Internal Growth Lines Research Articles

Mapping intrashell variation in Mg/Ca of brachiopods to external growth lines: Mg enrichment corresponds to seasonal growth slowdown

Determining secular changes in seawater temperature and Mg/Ca ratio is of high importance in paleooceanographic, paleoenvironmental and paleoecological studies. On the one hand, intra-shell variation in Mg/Ca in brachiopod shells is used to reconstruct historical changes in temperature and in seasonality. On the other hand, intra-shell analyses show a weak relationship between Mg/Ca and δ18O, but a positive correlation between Mg/Ca and Sr/Ca, and an increase of Mg/Ca at growth lines, indicating that Mg/Ca does not simply track seawater temperature alone. Internal growth lines are rarely visible in brachiopod shells, and the relation between growth lines that mark growth slowdown or cessation and Mg/Ca fluctuation is thus not properly understood. Here, using four species of extant brachiopods from the NE Pacific and the SW Pacific, from environments with low seasonality in seawater temperature (<5 °C), and two species of Late Triassic brachiopods (Western Carpathians), we measure intra-shell ontogenetic variation in Mg/Ca, S/Ca and Sr/Ca with laser ablation ICP-MS and electron microprobe. In contrast to previous studies, we map variation in Mg, S, and Sr to external growth lines. We find that, first, zones of Mg/Ca enrichment in the secondary layer form 10–50 μm-thick discrete bands or clusters of micrometric bands that consistently terminate at major external, predominantly annual growth lines that are associated with distinct notches that correspond to mantle retractions in most species. These bands generate distinct peaks in Mg/Ca that stand above low, more uniformly distributed background Mg/Ca values along laser-ablation and microprobe transects. The magnitude of Mg/Ca in these bands is comparable to Mg/Ca in the primary layer, exceeding background values of Mg/Ca in the secondary layer by 5–20 mmol/mol (by a factor of two to five). Second, Mg enrichment in discrete bands is closely associated with an increase in S concentrations in the secondary layer. Therefore, even when Mg and S uptake is expected to be highest under fast precipitation rate, these empirical observations show that Mg and S enrichment occur in the zones that were precipitated at times of a significant growth reduction (e.g., in cold-temperate brachiopods studied here during winters when primary productivity is low). The mechanisms for this paradox are unclear but can be related to uptake of Mg by amorphous calcium carbonate (ACC) to delay the transformation of ACC to calcite during the formation of growth lines. Therefore, intra-shell variation in Mg/Ca in brachiopods with major growth lines is primarily determined by seasonal decline or cessation in shell growth and not by seasonal changes in seawater temperature.

The growth of juvenile native mussels (Elliptio complanata) in lakes varies with sediment characteristics and site exposure

Abstract Unionid mussels are among the largest and longest‐lived freshwater invertebrates and can play an important role in these ecosystems. They are also one of the most endangered groups of organisms. The juvenile stage is a particularly vulnerable part of mussel life history and is one of the most poorly known. I compared the growth of young Elliptio complanata at 17 nearshore sites, in shallow (polymictic) and stratified lake basins, along gradients of sediment characteristics and site exposure (effective fetch). At each site, the growth of six to 14 small (20–68 mm) mussels collected on the sediment surface was measured, using internal growth lines. The growth of very young endobenthic mussels (22–40 mm) was also measured on four to six mussels at each of two sites. Juveniles spend several years in the sediments, and I found that during this period growth is not constant but declines rapidly with age. Shifts in δ15N signatures suggest that juveniles change their habitat use towards a more planktonic baseline around the time of maturation, when they reach a length of 30–50 mm. Identical δ13C signatures in juveniles and adults suggest that both rely on food of planktonic origin, whether deposited or suspended. The growth of juvenile mussels varies in a complex but predictable manner with sediment characteristics and wind‐driven physical forces. Growth was highest in fine sediments with low organic content, in highly organic but coarse sediments, and in protected nearshore areas with low effective fetch. Interestingly, I also found high growth rates at exposed nearshore areas with fine sediments, suggesting that areas where bottom topography creates a refuge from currents and waves may provide particularly good conditions for the early growth of juvenile mussels. Some parts of the shoreline may be more important than others for native mussel populations, and if we can identify those, they may warrant additional protection.

