# Developing a sclerochronology network in the Adriatic Sea: Growth synchrony among populations of Callista chione

Hana Uvanović, Melita Peharda, Nicole Pavin, Julien Thébault, Carlotta

Mazzoldi, Hrvoje Mihanović, Ivan Župan

► To cite this version:

Hana Uvanović, Melita Peharda, Nicole Pavin, Julien Thébault, Carlotta Mazzoldi, et al. Developing a sclerochronology network in the Adriatic Sea: Growth synchrony among populations of Callista chione. Regional Studies in Marine Science, 2023, 64, pp.103009. 10.1016/j.rsma.2023.103009. hal-04172276

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https://hal.univ-brest.fr/hal-04172276v1

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
Developing a sclerochronology network in the Adriatic Sea:
Growth synchrony among populations of *Callista chione*

Uvanović Hana <fnref n="1" />,*, Peharda Melita <fnref n="1" />, Pavin Nicole <fnref n="2" />, Thébault Julien <fnref n="3" />, Mazzoldi Carlotta <fnref n="2" />,
Mihanović Hrvoje <fnref n="1" />, Župan Ivan <fnref n="4" />

**Abstract :**

Callista chione samples were live collected at three localities in the Adriatic Sea: Gulf of Venice, Italy, Pag
Bay and Pašman Channel, Croatia. Acetate peel replicas were prepared and the Image Pro Primer
program was used to measure increment widths in samples that had clear boundaries. Visual cross-dating
of the images was performed using list-year method and validated using COFECHA, while the R package
dplR was used to construct the chronologies. The age of analysed shells ranged from 15 to 46 years
(N=32; 29,9 ± 8,8 years) at the Gulf of Venice, from 14 to 41 years (N=63; 26,0 ± 5,1 years) at Pag Bay,
and from 14 to 41 years (N=33; 26,8 ± 4,8 years) at the Pašman Channel. Final statistically robust
standard master chronologies spanned from 1986 to 2018 (Gulf of Venice), from 1994 to 2019 (Pag Bay)
and from 1994 to 2015 (Pašman Channel). Statistically significant correlation was obtained only between
the Gulf of Venice and Pag Bay residual master chronologies (1994–2018; r = 0.607; p <0.001). Although
there are some coincidences between all three localities, suggesting a common signal among
populations, the growth chronology in the Pašman Channel recorded a very different signal potentially
linked to differing oceanographic influences. The Pašman Channel locality is more affected by the inflow
of warmer and saline waters coming from the south than the two other sites which are located in
geographically and hydrographically isolated Adriatic areas. No correlation was found between any shell
master chronologies and surface seawater temperature. Also, no correlations between the shell C.chione
master chronologies and parameters describing the Adriatic-Ionian Bimodal Oscillating System (BiOS)
were observed. Correlation maps indicate different relationships between shell master chronology and
chlorophyll a concentration in the region. Significant correlations were mostly limited to March and April
and showed spatial variations.

<footnote n="1">¹ Institute of Oceanography and Fisheries, Split, Croatia</footnote>

<footnote n="2">² Department of Biology, University of Padova, Padova, Italy</footnote>

<footnote n="3">³ Univ Brest, CNRS, IRD, Ifremer, LEMAR, 29280 Plouzané, France</footnote>

<footnote n="4">⁴ Department of Ecology, Agronomy and Aquaculture, University of Zadar, Zadar, Croatia</footnote>

<footnote>* Corresponding author : Hana Uvanovic, email address : uvanovic@izor.hr</footnote>
**Graphical abstract**

<figure><img src="image_2.png" /></figure>

**Keywords**: Mediterranean Sea, dplR, Veneridae, shell growth, clams, sclerochronology
# 1. Introduction

Coastal and shelf areas are dynamic and complex multifunctional systems at the interface between land and sea (Salgado-Hernanz et al., 2022). These areas are subject to a variety of stressors that overlap, including the effects of climate change, land-based pollution, and commercial fisheries (Ramírez et al., 2018). Semi-enclosed seas, such as the Mediterranean Sea, are particularly vulnerable to disturbance due to high surface-to-volume ratios and strong pressures from various human activities (Halpern et al., 2015; Schroede et al., 2015; Piroddi et al., 2017). Anthropogenic pressures on Mediterranean marine ecosystems are predicted to increase in the future (Coll et al., 2010), particularly due to habitat destruction, resource exploitation, and climate change (Giorgi and Lionello, 2008; Coll et al., 2012; Adloff et al., 2015).

