Gastropod Crepipatella Dilatata Research Articles

SELECTION OF TARGET SPECIES FOR MARINE PROTECTED AREAS: A MULTI CRITERIA APPROACH USING BENTHIC ORGANISMS

The selection of optimal target species to define and manage protected marine areas (MPAs) has generated a great scientific discussion during the past decades. Benthic invertebrates are commonly less considered as important target species, despite their pivotal role in marine ecosystems. To address this issue, we determined target species among benthic marine organisms using a multi-criteria approach. For this purpose, we used a data base from the Katalalixar National Reserve (RNK) in central Patagonia, Chile. The data were obtained through underwater photography and quantitative sampling by means of scuba diving during three expeditions between 2017 and 2019. Based on the total taxonomical inventory from both methods, a SIMPER analysis was used to determine 10 candidate species, and the Landscape Selection Species program was used for the selection of target species. Finally, eight target species were selected. The black snail Tegula atra, the hermit crab Pagurus comptus, the gastropod Crepipatella dilatata, and the polychaete Platynereis australis were selected among errant species. Among sessile species, the encrusting coralline algae Lithothamnium sp., the sea anemone Actinostola chilensis, the parchment worm Chaetopterus variopedatus, and the encrusting ascidia Didemnum sp. were the selected species. Based on our results we expect that these species will be included as target species in future management plans to improve protection of the marine environment of the Katalalixar National Reserve, one of the most pristine areas of the Chilean fjord region.
 Keywords: macroinvertebrates, macroalgae, biodiversity, Patagonia.

The influence of season and the tidal cycle on division of labour by the radula during feeding in the estuarine brooding gastropod Crepipatella dilatata (Calyptraeidae)

The brooding gastropod Crepipatella dilatata can feed by scraping the substrate with the radula and by suspension-feeding, which also requires use of the radula. There is a “division of labour” for the radula among three discrete tasks associated with feeding: (1) removing mucous balls from the food pouch; (2) transferring the mucous cord from the neck channel to the mouth (both components of suspension-feeding); (3) scraping the substrate. We hypothesised that the proportion of time used for each feeding activity varies according to environmental conditions. Total radular activity in females was greatest at high tide and in summer. The rate of radular extrusion for ingesting the mucous cord varied seasonally and between brooding and non-brooding females. Non-brooding females exhibited higher rates of radular extrusion for ingesting the mucous cord and for scraping the substrate than did brooders. In females, radular activity in removing the mucous ball from the food pouch was strongly influenced by the tidal cycle during winter, reaching minimum values at low tide. Differences were recorded in substrate scraping among seasons and within tidal cycles, and among males, brooding females and non-brooding females. Brooding females displayed less rasping than non-brooders, since the area available for grazing was restricted by the egg mass. Throughout the year, including low salinity periods, males allocated a greater proportion of total radular activity to rasping than to removing the mucous ball or ingesting the mucous cord. The feeding behaviour of both males and females is modulated by salinity, but the principal determinants of radular activity are the mode of reproduction (brooding in females) and, in males, motility.

The influence of encapsulated embryos on the timing of hatching in the brooding gastropod Crepipatella dilatata

Encapsulated embryos are generally thought to play an active role in escaping from egg capsules or egg masses. However, for species that brood their egg capsules, the factors controlling the timing of hatching are largely unclear, particularly the degree to which hatching is controlled by the embryos rather than by the mother, and the degree to which the hatching of one egg capsule influences the hatching of sister egg capsules within the same egg mass. We studied aspects of hatching using the direct-developing gastropod Crepipatella dilatata, which includes nurse eggs in its egg capsules and broods clusters of egg capsules for at least several weeks before metamorphosed juveniles are released. Isolated egg capsules were able to hatch successfully, in the absence of the mother. Moreover, the hatching of one capsule did not cause adjacent sister capsules to hatch. Hatched and un-hatched sister egg capsules from the same egg mass differed significantly in the number of metamorphosed juveniles, average shell size, offspring biomass (juveniles+veliger larvae), and the number of nurse eggs remaining per egg capsule. Differences in when egg capsules hatched within a single egg mass were not explained by differences in egg capsule age. Hatching occurred only after most nurse eggs had been ingested, most offspring had metamorphosed into juveniles, and juveniles had reached a mean shell length>1.36mm. Whether the mother has any role to play in coordinating the hatching process or juvenile release remains to be determined.