Ligament, hinge, and shell cross-sections of the Atlantic surfclam (Spisula solidissima): Promising marine environmental archives in NE North America.

The Atlantic surfclam (Spisula solidissima) is a commercially important species in North American waters, undergoing biological and ecological shifts. These are attributed, in part, to environmental modifications in its habitat and driven by climate change. Investigation of shell growth patterns, trace elements, and isotopic compositions require an examination of growth lines and increments preserved in biogenic carbonates. However, growth pattern analysis of S. solidissima is challenging due to multiple disturbance lines caused by environmental stress, erosion in umbonal shell regions, and constraints related to sample size and preparation techniques. The present study proposes an alternative method for describing chronology. First, we analyzed growth patterns using growth lines within the shell and hinge. To validate the assumption of annual periodicity of growth line formation, we analyzed the oxygen isotope composition of the outer shell layer of two specimens (46°54'20"N; 56°18'58"W). Maximum δ18Oshell values occurred at the exact same location as internal growth lines in both specimens, confirming that they are formed annually and that growth ceases during winter. Next, we used growth increment width data to build a standardized growth index (SGI) time-series (25-year chronology) for each of the three parts of the shell. Highly significant correlations were found between the three SGI chronologies (p < 0.001; 0.55 < τ < 0.68) of all specimens. Thus, ligament growth lines provide a new method of determining ontogenetic age and growth rate in S. solidissima. In a biogeographic approach, the shell growth performance of S. solidissima in Saint-Pierre and Miquelon was compared to those in other populations along its distribution range in order to place this population in a temporal and regional context.

Isotopic fractionation between seawater and the shell of Scrobicularia plana (Bivalvia) and its application for age validation

This study analyzed the isotopic profiles of four aragonitic shells of Scrobicularia plana in conjunction with measured seawater temperatures and salinities. Comparison of δ18OSHELL with expected values revealed fractionation of δ18O in near equilibrium with the ambient environment. Growth cessation occurred between November and March. Carbonate deposition stopped when temperatures were <12°C. Analysis of δ13CSHELL values suggested that carbon in the shell does not reflect the DIC in ambient water, likely due to the incorporation of metabolic carbon. An ontogenetic trend of increasing δ13C values over time was observed, likely related to changes in metabolic activity. Annual growth patterns were inferred from δ18OSHELL profiles and compared with internal and external growth lines. Estimations of age based on external lines were unreliable, resulting in overestimation of age and underestimation of growth rates, likely due to the disturbance lines being wrongly identified as annual. Analysis of internal lines may lead to over- or underestimation of age and was more reliable in recent portions of the shell.

The population structure and biology of the ocean quahog,Arctica islandica, in Belfast Lough, Northern Ireland

The spatial distribution, density, growth rate, longevity, mortality and recruitment patterns of the long-lived clamArctica islandicain Belfast Lough, Northern Ireland, UK are described. TheA. islandicapopulation at Belfast Lough appears to be restricted to a small area at the mouth of the Lough. Additional searches for specimens further into the Lough and into deeper waters found no evidence of a larger more widespread population and we report population densities of 4.5 individuals m−2. The ages of the clams were determined from the number of internal annual growth lines in acetate peel replicas of shell sections. The population growth curve was fitted using the Von Bertalanffy growth equation: Lt = 93.7 mm (1−e−0.03(t–1.25)). Based on catch curve analysis, the Belfast Lough population has an estimated longevity of 220 years and a natural mortality rate of 0.02. We compare growth characteristics and life history traits in this population with other analogousA. islandicapopulations. The overall growth performance and the phi-prime index were used to compare growth parameters with data from the literature and we observed no significant relationship between the growth performance indices and longevity or latitude. Analysis of the age-structure and reconstructed dates of settlement indicate that this population has experienced almost continual recruitment over the last century with a gap in successful recruitment into the population 90–100 years ago and another 140–150 years ago. The size-structure revealed a scarcity of small individuals which we believe may be an artefact of the dredge sampling process.