To understand the significance of potential future changes, knowledge of present and past environmental variability and its influence on marine organisms is critical. This requires detailed records of oceanic conditions over broad temporal and spatial scales (Grebmeier, 2012). As observational multidecadal or multicentennial records are often lacking, scientists have been exploring possibilities for reconstructing environmental conditions from growth increments in hard tissues of various marine organisms including bivalve shells, fish otoliths, coralline algae and corals (Gröcke and Gilikin, 2008; Oschmann, 2009; Butler et al., 2019).

Bivalves are often used in sclerochronological research because they continuously deposit shell material throughout their lifetimes and populations may exhibit a common response to environmental forcing, exhibiting synchronous shell growth rates (e.g., Wanamaker et al., 2012; DeLong et al., 2014; Reynolds et al., 2016). Measuring of growth increment widths enables the development of absolutely dated, annually resolved, and environmentally sensitive proxy records ranging from several decades to a few millennia (e.g., Schöne, 2008; Black et al., 2009; Butler et al., 2013). By applying statistical methods adopted from the dendrochronological research, individual shell growth series data are used for constructing robust master chronologies (e.g., Wanamaker et al., 2012; Butler et al., 2013; Reynolds et al., 2022). These chronologies can be related to modern environmental conditions and used for the reconstruction of past climate changes (e.g. Black et al., 2009; Butler et al. 2010; Edge et al., 2021). Further, efforts have been devoted to the construction of shell chronology networks, based on data from multiple sites within a certain geographic region, in order to obtain more comprehensive insight into past environmental variability on a larger scale (e.g. Butler et al., 2009; Reynolds et al., 2017; Peharda et al., 2019).

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While the majority of bivalve chronologies have been developed at relatively high latitudes and in major ocean basins, such studies are still very rare in the Mediterranean and limited to the Adriatic Sea and to species from the genus *Glycymeris*, including *G. bimaculata* (Bušelić *et al.*, 2015) and *G. pilosa* (Peharda *et al.*, 2016: Peharda *et al.*, 2018; Peharda *et al.*, 2019). Previous studies on age and growth of the commercially important *venerid bivalve Callista chione* have shown that the longevity of this species can extend up to four decades (Forster, 1981; Ezgeta-Balić *et al.*, 2011), making it an interesting target species for sclochronological studies (Purroy *et al.*, 2018a). *Callista chione* is a relatively large (up to 10 cm), shallow-burrowing suspension-feeding bivalve that inhabits sandy sediments in coastal waters at depths up to 180 m and is widely distributed in the eastern Atlantic Ocean and the Mediterranean Sea, including the Adriatic Sea (Poppe and Goto, 2000). It is commercially exploited in several countries from the eastern Mediterranean to the Atlantic, including Croatia, France, Greece, Italy, Morocco, Portugal, and Spain (e.g., Gaspar *et al.*, 2001, 2002; Tirado *et al.*, 2002; Metaxatos, 2004; Moura *et al.*, 2009; Ezgeta-Balić *et al.*, 2011; Baeta *et al.*, 2014; Bouzaidi *et al.*, 2020). Previous studies conducted on *C.chione* include analyses of the reproductive cycle (Valli *et al.*, 1984; Tirado *et al.*, 2002; Moura *et al.*, 2008; Purroy *et al.*, 2019), population dynamics (Metaxatos, 2004), age and shell growth rate (Hall *et al.*, 1974; Forster, 1981; Keller *et al.*, 2002; Leontarakis and Richardson 2005; Moura *et al.*, 2009; Ezgeta-Balić *et al.*, 2011, Purroy *et al.*, 2018b). Understanding growth synchrony within and among populations in the species *C.chione* is needed in order to obtain an insight into its growth dynamics in relation to environmental conditions.

