Shell Growth Lines Research Articles

X-ray phase contrast reveals soft tissue and shell growth lines in mollusks

High-resolution 3D imaging of species with exoskeletons such as shell-bearing mollusks typically involves destructive steps. Nondestructive alternatives are desirable since samples can be rare and valuable, and destructive steps are time-consuming and may distort the tissue. Here, we show for the first time that propagation-based phase-contrast X-ray imaging can significantly increase contrast in mollusks with intact shells. By using the recently upgraded monochromator at the SPring-8 BL20B2 synchrotron beamline, we imaged six species of mollusks, showing that X-ray phase contrast enhances soft-tissue contrast. Features that are almost invisible in conventional attenuation-based micro-computed tomography (micro-CT) are clearly reproduced with phase-contrast imaging under the same scan conditions. Furthermore, this method can reveal features such as growth rings in the shell and differentiate between calcite and aragonite crystal forms. Phase-contrast imaging can thus serve as a compelling alternative when destructive methods are not an option.

IDENTIFYING THE TICKS OF BIVALVE SHELL CLOCKS: SEASONAL GROWTH IN RELATION TO TEMPERATURE AND FOOD SUPPLY

Sclerochronology uses shell growth lines or bands for the construction of environmental time-series and the measurement of organism growth, but more study is needed to constrain the triggers of the dark cessation bands observed in many bivalve groups. We constructed a database of direct observations of modern growth seasonality across the class Bivalvia and compared the occurrence of seasonal growth bands to environmental data including latitude, temperature, and chlorophyll-a concentration. Bivalves with cold-season (winter) cessations are more common towards the poles, with logistic regression showing that temperature, followed by latitude of occurrence, displays the strongest relationship with occurrence of winter cessation. Remotely sensed and directly measured chlorophyll-a concentration show no significant relationship. Summer cessations are sparse and only weakly associated with environmental controls but are concentrated at the subtropical latitudes among temperate bivalves at their equatorial extremes. The rarity of summer cessations can be explained by the limited annual ranges of temperature in the tropics, combined with the exponential relationship of metabolic rate to temperature leading to a narrow window between normal functioning and mortality at high temperatures. This data suggests that, unless annual temperatures have low variability like in equatorial or polar regions, the season of growth cessation across bivalves is primarily a function of temperature tolerance through restriction of scope for growth. At most latitudes, growth bands can be interpreted as being primarily triggered by temperature stress, rather than seasonal starvation.

Enigmatic traces in infaunal bivalves from the late Quaternary of Argentina, Southwestern Atlantic. Bioerosion, bioclaustration or nothing?

Ichnological investigations were carried out on late Quaternary shells of the intertidal deep infaunal bivalve Tagelus plebeius (Lightfoot, 1786) found along the southwestern Atlantic, between Uruguay and the southernmost Buenos Aires Province in Argentina. Analyses reveal distinctive marks that are spread on the outer shell surface only. The marks are regular-unbranched-elongate, perpendicular to the outer shell growth lines, with deflections on the margins, never interconnected, without bifurcations, conforming bottom-up constructions. They occur in hundreds of specimens from many samples taken from sediments ranging in age from the late Pleistocene to the Recent. These marks have never been reported or described for this species and their origin and formation remain elusive. We describe these traces thoroughly and we propose an explanation for their preservation on about half the shells examined. Potential destructive boring structures (excavated from outside-in) or bioerosion activities by other macro- or micro-organisms are dismissed. These antimarginal asymmetric traces point instead to a process of constructive bioclaustrations (grown from the bottom-up) produced in situ during the life of the bivalve by unknown symbiont organisms. Additionally, the regular pattern observed for the marks exclude host growth as a consequence of abiotic/extrinsic causes. From a palaeoecological perspective, these structures suggest a biotic interaction that was hitherto undescribed neither for bivalves nor for the late Quaternary of the southwestern Atlantic.

