated embryos exposed to photosynthetically active radiation (PAR) and PAR + UV-A + UV-B to understand if the capsule wall is a protective structure for encapsulated embryos. The results showed the presence of TC in adult pedal and gonad tissues, and in all encapsulated stages. MAAs were not detected. The physical structure of the capsule wall retained most wavelengths, being particularly efficient in the UV-B range. Excapsulated embryos exposed to PAR + UV-A + UV-B radiation increased its OCR compared to encapsulated embryos, indicating the protective character of the capsule wall.

Long-term effects of contrasting pCO2 levels on the scope for growth in the carnivorous gastropod Concholepas concholepas.

We evaluated the effect of contrasting pCO2 levels: lower (390 µatm), moderate (700 µatm) and extreme (1000 µatm), on the scope for growth of the keystone snail Concholepas concholepas over an exposure period of 6 months. Juvenile snails were collected from rocky intertidal habitats and acclimated for 5 months to those pCO2 levels. Subsequently, three groups of snails were randomly taken (n = 7 for each treatment) and reared for an additional 1 month for each of the three pCO2 levels. Physiological traits related with energy gain and energy expenditure were quantified. The scope for growth index decreased significantly with increases in pCO2, yielding negative values throughout the experimental period for the snails exposed to 1000 µatm pCO2, probably due to the extra energy required to maintain their metabolic functions in balance. This suggests that future climate change scenarios with elevated pCO2 levels could threaten the growth and other basic functions of juvenile snails of this species.

Relationship between over-crowding within egg capsules of the marine gastropod Acanthina monodon and prospects for juvenile success.

Encapsulated development with extraembryonic yolk may lead to competition for nutrients within egg capsules. In this research, different degrees of competition among embryos in subtidal egg capsules of Acanthina monodon resulted in considerable differences in hatching size. For newly hatched juveniles, individuals hatching from less crowded egg capsules showed better survival, larger SL, higher rates of oxygen consumption, and higher rates of food consumption. However, by 28 days after hatching, the largest surviving juveniles were the best-performing individuals, regardless of the initial embryo density within the capsules. In summary, more crowded egg capsules resulted in poorer survival. These findings may help to explain the variability seen in juvenile success in some field populations; much of that variation may reflect stressful experiences that the new recruits have had during the early stages of their encapsulated development.

Energetic trade-offs: Implications for selection between two bivalve prey species by a carnivorous muricid gastropod.

Active predators obtain energy and nutrients from prey through complex processes in which the energy gained must exceed the energy invested in finding and ingesting the prey. In addition, the amount of energy available will vary with the prey that are selected for consumption. The muricid gastropod Acanthina monodon inhabits rocky shores, where it routinely feeds on the mytilids Semimytilus algosus and Perumytilus purpuratus. In this study, S. algosus was highly preferred by the predator (over 90% were eaten) versus P. purpuratus (only 9% were eaten) when offered a mixed diet. The energetic cost of attacking one S. algosus individual was 91 J bivalve-1 while for P. purpuratus it was slightly higher: 95 J bivalve-1. Also, whereas A. monodon required on average 19 h to consume S. algosus, successful attacks on P. purpuratus required about 32% more time (25 h). In addition, a longer resting time was needed by the predator after preying on P. purpuratus before it initiated another attack. Moreover, the active metabolic costs associated with successfully attacking the prey increased 3.2 times over the basal metabolic costs when attacking S. algosus, but only by 2.5 times when attacking P. purpuratus. The calculations associated with preying on each species showed that the energetic gain per unit time likely accounts for the predator's preference for attacking S. algosus, even though predation on both species provided net energy gains for the predator. However, as S. algosus occurs seasonally at our study site, P. purpuratus would probably also be consumed due to its constant availability throughout the whole year.

Respiratory and desiccation constraints during encapsulated intertidal development of the marine gastropod Acanthina monodon.

Acanthina monodon commonly deposits its egg capsules in the intertidal zone. Capsule aerial exposure during low-tide can impact oxygen consumption rates (OCR) of embryos and intracapsular oxygen availability, and expose embryos to desiccation. OCR increased as embryonic development progressed, and was greater when capsules were submerged in seawater than when exposed to air. Oxygen available within the capsule was always less than that available in the immediate external environment, whether capsules were immersed or exposed. The highest internal oxygen concentrations were recorded during periods of air exposure for embryos in more advanced development stages. When exposed to air, capsules lost water the fastest when they contained early embryos, and suffered the highest mortalities following exposure. Collectively, these data suggest that, although encapsulation helps the embryos to develop across wildly fluctuating environmental conditions, the amount of stress the embryos experience will vary depending on their exact positioning within the intertidal zone.

Possible Mechanisms of Hatching from Egg Capsules in the Gastropods Crepipatella dilatata and Crepipatella peruviana, Species with Different Modes of Early Development.