The main objectives of this study were to: (1) determine if well-replicated, annually-resolved, shell growth chronologies can be developed from *C.chione* shells collected at three localities in the Adriatic Sea, (2) determine the potential of *C.chione* for developing a network of bivalve chronologies in the Adriatic Sea, and (3) test possible environmental influences on the shell growth of this species.

## 2. Materials and methods

Individuals of *Callista chione* were collected live at three localities in the Adriatic Sea: (1) the Gulf of Venice, Italy (45.344° N, 12.525° E; 17-18 m depth); (2) the Pag Bay, Croatia (44.495° N, 14.987° E; 4-6 m depth); and (3) the Pašman Channel, Croatia (43.948° N, 15.388° E; 1.5-3 m depth) (Fig. 1). Specimens were obtained from the catch of the commercial fishing vessels at the locality in the Gulf of Venice in 2018, and by SCUBA and skin-diving at the

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106 other two localities on several occasions from 2013 to 2020 (Supplementary Material; Table S1). For the laboratory analysis, we selected the largest-sized shells (>60 mm).

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<figure><img src="image_3.png" /><figcaption>**Figure 1.** The study area: **A.** The bathymetry of the Northern Ionian Sea and the Adriatic Sea. The localities of *Callista chione* sampling in the Adriatic are denoted by red dots. Schematic **representation** of the Adriatic circulation is also depicted (the yellow line represents the Eastern Adriatic Current – EAC, while the blue line represents the Western Adriatic Current – WAC). **The river mouth of the Zrmanja River (Croatia) is indicated by black arrow, while the delta of the Po River (Italy) is denoted by white arrow.** Black and white rectangles in the Northern Ionian denote **the** areas between which the height difference of the absolute dynamic topography (ADT) was calculated. The red rectangle in the Northern Ionian represents the area used for **computating** vorticity. **B.** Gulf of Venice (**the Po River delta is indicated by black arrow**), **C.** Pag Bay and **D.** Pašman Channel.</figcaption></figure>

Immediately after collection, the specimens were frozen, and in the laboratory the shells were thawed and the tissue removed. The shell length (anterior-posterior axis) of each
specimen was measured with a digital caliper to the nearest 0.1 mm, and the dry weight was determined using a scientific scale with a precision of 0.01 g.

The hinge area of each shell was cut and embedded in epoxy resin. The resin blocks containing the hinge were cut along the axis of maximum growth, ground, and polished. The polished surfaces were etched in 0.1 M HCl for 2 min. After etching, samples were rinsed in tap water and left to air dry. Acetate peels were prepared by pouring ethyl acetate with a pipette on the polished and etched shell section and covering the surface with a piece of acetate sheet. Acetate peels were placed between two microscope glass slides and photographed using an Axio Lab A1 microscope equipped with a Zeiss AxioCam ERc 5s camera. Multiple photographs were taken for each sample and then stitched together into a single composite photograph using Image-Pro Plus 10 software. Due to the better visibility of annual growth lines, all measurements were done in the inner shell layer and were conducted from the ontogenetically youngest part of the shell towards the oldest part (Fig. S1).