Precipitation variability in the Sahel during the last 2000 years revealed by archaeological shell middens in Senegal

In the second half of the 20th century, a strong multidecadal drought occurred in the Sahel that had catastrophic social and economic consequences. This event made it urgent to better understand the forcing driving precipitation changes in the Sahel and potential impact of anthropogenic global warming. Here, we reconstruct past changes of the precipitation regime in the Saloum Delta, Senegal, from stable isotope analyses in fossil shells of Senilia senilis. The shells were collected in large radiocarbon dated shell middens built by ancient fishermen during the last two millennia. Oxygen isotopic composition in shells is related to salinity conditions in this hypersaline estuary that is very sensitive to changes in precipitation and evaporation. Our dataset shows that salinity is today at its highest level in the past 2000 years. These values were reached abruptly in the 20th century and lie outside the range of natural climatic variability in this site. Monthly resolved isotopic profiles in fossil shells combined with analyses of shell growth lines allowed us to explore the role of rainfall seasonality in the variability of mean conditions.

Nanoscale structure and mechanical behavior of growth lines in shell of abalone Haliotis gigantea

In the natural world, bottom-up hierarchical construction of complex structures results in materials with remarkable properties. A well known example is the nacre of mollusk shells, commonly called "mother of pearl", whose excellent strength and toughness has been the subject of research for many decades. A significant discovery has been the presence of periodic layers called "growth lines". These are thin distinct layers within the bulk of the shell which form periodically, with their structure affected by environmental changes. Studies of their formation and behavior offer valuable insight into the architecture of seashells. In this work, the structure and mechanical behavior of growth lines in shells of abalone Haliotis gigantea were investigated using electron microscopy and nanoindentation. Growth lines form directly out of nacre into layers of blocks and irregular particles. In comparison to nacre, they have basic structures, form rapidly, and are harder, which suggest that they serve a protective role during lifecycle transitions. This exemplifies how natural structures are able to closely control growth architecture in order to form different structures for different functions, all from the same base materials.

Climatic regulation of Clinocardium ciliatum (bivalvia) growth in the northwestern Barents Sea

We examined the growth of the Arctic bivalve Clinocardium ciliatum in the Barents Sea to evaluate the effect of oceanographically distinct water masses on growth and to assess the influence of climatic forcing on ecological processes over decadal scales. Analysis of annually-deposited growth lines in shells of 22 individuals from 3 stations allowed us to assess growth conditions from 1977–2006, encompassing both warmer and colder climatic phases of the 20th century. Growth rates of juvenile specimens (6–13 years) were highest in Atlantic water, resulting in a 20% greater average shell size compared to similarly aged individuals from Arctic water or at the Polar Front. This may reflect comparatively warmer sea temperatures and/or greater food supplies in regions of the Barents Sea dominated by Atlantic water. Despite different absolute growth rates, temporal patterns of ontogenetically-adjusted incremental growth (i.e. Standard Growth Index = SGI) were similar at all sites, with low but increasing SGI throughout the 1980s and peaking in 1994 or 1995. An abrupt decline starting in 1996 led to low SGI values for most years from the turn of the century to the last year of bivalve growth in 2006. The decline in SGI coincides with abrupt phase shifts in two hemispheric oscillatory indices: the North Atlantic Oscillation (NAO) and the Arctic Climate Regime Index (ACRI). The strongest statistical relationships were found between standardized growth and the ACRI and its local manifestations through precipitation and sea ice cover. The ACRI explained 51% of the variation in growth from all the samples, while ACRI, annual precipitation, and ice-free days together explained 65% of the growth variability. Using a two-year running mean of the ACRI improved these relationships substantially and indicates a possible lag in the relationship between external forcing and bivalve growth. These results show that benthic communities in this area are intricately linked to regional climatic forcing and that the predicted increase in Atlantic water influence in the Barents Sea in response to climate change will impact growth of benthic organisms.

Insights into early Holocene hunter-gatherer mobility on the Peruvian Southern Coast from mollusk gathering seasonality