Many invertebrates enclose their embryos within egg capsules, from which the offspring hatch. In marine gastropods that brood their egg capsules, hatching could involve radular activity by the mother or by unhatched stages, increased osmotic concentration of the intracapsular fluid, or production of hatching enzymes. The present research sought to determine whether mechanical action by the brooding female or by the encapsulated embryos was involved in the hatching for two sympatric and closely related species of calyptraeid: Crepipatella dilatata, which exhibits direct development without free-living larvae, and Crepipatella peruviana, which releases free-living veliger larvae. We also considered the role that enzymatic action or osmotic changes in the intracapsular fluid might play in hatching. Using scanning electron micrograph analyses, we found no evidence that the well-developed, pre-hatching juvenile radula of C. dilatata played any role in the hatching process and that the radula of C. peruviana did not even develop until long after hatching; so there was no evidence of radular activity involved in the hatching of either species. For C. peruviana, the intracapsular fluid osmolality was always higher than that of the surrounding seawater, suggesting that there is a strong natural water inflow during development. Moreover, when egg capsules of C. peruviana were exposed to lower ambient salinities, the substantial entry of water correlated well with high percentages of hatching, particularly for egg capsules containing advanced veligers, suggesting that an osmotic mechanism may be involved in the hatching process of this species. In contrast, hatching in C. dilatata appeared to be enzymatically mediated.

Volcanic ash in the water column: Physiological impact on the suspension-feeding bivalve Mytilus chilensis.

Ashes settling into the sea from volcanic explosions expose suspension-feeding species to reduced seston quality. Adults and juveniles of the mussel Mytilus chilensis were exposed for 15days to the phytoplankton Isochrysis galbana together with various concentrations of ashes. We then quantified impact on survival and physiology. Although no individuals died during the experiment, by the end of the study clearance rates and oxygen consumption rates had decreased substantially, and tissue weight of mussels exposed to the highest ash concentrations declined substantially. Gills showed no physical damage, but did show abundant mucus secretion in response to ash particles. Moreover, as the relative proportions of microalgae to ash in the diet decreased, individuals showed increasing preferential ingestion of microalgal particles. Increased ash content in the diet altered physiological rates and activated distinct particle selection with a high production of pseudofeces and high energy costs, with potential long-term consequences.

Embryonic velar structure and function of two sibling species of Crepidula with different modes of development.

The structure and function of the embryonic velum of two closely related species of Crepidula with different modes of development are examined. The velum of C. dilatata, a direct developer whose embryos feed on nurse eggs, does not differ substantially from the velum of C. fecunda, a species with planktotrophic larvae. Although velar ciliation develops earlier in embryos of C. dilatata, embryos of both species were able to feed on small particles, using the opposed-band ciliary mechanism. However, the embryos of C. dilatata lose this ability as they grow. The embryos of C. dilatata were not able to swim, whereas those of C. fecunda swam consistently in vials of seawater. This difference in swimming ability is probably due to differences in velum-body size allometry between the two species.

The Velar Ciliature in the Brooded Larva of the Chilean Oyster Ostrea chilensis (Philippi, 1845).

The Chilean oyster (Ostrea chilensis) broods its offspring almost to the settlement stage (about 8 weeks). Larvae are maintained inside the infrabranchial chamber of the female. Samples from all embryo and larval developmental stages were obtained from mantle cavities of brooding females and analyzed by scanning electron microscopy, with particular attention to the velar structures. All embryos and the earliest veliger stages of O. chilensis are devoid of cilia. Cilia first appear when shell length reaches 290-300 {mu}m, and the first cilia to grow on the velum form the outer preoral cilia. In larvae 340 {mu}m long, all the ciliary rings on the velum can be distinguished. These are the apical cilia (AC), inner preoral cilia (IPC), outer preoral cilia (OPC), and adoral cilia (AOC). The absence of the apical tuft in both O. chilensis and the closely related species O. edulis represents an adaptation to brooding by the embryos and larvae, but the lack of the postoral cilia (POC) in O. chilensis and the lack of cilia in the embryonic and early veliger stages are associated with an extreme brooding condition in this species.

In Vivo Observations of Larval Brooding in the Chilean Oyster, Ostrea chilensis Philippi, 1845.

The Chilean oyster Ostrea chilensis broods its larvae within the mantle cavity. In vivo observations, made with an endoscope, have demonstrated that the female does not undergo gill modification before or during the brooding process. The veliger larvae move freely, have no physical connections with the tissues of the mother, and are often seen as an aggregation ("swarm") around the labial palps. The larvae show a distinct circulation pattern inside the mantle cavity of the mother. Sporadic but strong pallial currents eject larvae from the swarm and transport them between the demibranchs to the posterior region, from which some return anteriorly in the basal ciliated tracts of the gills, and others on the marginal ciliated grooves. Larvae frequently move from the basal to the marginal groove of a demibranch via the ordinary filaments, although they occasionally travel in the opposite direction, moving along the principal filaments from the marginal groove to the basal tract. The circulation of the larvae in the mantle cavity may serve to irrigate them, thereby facilitating gas exchange and suspension-feeding. The veligers are not lecithotrophic, but readily remove and ingest particles suspended in the mantle cavity. The impact on the nutrition of the mother is not yet known, although the presence of particles in the food grooves and tracts and the transfer of material to the palps suggest that the feeding mechanism functions normally during brooding.