<figure><img src="image_4.png" /><figcaption>**Figure 2.** A. *Callista chione* shell, black rectangle represents hinge area that was cut from each sample, while dashed black line presents axis of maximum growth along which the shells were sectioned. B. Shell of *C. chione* embedded in epoxy resin. DOG – direction of growth. Scale bar 1 cm.</figcaption></figure>

At each locality the age was estimated for all specimens that had clearly visible growth lines, but only shells that had clearly delineated growth increments boundaries were used to construct master chronologies. Counting of growth lines was performed independently by two experienced researchers and age estimates are reported only for shells for which estimates
matched. Acetate peel images were visually cross-dated using the list-year method (Yamaguchi, 1991) to ensure that each increment was assigned to the correct year of formation. This technique is based on the assumption that some aspects of the environment limit growth, and as **the environmental conditions** vary over time, they induce a synchronous growth pattern in contemporaneous individuals sampled from the same area (Fritts, 1976; Yamaguchi, 1991). The correct calendar year of each increment was assigned by cross-dating backward from the known year of sampling. Cross-dating was also checked using the program COFECHA (Holmes, 1983). It is important to note that analysis of stable oxygen isotope composition (δ18O) in shells of *C. chione* specimens collected from Adriatic Sea showed that this species deposits an annual growth line during late summer/early autumn (Purroy *et al.*, 2018b; Uvanović, 2022) while the growth stop/cessation occurs during January and February. This means that a given annual growth increment can contain environmental data from two calendar years. For example, the annual growth increment marked as "2015" in our time series contains shell material deposited over two time periods: from September to December 2014, and from March to August 2015. **This was taken into account when analysing the potential correlations with environmental data.**

After visual cross-dating, individual growth increment widths were measured from the internal shell surface **towards the** external surface (Figure 2B) along the axis of maximum growth and perpendicular to **the** growth increment boundaries using **the** Image-Pro Plus 10 software (Supplementary Material; Figure S1). All detrending and chronology construction were performed in R (R Core Team, 2022) using dplR package (Bunn, 2008). Detrending was performed with a cubic spline with a rigidity of 10 years and a cut-off frequency of 50%. Population-level signal strength in the chronology was assessed using the Expressed Population Signal (EPS). Although arbitrary, an EPS ~0.85 is considered the threshold at which the sample set adequately reflects the theoretical population from which it was drawn (Wigley *et al.*, 1984). EPS was calculated over a window of 5 years. For each locality, **two versions of the chronologies** were built: **a standard and a residual version**. To build **the** residual chronology, each individual growth time series was first prewhitened by fitting an autoregressive model, in order to remove autocorrelation. Then all prewhitened time series were averaged using the Tukey's biweight robust mean, in order to minimize the effect of outliers.

In order to test possible environmental influences on the growth of *C. chione*, available data of surface seawater temperature (SST) and chlorophyll-a concentrations were **correlated** with the shell growth chronologies. Seawater temperature can affect growth directly, but also
indirectly - through its influence on bivalve reproductive cycle and food supply (Schöne et al., 2005). Bivalve shell growth is known to be strongly influenced by food quantity and quality (Ballesta - Artero et al., 2018). In order to highlight possible relationships between *C. chione* master chronologies and environmental data, correlation maps (Pearson's r) were computed over a large area (36°-46°N 12°-22°E) around our three localities. The sea surface temperature data used to compute correlation maps were retrieved from the NOAA Optimum Interpolation Sea Surface Temperature (OI SST V2) dataset, provided by the NOAA PSL, Boulder, Colorado, USA (https://psl.noaa.gov). An estimation of the monthly concentration of chlorophyll-a (Chl- a) in the Adriatic, Ionian and Tyrrhenian Seas was obtained for the period 1998-2019 from GlobColour (http://globcolour.info). High-resolution (1/24°, i.e. approx. 4 km × 4 km) ocean colour data retrieved from different sensors (SeaWIFS, MERIS, MODIS Aqua, and VIIRS) were averaged using the Garver-Siegel-Maritorena (GSM) model (Maritorena and Siegel, 2005). All files were downloaded in NetCDF4 format. For each cell of the gridded environmental dataset, pairwise Pearson's correlations were computed between the annual values of the master chronology and environmental data for the months of March, April, May, June, July and August. Only correlations at a 90% significance level (or higher) are displayed on these maps. NetCDF4 files were processed using R 4.2.0 "Vigorous Calisthenics" (R Core Team, 2022), after loading of packages 'rgdal', 'raster', and 'ncdf4'. Correlations between the chronologies and environmental time series developed for the sampled locations were performed in order to detect the environmental force at each site. All additional information can be found in Supplementary material.