Consequences of maternal isolation from salinity stress for brooded embryos and future juveniles in the estuarine direct-developing gastropod Crepipatella dilatata

At reduced salinities, brooding females of some gastropods and bivalves may isolate their mantle cavities from the environment for several days, maintaining internal osmotic concentration but causing severe declines in dissolved oxygen and pH, and increases in ammonia and other toxic substances in the mantle fluid. This study in November–December examined the immediate consequences of such stresses for brooded embryos of Quempillen estuary gastropod Crepipatella dilatata, in terms of time to juvenile emergence and rates of embryonic growth [measured as shell length (SL)]. Juveniles were also monitored for latent effects on feeding rates, oxygen consumption, and growth for the first 4 weeks after emergence into normal salinity seawater. An acute salinity stress lasting 3 days applied to females that were brooding pre-shelled or intermediate-shelled stages increased embryonic incubation periods, but without affecting SL at emergence. Growth rates were reduced for encapsulated embryos regardless of the stage at which the salinity stress was applied. Latent effects on juvenile development included slower shell growth and reduced rates of oxygen consumption and feeding. These effects were sustained for the first month after release from the female. The results suggest that marked reductions in salinity lasting for several days indirectly but negatively affect the development of brooded embryos of C. dilatata and also affect the juveniles for at least several weeks following their release, even after salinity has returned to normal.

Crepipatella dilatata (Lamarck, 1822) (Calyptraeidae): an example of reproductive variability among gastropods

Reproductive characteristics of a species are often defined from a small number of individuals collected from a single location at one particular time. However, this study reveals that the South American gastropod Crepipatella dilatata (Lamarck, 1822) shows an unusually high level of intraspecific variability in some key reproductive characteristics: the number of egg capsules brooded per female, the size of the egg capsules, the number of eggs per capsule and the sizes and size distributions of the uncleaved eggs. Larger females were more fecund than smaller ones, not because they produced more egg capsules, but because they produced capsules of significantly larger size. Such variability was evident not only when considering different populations, but also within a single population sampled in different years, as well as among specimens collected during a single sampling event. Thus our data emphasize the importance of obtaining information from numerous specimens per locality as well as from specimens from different localities and in different years when describing the reproductive characteristics of any particular taxon.

Phylogeography and Biogeography Concordance in the Marine Gastropod Crepipatelladilatata (Calyptraeidae) along the Southeastern Pacific Coast

The biogeography and phylogeography concordance hypothesis suggests that the same factors, for instance physical barriers or environmental gradients, shape both species assemblages and intraspecific genetic structure. In the marine realm, previous studies have however suggested that phylogeographic patterns are also explained by the life-history strategy of the species. However, evidence is contradictory and comes mainly from the northern hemisphere, which is characterized by specific environmental conditions and evolutionary histories of species. In this work, we evaluated the concordance hypothesis in the southern Pacific using the marine gastropod Crepipatella dilatata as a case study. This intertidal species with direct development exhibited a restricted dispersal potential, a feature that contrasts with previous species studied in the same area. Using the gene cytochrome oxidase I, we analyzed 253 individuals sampled at 10 locations covering 543 km of the coast of Chile. The study sites also incorporated 2 biogeographic regions separated by a well-studied biogeographic break (at 30°S). Populations of C. dilatata displayed a high degree of genetic structure and a perfect match between phylogeographic and biogeographic breaks at 30°S. When comparing our data with previous research over the same geographic range, life history traits related to dispersal ability seem to be a good proxy for explaining the concordance between biogeography and phylogeography along the southeastern pacific coast. In addition, in this and other marine invertebrate species, gene flow limitations across both sides of the 30°S break may act as a driver of the speciation process.

Ammonia accumulation in the brood chamber of the estuarine gastropod Crepipatella dilatata: How big a problem for mothers and brooded embryos?

