Large Marine Gastropods Research Articles

Population genetics of queen conch, Aliger gigas (Linnaeus, 1758) (Gastropoda: Strombidae) at the Cuban island platform

Abstract The queen conch, Aliger gigas is a large marine gastropod mollusc that inhabits shallow seagrass meadows and sandplain habitats throughout the Caribbean. Owing to overfishing and degradation of the environment, it has become an endangered species in most of its habitat. Research on Cuban populations of A. gigas is scarce and mostly focused on conch exploitation. The present study assesses, for the first time, the genetic diversity and population structure of A. gigas from six locations on the Cuban platform, using five microsatellite loci. At most of the sampled locations, the observed heterozygosity was lower than expected and the FIS value was significantly positive, both of which suggest inbreeding. Also, we found evidence of bottlenecks for two of the locations with a deficit of heterozygotes. Although statistically significant, only 1.66% of the total variance was explained by genetic differentiation among populations, and discriminant analysis of principal components showed different degrees of overlapping between all locations. Accordingly, the results showed that there is an extensive and symmetrical exchange of genetic information. Sparse non-negative matrix factorization analysis determined the existence of three ancestral populations admixed across the sampled locations. Thus, our results suggest that A. gigas from the Cuban island platform could be a unique population, which is relevant for management and conservation strategies.

From reproductive behaviour to responses to predators: Ocean acidification does not impact the behaviour of an herbivorous marine gastropod

Ocean acidification (OA), which reduces ocean pH and leads to substantial changes in seawater carbonate chemistry, may strongly impact organisms, especially those with carbonate skeletons. In marine molluscs, while the physiological effects of OA are well known, with a reduction of growth and shell calcification, there are few studies on behavioural effects. A large marine gastropod, Haliotis tuberculata, was exposed to ambient (pHT 8.0) or low pH (pHT 7.7) during a 5-month experiment. Because animal fitness can be affected through various behavioural changes, a broad spectrum of behavioural parameters was investigated, including situations involving no stress, responses to predators, righting to evaluate indirectly the level of energy reserves, and finally, reproductive behaviour. In addition, we measured the expression profile of the GABA A-like and serotonin receptor genes, often described as central neuromodulators of sensory performance and behaviour and known to be affected by OA in molluscs. No significant effect of low pH as compared to ambient pH was observed on abalone behaviour for any of these behavioural traits or gene expressions after either one week or several months of exposure to OA. The significance tests were corroborated by estimating the size of pH effects. The behaviour of this mollusc appears not to be affected by pH decrease expected by the end of the century, suggesting some resilience of the species to OA at the adult stage. This is probably related to the ecological niche of this abalone, where important pH variations can be observed at tidal, diurnal or seasonal scales.

Densities of Large Marine Gastropods in Seagrass, Oyster Reef, and Sandy Habitats in Tampa Bay and along the Gulf Coast of Florida

Marine gastropods in Florida are harvested by the marine-life trade, tourists (for shells), and traditional commercial fisheries, but stocks are not formally assessed for most species. The main goal of this project was to estimate biological variables that may be used to evaluate the Species of Greatest Conservation Need status of the banded tulip Cinctura lilium and six other large marine gastropod species that are commonly encountered in the targeted habitats. The principal target, C. lilium, was listed in the 2012 State Wildlife Action Plan. The densities and size structures of C. lilium and six co-occurring species of large marine gastropods in Tampa Bay were examined to evaluate population dynamics, seasonal variation, and habitat preferences of these species. Long-term trends in the densities of large, predatory marine gastropods in 10 regions from 2009 to 2017 were included. In Tampa Bay, strong habitat preferences were observed for all species studied: C. lilium and Melongena corona were most likely to be observed on oyster reefs, and Fasciolaria tulipa was found only in seagrass, whereas Strombus alatus, Triplofusus gigantea, Sinistrofulgur sinistrum, and Fulguropsis spirata were more common on soft sediments. Seasonal variations in densities were weak; seasonal differences in size structure were more pronounced. The smallest individuals of C. lilium appeared in spring and summer; F. spirata, S. alatus, and S. sinistrum reached a detectable size in fall. The smallest detectable M. corona appeared in winter. Regionally, there were more gastropods in southwestern bay grass beds (Tampa Bay, Sarasota Bay, and Pine Island Sound) than in coastal seagrass beds (Big Bend, Citrus, Hernando, Pasco, and coastal Pinellas) or northern bays (St. Joseph Bay and St. Andrew Bay), and each region had characteristic species. As a group, tulip snails exhibited modest local declines in densities at two sites, whereas the whelks and T. gigantea varied annually but did not exhibit consistent trends during 2009 to 2017. The present study establishes a baseline of abundance for seven species of common marine gastropods and recommends expanded monitoring in multiple habitats to improve future analyses of abundance trends.