Age, growth, and population structure of the smooth clam Callista chione in the eastern Adriatic Sea

The age, growth, and population structure of the smooth clam Callista chione were determined from samples collected by hydraulic dredge and SCUBA at four locations in the eastern Adriatic during 2007 and 2008. The age of 436 clam shells was determined from internal growth lines present in shell sections, and the timing of growth line formation was ascertained from monthly collections of clams to occur between August and September when sea water temperatures were maximal. In addition, age of 30 older individuals was verified with acetate peels of polished and etched shell sections. Differences were apparent in the age structure and growth rates of clams collected from the four locations studied. Von Bertalanffy growth (VBG) curves obtained for clams from these locations were L t = 72.4 (1−e−0.25(t − 2.68)) (Rab Island), L t = 74.5 (1−e−0.15(t + 0.57)) (Pag Bay), L t = 79.3 (1−e−0.34(t − 0.97)) (Cetina estuary), and L t = 82.5 (1−e−0.11(t + 2.88)) (Kaštela Bay). The age of the clams ranged between 3 and 44 years; median clam ages were similar at three of the four locations (14, 12, and 12 years, respectively), but was significantly lower in the Cetina estuary (4 years). The VBG growth constants recorded from clams were within the range of values obtained for this species by previous authors. The observed local differences in population structure indicate different levels of exploitation and illustrate the need to establish long-term strategies for a sustainable exploitation of smooth clams in the Croatian Adriatic.

Age, growth and population structure of Modiolus barbatus from the Adriatic

Age, growth and population structure of Modiolus barbatus from Mali Ston Bay, Croatia were determined using modal size (age) classes in length frequency distributions, annual pallial line scars on the inner shell surface, internal annual growth lines in shell sections of the middle nacreous layer and Calcein marked and transplanted mussels. The length frequency distributions indicated that M. barbatus attain a length of ∼40 mm in 5–6 years indicating that a large proportion of the population in Mali Ston Bay is 6 years) was determined from the middle nacreous lines in shell section, which formed annually in winter between February and March; the wider dark increments forming during summer (June to September). The oldest mussel, determined from the middle nacreous lines, was >12 years, with the majority of mussels aged between 3 and 6 years of age. The ages of mussels ascertained using the growth lines were not dissimilar to the ages predicted from the length frequency distributions. Age at length curves produced using modal size class data were not different from the data obtained using the pallial scar rings and internal growth lines. Taken together these data suggest that M. barbatus attains a length of 40 and 50 mm within 5 and 8 years, respectively. Eighty one percent of individual M. barbatus injected with a Calcein seawater solution (300 mg Calcein l−1), into their mantle cavity successfully deposited a fluorescent line, which was visible in suitably prepared shell sections under ultra violet light. Incorporation of Calcein into the mussel shells was seasonally variable with the lowest frequency of incorporation in mussels marked in February and recovered in May. Seasonal shell growth was observed with significantly higher growth rates in mussels marked in May and removed in August (ANCOVA, F3,149 = 23.11, P 2.5 mm month−1 compared with a mean mussel growth rate of 1.2 ± 0.6 mm month−1. At other times of the year mussel shell growth ranged from immeasurable to 1.48 mm month−1.

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.

A new model for periostracum and shell formation in Unionidae (Bivalvia, Mollusca)

The periostracum in Unionidae consists of two layers. The outer one is secreted within the periostracal groove, while the inner layer is secreted by the epithelium of the outer mantle fold. The periostracum reaches its maximum thickness at the shell edge, where it reflects onto the shell surface. Biomineralization begins within the inner periostracum as fibrous spheruliths, which grow towards the shell interior, coalesce and compete mutually, originating the aragonitic outer prismatic shell layer. Prisms are fibrous polycrystalline aggregates. Internal growth lines indicate that their growth front is limited by the mantle surface. Transition to nacre is gradual. The first nacreous tablets grow by epitaxy onto the distal ends of prism fibres. Later growth proceeds onto previously deposited tablets. Our model involves two alternative stages. During active shell secretion, the mantle edge extends to fill the extrapallial space and the periostracal conveyor belt switches on, with the consequential secretion of periostracum and shell. During periods of inactivity, only the outer periostracum is secreted; this forms folds at the exit of the periostracal groove, leaving high-rank growth lines. Layers of inner periostracum are added occasionally to the shell interior during prolonged periods of inactivity in which the mantle is retracted.