Crepipatella dilatata is an estuarine gastropod that broods its encapsulated embryos in the pallial cavity for several weeks before releasing juveniles. When environmental quality declines (e.g., in response to decreased salinity), females seal themselves against the substrate and isolate the pallial cavity from surrounding seawater, altering the chemistry of the pallial fluid surrounding the embryos. We documented rates at which total ammonia concentrations (NH 4 +–N + NH 3) increased in the pallial cavity during these extended periods of isolation, as well as excretion rates for both adult females and developing embryos (veligers). Also, we quantified the effects of elevated ammonia concentrations on both adults (mortality, egg capsule abandonment, and neck-radular activity) and veligers (mortality, and activity of the velum and velar cilia). In the pallial fluid, ammonia concentration increased about 150% during the first 16 h of female isolation from about 7–17 μg ammonia l −1, while excretion rates decreased nearly 85%, from an average of 5.5 to about 0.85 μg ammonia h −1 g −1 after 12 h of isolation. Brooded veligers also decreased their individual excretion rates over time, from 0.0035 to 0.0007 μg ammonia h −1 veliger −1 over 12 h. Ammonia accumulation eventually caused females to abandon their egg capsules and to detach from the substrate; in the field, this would probably lead to the death of both the encapsulated embryos and the detached females, but this happened only at concentrations of ≥ 0.1 mg ammonia l −1. In contrast, veligers withstood concentrations up to 34 mg ammonia l −1 for 72 h without dying, although ciliary activity and velar lobe activity decreased at concentrations of ≥ 0.1 mg ammonia l −1. Ammonia tolerance did not seem to change with continued development. Although previous studies have shown that prolonged isolation causes dangerous declines in oxygen and pH in pallial fluid for this species, the accumulation of ammonia in itself seems too low to cause direct harm to adults or developing embryos.

Capsule walls as barriers to oxygen availability: Implications for the development of brooded embryos by the estuarine gastropod Crepipatella dilatata (Calyptraeidae)

Encapsulation of developing embryos imposes potential restrictions, because the capsule wall must allow for adequate inward diffusion of oxygen and for increased diffusion of oxygen as metabolic demand increases with continued development. Samples of egg capsules from the gastropod Crepipatella dilatata were used to document surface characteristics, composition of the different capsule wall layers, and alterations in wall thickness during development. The diffusion coefficient and capsule wall permeability were determined experimentally for capsules containing embryos at different developmental stages. We also determined oxygen consumption rates for various embryonic stages and for nurse eggs, which provide food for embryos during development. The capsule wall of C. dilatata possesses 2 differentiated layers: the external capsular wall (ECW) and the internal capsular wall (ICW). The ECW is compact and fibrous, features that remain invariable during development, and lacks surface features that might make some portions of the capsule wall more permeable to oxygen than others. On the other hand, the ICW is initially spongy and thick, but significantly decreases in thickness over time, particularly before the embryos begin feeding on nurse eggs. Although the capsule wall is a serious barrier to diffusion, permeability to oxygen increases over time by 112% due to the dramatic thinning of the inner capsule wall layer. Nurse eggs consume oxygen but at very low rates, supporting the idea that they correspond to living embryonic cells that have stopped their development. Respiration measurements indicated that embryos are initially supplied with enough oxygen within the egg capsules to carry out the activities characteristic of embryogenesis, even though the capsular walls show their maximum thickness and lowest permeability at this time. However, as the embryo develops its velum and becomes more active, capsule wall thickness decreases and capsule permeability to oxygen increases. Correspondingly, the oxygen demands of metamorphosed but still encapsulated specimens are approximately 135% higher than those of pre-metamorphosed sibling embryos.

Brood chamber isolation during salinity stress in two estuarine mollusk species: from a protective nursery to a dangerous prison

Faced with environmental stress, the females of many marine invertebrate species can isolate their brood chambers from the external environment for prolonged periods. Although brood chambers have therefore typically been assumed to protect the brooded embryos, the effects of continued isolation on conditions within brood chambers have not been examined. In the present research, we investigated the effects of external stress on conditions in the brood chambers for 2 sympatric species, the gastropod Crepipatella dilatata and the bivalve Ostrea chilensis. Both species incubate their embryos in the pallial cavity for at least 4 wk before the young emerge as larvae (oyster) or juveniles (gastropod). Brooding and non-brooding females were stimulated to isolate the pallial cavity from the external environment by exposing them to water of reduced salinity (<22 to 24 psu). We then recorded subsequent changes in salinity, dissolved oxygen, pH, and ammonium ion concentration within the pallial fluid. Although salinity within the pallial cavity remained high for both species, oxygen availability for brooding females of C. dilatata and O. chilensis dropped to hypoxic levels (<1.5 mg O2 l -1 ) within 12 h and 20 min, respectively. In addition, pH of the intrapal- lial fluid dropped substantially with prolonged maternal isolation, suggesting a possible impact on shell formation for brooded veligers. Indeed, in the case of C. dilatata, the pH of pallial fluid initially fell to 6.4, but then tended to become more basic after 6 h of maternal isolation, a possible conse- quence of shell dissolution. On the other hand, ammonium ion concentration increased progressively with prolonged maternal isolation. Our data show that, whereas initially the isolation mechanism protected incubated embryos from exposure to low salinity stress, continued isolation from the exterior transformed the brood cavity from a protective environment to an oppressive one, i.e. from a protective nursery to more of a prison.