Quebrada de los Burros (QLB) is an early Archaic coastal archaeological site in southern Peru (∼18.1°S) and the most extensively studied in the area for this period. It was occupied from 10 to 6.5 ka by fishermen also practicing hunting and mollusk gathering. Shell growth lines in 116 individuals of the surf clam Mesodesma donacium were studied to determine the month of their death (±2 months). Our results show that, for the whole occupation period, mollusk gathering was a seasonal activity mainly practiced during austral spring and summer. A change occurred between the early and the middle Holocene: the mollusk gathering season in the middle Holocene occurred ∼3 months earlier in the year than in the older levels. This behavior change could have a cultural origin, rather than dictated by the environment for it is associated with changes in the lithic industry. QLB occupants also hunted herbivores in the nearby lomas ecosystems. These plant communities only grow during the fog season from June to December, suggesting that the site was occupied during this season. A comparison of the span of the mollusk gathering season and the lomas season suggests that, at least during the early Holocene, QLB was occupied all the year round. A permanent freshwater source and the proximity of the sea, the lomas, and raw lithic materials, provided ideal conditions for a permanent occupation. This result reveals a strategy based on a seasonal alternation between marine and terrestrial resources exploitation.

Growth trends in three bivalve species indicate climate forcing on the benthic ecosystem in the southeastern North Sea

Internal growth lines in shells of 3 suspension-feeding bivalves (Arctica islandica, Mya truncata and Chamelea striatula) from the SE North Sea were analysed in search of common inter- annual variations of their growth rate. The high similarity (69 to 80%) between the growth records in the 3 species suggests that a large-scale (climatic) factor is responsible for an important part of the variation in annual shell growth. The common trend extracted from the individual growth records was correlated with monthly data on phytocolour, NAO index, temperature and wind. The strength and sign of the effect of the last 3 factors varied seasonally. Effects of wind strength and direction were analysed in detail, as in situ measurements showed that wind speeds >10 m s -1 (Beaufort 6) cause resuspension of fine sediment at the site where the bivalves were collected. Resuspended sed- iment causes a drop in the quality of food for suspension feeders. During the bivalve growing season, northwesterly to easterly winds tended to depress growth, whereas winds with a westerly component mainly had a positive effect. Strong winds from a WNW direction in May, however, had a negative effect and could explain the highest proportion of variance in the common growth trend; WNW winds have a long fetch at the study area and generate (high) long waves, facilitating resuspension of fine sediment at relatively low wind speeds.

Effects of environmental conditions on planktonic abundances, benthic recruitment and growth rates of the bivalve mollusc Ruditapes decussatus in a Portuguese coastal lagoon

Controlling environmental parameters for the early stages of marine invertebrates have received little attention, particularly in field studies. This study involves measurement of abundances and growth rates of the bivalve Ruditapes decussatus Linnaeus 1758 during its planktonic larval and early benthic life stages in a coastal lagoon: Ria Formosa, Portugal. Measured abundances were compared with tidal amplitude, water temperature, salinity, wind velocity and direction, and a food availability indicator (chlorophyll a). Data were obtained on abundance and prodissoconch length of the larvae, measured two to three times per week, and of post-larval stages individuals that had settled in artificial collectors over 10 months. Larval and juvenile cohorts were identified using size-frequency distributions and larval ages estimated by larval shell growth lines. Data were fitted to linear, exponential, and Laird–Gompertz growth models. Larval growth rates best matched a linear model: 3.78±0.55 per day, r 2=0.75, p<0.001. Early benthonic growth rates best matched a Laird–Gompertz model: 3.97±0.15 per month, r 2=0.98, p<0.001. It was concluded that there was a significant relationship between planktonic and recruitment abundances. Water temperature (as a coarse factor) and advection (as a fine factor) effects were inferred to be the prime environmental factors affecting early life stages of this species in this coastal lagoon system.

Estimation of the life history parameters of Mytilus galloprovincialis (Lamarck) larvae in a coastal lagoon (Ria Formosa — south Portugal)

Abstract The life history parameters of early stages of marine invertebrates, particularly field estimations, have received relatively little attention. The aim of this research was to estimate in situ abundance and growth of Mytilus galloprovincialis planktonic larvae. Plankton samples were filtered through gauze of 63 μm mesh and identified, counted and measured using an inverted microscope. Short-term fluctuations in Mytilus galloprovincialis larvae abundance and environmental parameters (water temperature, salinity, wind velocity direction, tidal amplitude and chlorophyll a ) were monitored (two to three times a week). Larval cohorts were identified using size–frequency distributions and age estimates compared with larval shell growth lines. Data were fitted to the linear, exponential, von Bertalanffy and Laird–Gompertz growth models. Larval growth adjusted better to the Laird–Gompertz model (0.525±0.073 μm d −1 ; r 2 =0.768; P