Can shell scars on dog cockles ( Glycymeris glycymeris L.) be used as an indicator of fishing disturbance?

The use of shell damage records as an in situ indicator of past fishing disturbance was investigated using the dog cockle Glycymeris glycymeris L. Shell sections of dog cockles collected from four areas subjected to varying levels of fishing disturbance were examined for the presence of damage records or shell ‘scars’. Animals from a heavily fished area had significantly higher levels of scarring than those from three lightly fished areas. From an estimation of the age of the shells (from internal growth lines and dating of each line), the year in which scarring occurred was determined and this was compared to yearly records of fishing effort. There was a weak but significant positive correlation between the frequency of shell scars per year and the intensity of fishing effort. Our data suggest that whilst scarring in shells of G. glycymeris cannot accurately be used to estimate past fishing intensity on a year-by-year basis, it can be used to differentiate between severely impacted and lightly fished areas of the sea bed.

A Long-Term Growth Record Derived from Arctica Islandica (Mollusca, Bivalvia) from the Fladen Ground (Northern North Sea)

Long-term variations in shell growth of the mollusc Arctica islandica (Mollusca, Bivalvia) from the northern North Sea have been assessed retrospectively using the annually deposited internal growth lines. Relatively young specimens yielded a detailed year-to-year chronology while the growth record of specimens older than 30 y yielded a time series with a length exceeding 100 years. The long-term growth trends demonstrated a marked alternating sequence of periods in which growth was below and above expectation. A 33-y long cycle could be discerned. Since the 1960s the growth patterns in Arctica from two nearby locations were opposite, while they resembled each other in the period before 1960.

A description of the skeletal development pattern of the temperate coral Caryophyllia smithi based on internal growth lines

Scanning electron microscopy was used to study the microstructure and internal growth lines of the temperate ahermatypic coral Caryophyllia smithi (Cnidaria: Anthozoa). The arrangement of internal growth lines in combination with the orientation of aragonite crystals were used to describe the pattern of skeletal development in C. smithi. The observed pattern was verified using observations from another study on skeletal development in C. smithi, but which was based only on external observations of skeletons of living and dead specimens in different stages of development. The pattern of skeletal development in C. smithi is suggested to be subdivided into three stages, based on the deposition of specific skeletal elements during the development of the skeleton. In the first ‘juvenile’ stage, various primary skeletal elements are formed: the basal plate, the septa and a primary and secondary septotheca. The second ‘half full grown’ stage is characterized by development of apparently only an extended basal attachment, which enlarges the attachment area to the substratum. In the third ‘full grown’ stage, the edge zone of the polyp tissue is retracted from the extended basal attachment to the calice, and upward growth of the coral predominates followed by lateral thickening of the septotheca, costae, septa and columella. Internal growth lines were found throughout the skeleton and may be composed of, or resulting from the presence of organic matter. The septotheca and the extended basal attachment, which are important for a strong skeletal structure and a strong attachment to the substratum, respectively, are probably thickened faster than the other skeletal elements. Attachment scars were found in areas where attachment of the coral tissue to the skeleton is critical.

Annual variation in the growth rate of Yoldia notabilis (Bivalvia: Nuculanidae) in Otsuchi Bay, northeastern Japan, analyzed using shell microgrowth patterns

Annual variation in the growth rate of the protobranch bivalve Yoldia notabilis (collected in Otsuchi Bay, northeastern Japan between 1989 and 1991) was determined by measuring shell length at successive growth lines. Factors affecting growth rates were assessed by examining long-term environmental data. Shell cross-sections of Y. notabilis showed a clear pattern of internal growth lines which formed simultaneously with the annual external lines on the outer shell surface. Hence, they were used as an age marker. A maximum lifespan of 17 yr was determined for this species, and a sigmoidal growth curve was obtained by the internal growth line analysis. Examination of the growth lines also revealed a large annual variation in growth rate, fluctuating as much as 32-fold during the past 9 yr. The variation correlated negatively with water temperature and positively with chlorophyll a content in the water column. It is suggested that the variation in annual growth rate is dependent on food supply during the spring phytoplankton bloom which varies from year to year according to the flow of the cold Oyashio current each spring.