Isolation of incubation chambers during brooding: effect of reduced pH on protoconch development in the estuarine gastropod Crepipatella dilatata (Calyptraeidae)

The sedentary gastropod Crepipatella dilatata encapsulates its embryos and incubates them in the pallial cavity. Females can deliberately isolate their embryos from the external environ- ment for many hours at a time by pressing their shells tightly against the substrate. We documented the effects of such isolation on pH in the pallial cavity and the effects of reduced pH on changes in shell thickness and the proportion of calcium in embryonic shells. We also quantified the concen- tration of calcium in the water retained in the pallial cavity during isolation, as well as the growth of encapsulated veligers. Average protoconch thickness decreased by as much as 50% at reduced pH (pH = 6 to 3). During 24 h of exposure to water at the different pHs, calcium was lost from shells, but in same proportion as the loss of other components. Calcium in the pallial fluid increased during the first 5 h of isolation for both brooding and non-brooding females, suggesting shell dissolution. The calcium content of pallial cavity fluid for brooding females differed from that of non-brooding females, but did not differ from that in the intracapsular fluid, suggesting that calcium diffuses freely through the egg capsule wall. Isolation of the incubatory chamber impeded embryonic shell growth, possibly because the calcium was acting as a 'buffer' to regulate pH changes in the pallial fluid. The isolation of embryos by incubating females, usually viewed as an adaptive benefit of brood- ing, can cause pronounced negative effects on embryonic development during the period of shell formation.

Variations in the quantity and composition of seston from an estuary in southern Chile on different temporal scales

Estuaries are characterised by highly variable environmental conditions largely driven by tidal and atmospheric forces. This study investigates variation in the physical environment and the composition of the seston on various temporal scales in the Quempillén estuary, southern Chile. The water column was sampled throughout the tidal cycle at various times of the year. Total particulate matter, particulate inorganic matter, particulate organic matter, particle numbers, total particle volume, proximate biochemical composition and energy content of the seston, chlorophyll a and chloropigments were routinely measured. In each of the months in which sampling took place, two or three tidal cycles were examined. The information not only helps to explain the dynamics of the estuary, but is essential for an understanding of the physiology and ecology of the suspension-feeders which exploit the seston as a food source, the most dominant being the gastropod Crepipatella dilatata. Temperature and salinity were generally highest during summer, but seston quality, defined by energy content and biochemical composition (lipid, protein and carbohydrate) was higher at the end of winter and during spring. Chlorophyll a values were greatest in late spring (November). Many of the variables studied changed frequently according to the phase of the tidal cycle, and in several cases significant differences were observed among tidal cycles from the same month of the same year. In general the variables measured did not exhibit consistent patterns linked to the tidal cycle, possibly because any such patterns were masked by atmospheric conditions (wind and rain) that dominate the region and greatly influence the estuary. The quantity and quality of the seston available to suspension-feeders is largely determined by these atmospheric forces, which cause an influx of terrigenous material from adjacent areas and also resuspend bottom sediment. These effects are magnified by the shallowness of the estuary (<2 m depth). The food supply for C. dilatata and other suspension-feeders therefore varies on temporal scales varying from hourly (tidal cycle) to daily/weekly (atmospheric forces) to monthly (seasonal influences), but inhibition of feeding by low salinity sometimes limits the ability of C. dilatata to exploit fully the available organic matter.

The effect of salinity on clearance rate in the suspension-feeding estuarine gastropod Crepipatella dilatata under natural and controlled conditions

The suspension-feeding gastropod Crepipatella dilatata occurs in estuaries in southern Chile that experience considerable fluctuations in salinity, driven by tidal and atmospheric forces. In the Quempillén estuary salinities as low as 9 psu may occur after severe rainstorms, and persist for several hours. In this study salinity was the major factor influencing the clearance rate of C. dilatata. At salinities below 20 psu, filtration ceased, whereas at high salinities (>22 psu) mean clearance rate was 0.24 l h −1 standard animal −1 (S.D. 0.18) for actively filtering individuals. This was confirmed by laboratory experiments under controlled conditions. Endoscopic observations were consistent with measurements of clearance rate, and showed that at salinity 25–30 psu the rate of transport along the gill filaments of particulate material embedded in mucus was 759 μm s −1 (S.D. 480), but particle transport ceased at and below salinity 20 psu. Complete or partial isolation of the mantle cavity from the environment may be a mechanism to protect soft tissues and/or incubated egg capsules from osmotic stress.