Integrating Genetic, Environmental, and Social Networks to Reveal Transmission Pathways of a Dolphin Foraging Innovation

Cultural behavior, which is transmitted among conspecifics through social learning [1], is found across various taxa [2-6]. Vertical social transmission from parent to offspring [7] is thought to be adaptive because of the parental generation being more skilled than maturing individuals. It is found throughout the animal kingdom, particularly in species with prolonged parental care, e.g., [8, 9]. Social learning can also occur among members of the same generation [4, 10, 11] or between older, non-parental individuals and younger generations [7] via horizontal or oblique transmission, respectively. Extensive work on primate culture has shown that horizontal transmission of foraging behavior is biased toward species with broad cultural repertoires [12] and those with increased levels of social tolerance [13, 14], such as great apes. Vertical social transmission has been established as the primary transmission mechanism of foraging behaviors in the Indo-Pacific bottlenose dolphin (Tursiops aduncus) population of Shark Bay, Western Australia [6, 9, 15, 16]. Here, we investigated the spread of another foraging strategy, "shelling" [17], whereby some dolphins in this population feed on prey trapped inside large marine gastropod shells. Using a multi-network version of "network-based diffusion analysis" (NBDA), we show that shelling behavior spreads primarily through non-vertical social transmission. By statistically accounting for both environmental and genetic influences, our findings thus represent the first evidence of non-vertical transmission of a foraging tactic in toothed whales. This research suggests there are multiple transmission pathways of foraging behaviors in dolphins, highlighting the similarities between cetaceans and great apes in the nature of the transmission of cultural behaviors. VIDEO ABSTRACT.

Haliotis tuberculata, a generalist marine herbivore that prefers a mixed diet, but with consistent individual foraging activity

AbstractWhile population foraging behaviour of herbivores has been extensively studied, individual choice is still poorly understood. Very few studies have focused on the individual consistency of foraging behaviour in marine herbivores. Because marine ectotherms are strongly influenced by their environment and because a mixed diet is appropriate for herbivores, we hypothesized that Haliotis tuberculata, a large marine gastropod, would not exhibit significant individual consistency in foraging activity and would display generalist food choices. To test these hypotheses, the behaviour of 120 abalone was studied using a choice test of eight macroalgal species over 3 weeks, with video recording 24 hr a day. In addition, primary components, secondary metabolites and toughness of the eight algae were measured. At the population level, food choice was mainly related to the protein composition and the toughness of the macroalgae. We found that H. tuberculata is a generalist species feeding on a variety of algae (IS = 0.64), even if 21% of the individuals can be considered to be specialists. However, in contrast to our hypothesis, highly consistent between‐individual variation was observed in foraging activity (ICC = 0.81 for time spent feeding and ICC = 0.74 for number of feeding visits per day). The high individual consistency of foraging activity has some ecological and evolutionary implications currently not understood for this marine herbivore.

Investigating δ18O of Turbo sarmaticus (L. 1758) as an indicator of sea surface temperatures

The large marine gastropod Turbo sarmaticus was (and still is) an important food item for coastal foragers along the south coast of South Africa. Opercula of this species are well-preserved in both Holocene and Pleistocene archaeological sites, offering the opportunity to reconstruct past sea surface temperatures from δ18O of shell carbonate over much of the last glacial cycle. We have analysed δ18O and δ13C in 16 opercula and one shell of modern animals collected alive from an area with good SST records, in order to explore how reliably this species records water temperature through the year and to investigate possible ‘vital effects’ that may influence the isotope record. We find that T. sarmaticus deposits aragonite in both operculum and shell in oxygen isotopic equilibrium with seawater. Operculum δ18O values of this species reliably reflect water temperatures between c.14 and 24°C, although they do not always capture temperature extremes, especially in winter, likely due to slower growth under stressful growth conditions. These thresholds probably alter according to factors such as variations in nutrient supply. The averaged maximum and minimum values across the set of sixteen serially sampled opercula very closely approximate the temperatures of the warmest and coolest months and therefore provide a good measure of the seasonal temperature range, and of mean annual SST. δ18O of edge increments can, to some extent, be used to indicate season of collection, within the broad categories of warmer/cooler seasons.

Spatiotemporal Variability in ΔR in the Northern Gulf of Mexico, USA

AbstractStrombus alatus and Busycon sinistrum are large marine gastropods that are frequently recovered from archaeological contexts in southeastern North America. We previously proposed a reservoir age offset (ΔR) for B. sinistrum from the northern Gulf of Mexico region based on known-age pre-bomb 20th-century specimens. We also reported significant variability in radiocarbon both among and within S. alatus specimens, which precluded a reliable estimation of ΔR for this taxon. In this paper, we present a complementary data set from archaeological contexts to re-evaluate marine reservoir effects in the northern Gulf Coast region at multiple spatial and temporal scales. The new data set consists of a total of 13 14C age determinations from well-associated marine (B. sinistrum and S. alatus) and terrestrial (Odocoileus virginianus) samples from a closed context at the Bayou St. John (1BA21) archaeological site. We suggest a slightly updated ∆R value of –2±53 14C yr for late Holocene-age B. sinistrum from the northern Gulf Coast region. S. alatus, and possibly other species of strombid conchs, are poor candidates for 14C dating due to the highly variable 14C content observed within and among specimens. Though subregional variability in inputs of 14C-depleted waters is likely, life-history factors related to ontogenetic niche and/or habitat shifts appear to be a major influence in shell 14C for S. alatus.