Growth variations inArctica islandicaL. (Mollusca): a reflection of hydrography-related food supply

The growth lines in shells of Arctica islandica from the Fladen Ground have been used to construct long-term chronologies of growth variations. Individual specimens showed characteristic sequences of periods in high and low growth rates. Because the deviations were strongly synchronized, an environmental factor is held responsible. Inter-annual variations in either temperature or phytoplankton abundance could not explain the observed variations. The hypothesis is therefore put forward that the occurrence of dense patches of Arctica and the variations in growth result from variations in import and accumulation of organic matter by an eddy system overlying the area. Evidence for this hypothesis is provided by the correlation between the estimated inter-annual influx of Atlantic water into the North Sea and the observed growth variations.

Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis.

Correlations between allozyme heterozygosity and fitness-related traits, especially growth, have been documented in natural populations of marine bivalves. However, no consistent pattern has been exhibited, because heterotic effects on size vary with age and individual growth parameters are generally unknown. No consensus has emerged on the genetic basis of allozyme-associated heterosis. The species studied here, Spisula ovalis, displays annual shell growth lines, which allows us to compute individual age and growth dynamics over the whole life span. Our morphological study was coupled to a protein electrophoresis study at seven polymorphic loci. While the maximum size gained is not related to heterozygosity, the age at half maximum size, t1/2, is significantly negatively correlated with heterozygosity, indicating an heterotic effect on initial growth. The correlation between heterozygosity and size is expected to vanish when age increases, due to the form of the growth function. This decreasing correlation is consistent with previous studies. We compare the relative performances of five linear models to analyze the genetic basis of heterosis. Surprisingly, the largest part of variance in t1/2 is due to additive effects, the overdominant components being much weaker. Heterosis is therefore due to general genomic effects rather than to local overdominance restricted to allozymes or small neighboring chromosomal segments. A significant dependence of individual heterotic contributions of the enzyme loci upon expected heterozygosities, rather than metabolic function, further supports the hypothesis of enzymes acting as markers. General genomic effects can hold only if allozyme heterozygosity is positively correlated with heterozygosity at fitness-related genes scattered throughout the genome. This hypothesis is supported here by heterozygosity correlations between enzymatic loci.

An attempt for age estimation of bivalves, using shell growth lines

An attempt for age estimation of bivalves, using shell growth lines

Age Estimation of Sea Scallop Larvae (Placopecten magellanicus) from Daily Growth Lines on Shells

Larval sea scallops (Placopecten magellanicus) were reared in the laboratory and their shell growth lines were counted and used to estimate age in days. The first growth line was deposited 3 to 4 days after fertilization. Age estimates from growth-line counts were strongly correlated with the actual ages of the larvae. Photoperiod had no detectable effect on the rate of growth-line deposition.

Periodicity of chamber formation in chambered cephalopods: evidence fromNautilus macromphalusandNautilus pompilius

The growth rates of ammonites and extinct nautiloids have been estimated in two ways: through analyses of shell growth lines and by analyzing the patterns of oxygen isotopic values from successive septa. In both types of studies, it has been assumed that the amount of time between successive chamber formation events is approximately constant. This assumption has never been tested with living cephalopods, however. To examine this, 10 immatureNautilus pompiliusand two immatureN. macromphaluswere maintained in a surface aquarium for a period of 1 yr and periodically radiographed. The radiographs allowed direct observation of chamber formation events and apertural shell growth. During this observational period 61 separate chamber formation events were observed in the nautiluses. The time between separate chamber formation events increased in successively produced chambers, and varied from a minimum of 2–3 wk in a specimen of 45-mm shell diameter to a maximum of 13–15 wk in a specimen of 132-mm shell diameter. Unlike interval of chamber formation, which increased during ontogeny, rate of apertural shell growth showed no observable rate increase or decrease during ontogeny prior to maturity. With the onset of maturity, as marked by the shell characteristics defined by Collins et al. (1980), apertural shell growth rates dropped markedly, and ceased coincident with the removal of the last volumes of cameral liquid in the last formed, approximated chamber. Both rate of apertural shell growth and septal spacing were affected by degree of shell breakage.