Age determination, growth rate and population structure of the horse musselModiolus modiolus

The age and growth rate ofModiolus modiolushave been studied from acetate peel replicas of polished and etched shell sections. Age estimates could be reliably obtained from the alternating patterns of light (summer) and dark (winter) growth lines present in the middle nacreous layer of the shell. Growth lines in the inner nacreous layer, however, generally converged to form blocks of nacre such that the identity of individual lines was lost, whilst in the umbones growth lines were often tightly compressed and difficult to resolve. Data obtained from analyses of the internal growth lines in the middle nacreous layer were used to construct growth curves for several subtidal populations using the von Bertalanffy growth equation. The fastest growth rate was recorded for mussels growing epifaunally on the legs of a drilling platform in the North Sea; these mussels achieved a maximum shell length of 110 mm within ten years. The oldest mussel (from Ling Bank in the northern North Sea) was 48 years old and measured 133 mm in length whilst the largest mussel (from Loch Spelve in western Scotland) was 147 mm long and 38 years old. With the exception of the relatively young population (maximum age 10 years) from the drilling platform, most of the benthic populations studied included mussels in excess of 35 years of age. It is clear, therefore, thatM. modiolusis a potentially long-lived member of the subtidal benthos.

Potential habitat dependence in deposition rate of presumptive annual lines in shells of the bivalve Protothaca staminea

Although repeating depositional features in shells of bivalve molluscs continue to be used in ecology and paleoecology to age individual specimens and thereby provide a potentially powerful tool for geochronological reconstruction of past events, few studies actually test the basic assumptions of growth line analysis: (1) that line deposition is truly periodic and (2) that the length of the period is one year. Recapture of marked individuals of the bivalve Protothaca staminea after 12 or 24 months in field plots in two habitats of Mugu Lagoon (California, U.S.A.) suggests a habitat-specific pattern of deposition of the major growth lines previously assumed to be annual. External (surface) and internal (cross-sectional) growth lines were in excellent agreement on any given specimen and showed that each specimen from a muddy-sand environment deposited a single annual line over 12 months, whereas all but one specimen from a clean-sand environment deposited several more major growth lines than predicted from the numbers of years of additional growth. Although more frequent handling or natural disturbance in the higher-energy, clean-sand habitat may explain these differences, the results demand caution in extrapolating tests of annual periodicity in growth line deposition across species or even across habitats for a single species.

Geodock (Panope generosa: Bivalvia) Age as Determined by Internal Growth Lines in the Shell

Geoduck (Panope generosa) age was determined by counting internal growth lines in the hinge plates of the shells. Several experiments substantiated the hypothesis that one growth line is deposited every year. Growth line deposition was found to occur during the winter.Key words: age, geoducks, Bivalvia, growth lines

Age determination of the soft-shell clam Mya arenaria using shell internal growth lines

Shells of known-age Mya arenaria have revealed an internal annual growth pattern in this bivalve. The number of external growth rings on the shell exterior does not correspond to the age of the clams. This study provides an alternative method to using external annual rings for age determination. The internal growth lines are visible in thin sections when the shells are cut from the umbo to the ventral margin. The lines are formed by late spring of each year prior to spawning and are probably in response to decreased winter growth. When the 7 year olds were examined it was difficult to distinguish the most recent growth line and the inner shell layer. This could result in ages being underestimated. This annual pattern of internal growth lines could be useful to biologists and paleoecologists engaged in population studies.

Age and growth rate determinations for the Atlantic surf clam Spisula solidissima (Bivalvia: Mactracea), based on internal growth lines in shell cross-sections

Marked and recovered surf clams, Spisula solidissima Dillwyn, from Virginia (USA) deposited one internal growth line during a period of 11/2 years, probably in response to spawning during late summer. We have used these annual growth lines to make growth curves for two samples of New Jersey (USA) clams, one from inshore (1.8 km from shore, 15 m deep), the other from offshore (17.5 km from shore, 28 m deep) waters. The offshore and inshore clams grow at approximately the same rate until Age 3 years, after which time the growth rates differ, as does the ultimate lifespan; the offshore clams grow more rapidly and attain a greater age — up to 31 years. Comparison of our growth curves with other published curves revealed a close correspondence to a curve which was based on a study of growth over a 5-year period. Curves based on external growth lines probably underestimate growth rate in early life and overestimate it in later years.