Chronology of Red Abalone Middens on Santa Cruz Island, California, and Evidence for Subsistence and Settlement Change

Red abalone middens on Santa Cruz Island, California, are conspicuous because they contain the shells of red abalone, a large marine gastropod, even though mussel shells are the most abundant by weight. Recently obtained radiocarbon dates push back the time interval of the island's red abalone middens to ca. 6200 cal B.C., with the bulk of them dating between 5000 and 3300 cal B.C. Faunal remains from two sites indicate that subsistence on marine resources intensified at the onset of the time interval of the middens. In addition, beginning ca. 3900 cal B.C. the island settlement system became more complex and subsistence on marine resources, particularly with respect to marine mammals such as dolphins, once again became more intensive. Proposed explanations for the subsistence and settlement shift concern the development of possibly more complex watercraft and the adoption of the mortar and pestle for processing plant foods. The expanded time interval during which red abalone middens occur has revealed that cooler sea-surface temperature is only a partial explanation for their occurrence.

Cascading effects from survival to physiological activities, and gene expression of heat shock protein 90 on the abalone Haliotis discus hannai responding to continuous thermal stress

Increasing temperatures can be a significant stressor for aquatic organisms. Abalones, a type of large marine gastropods, are the most commercially important species in aquaculture for Asia. To evaluate the potential ecological risk posed by temperature stress, we measured biological responses such as survival rate, adhesion ability (falling rate), and foot abnormalities in the abalone Haliotis discus hannai. Additionally, biochemical and molecular responses were evaluated in H. discus hannai exposed to various temperature gradients. The survival rate was reduced in abalones exposed to relative high temperatures (more than 26 °C). Increased temperature stress induced a higher falling rate and abnormal foot structure. Furthermore, increased antioxidant enzyme activities were observed in abalones exposed to relative high temperatures (26 and 28 °C). The activities of superoxide dismutase were induced in a time-dependent manner after high temperature stress. Generally, heat shock protein 90 also increased significantly in H. discus hannai exposed to temperature gradients (more than 24 °C) for 12 h. These results provide valuable information regarding stress responses to increased temperatures, in H. discus hannai: adverse biological and molecular outcomes could be utilized as risk assessments and stress monitoring of marine ecosystems under increased water temperatures.

Abundance and Distribution of Large Marine Gastropods in Nearshore Seagrass Beds Along the Gulf Coast of Florida

Local abundance was estimated and distribution determined for selected large gastropod species based on observations made during underwater visual surveys at 10 sites along the Gulf coast of Florida each summer from 2009 through 2012. The total number of tulip snails (Fasciolaria spp., including the true tulip, Fasciolaria tulipa, and banded tulip, Fasciolaria lilium), lightning whelk (Busycon sinistrum), and horse conch (Triplofusus giganteus) were counted at 190 stations (each 600 m2) each year in shallow-water seagrass beds. Tulip snails were observed most frequently, with a mean density of 1.93 ± 3.56 snails/ 600 m2, with substantially fewer lightning whelks (0.29 ± 1.04/600 m2) and horse conchs (0.10 ± 0.37/600 m2) observed. Horse conchs were distributed more evenly across the 4 Gulf coast regions studied: Panhandle, Big Bend, Nature Coast, and South. Tulip snails were most abundant in the Panhandle and the South, whereas lightning whelks were found predominantly in the South. Snail counts peaked in 2010 and were greatest at the Pine Island Sound site, although mean density was greatest in Sarasota Bay (2.2 snails/600 m2). Snails were observed most frequently at the St. Joseph Bay site, where they were present at 74 of the 80 stations surveyed. Statewide commercial fisheries landings data were examined for years 1994 through 2011 and totaled 130,710 true tulip snails (banded tulip snails were not included), 72,230 lightning whelks, and 33,087 horse conchs. The total number landed of both lightning whelks and horse conchs was greater on the west coast of Florida, whereas the total number of true tulip snails landed was greater on the east coast.

A permanent tag for large marine gastropods

An individual aluminum tag was developed which is simple, quick to fasten and inexpensive. The tagging method is described. Satisfactory results have been obtained in tests with gastropods of several genera.

A note on blood and water mixing in large marine gastropods

1. 1. The foot in Busycon carica is inflated by the uptake of seawater from the ambient medium. 2. 2. Blood and water mix freely in the foot, and blood is concentrated before returning to the gill or mantle, probably in the nephridium. 3. 3. During full retraction into the shell, both blood and water are expelled into the meium, which is necessary to reduce body volume and to allow fit deep into the shell.