The regime of the Adriatic - Ionian Bimodal Oscillating System (BiOS, Gačić *et al.*, 2010) indicates the origin of waters entering the Adriatic Sea. In order to estimate the state of the BIOS, the monthly values of the height difference of the absolute dynamic topography (ADT), here termed ADTDifference, were computed for a 0.5°x0.5° area centered on the northern edge of the eddy in the northern Ionian Sea (black rectangle in Fig. 1A) in relation to an area of the same dimensions at the center of the eddy (white rectangle in Fig. 1A). Another parameter used to describe the state of the BIOS was vorticity, calculated in for the northern part of the Ionian Sea (37.0°N - 39.0°N; 17.0°E - 19.5°E; red rectangle in Fig. 1A), using the procedure described by Shabrang *et al.* (2016). When the value of the parameter ADTDifference is positive, the level in the center of the vortex is lower than the level at the edge of the vortex, which indicates cyclonic (counter-clockwise) rotation of the vortex. In the mentioned periods, the vorticity mostly has a positive value. The positive value of the
ADT parameter indicates the inflow of ultra-oligotrophic and highly saline water from the eastern Mediterranean into the Adriatic, which is characterized by low nutrients and lower primary production (Civitarese *et al.*, 2010). When the value of the parameter ADTDifference is negative, the level at the center of the vortex is higher than the level at the edge of the vortex, indicating an anticyclonic (clockwise) rotation. Then, the vorticity mostly has negative values. In anticyclonic periods, the inflow of less oligotrophic water with lower salinity goes from the western Mediterranean into the Adriatic prevails

### 3. Results

In the Gulf of Venice, it was possible to estimate the age of 34 out of 52 processed shells, 19 of which were used in chronology construction. In Pag Bay, a total of 85 shells were processed and it was possible to estimate age for 64 shells, 47 of which were used to construct the chronology. In the Pašman Channel it was possible to estimate the age of 33 out of 37 processed shells, 26 of which were used in chronology construction (Table 1).

<table><caption>Table 1. Overview of the *Callista chione* specimens analysed in this study.</caption><thead><tr><th></th><th></th><th>Gulf of Venice</th><th>Pag Bay</th><th>Pašman Channel</th></tr></thead><tbody><tr><td rowspan="3">Shells used for chronology construction</td><td>N</td><td>21</td><td>48</td><td>27</td></tr><tr><td>L (mm)</td><td>66.5 - 85.5</td><td>62.2 - 81.3</td><td>69.3 - 87.3</td></tr><tr><td>min - max (x̄ ± sd)</td><td>(73.4 ± 3.3)</td><td>(73.4 ± 3.7)</td><td>(76.2 ± 4.7)</td></tr><tr><td rowspan="3">Age (years)</td><td>min - max</td><td>18 - 46</td><td>18 - 41</td><td>21 - 41</td></tr><tr><td>(x̄ ± sd)</td><td>(29.9 ± 8.8)</td><td>(26.3 ± 4.9)</td><td>(26.8 ± 4.8)</td></tr><tr><td>N</td><td>13</td><td>16</td><td>6</td></tr><tr><td rowspan="3">Other shells</td><td>L (mm)</td><td>70.1 - 79.5</td><td>70.0 - 76.9</td><td>56.0 - 88.6</td></tr><tr><td>min - max (x̄ ± sd)</td><td>(72.9 ± 2.4)</td><td>(73.4 ± 2.1)</td><td>(76.2 ± 10.9)</td></tr><tr><td>Age (years)</td><td>15 - 39</td><td>14 - 32</td><td>21 - 33</td></tr><tr><td></td><td>min - max</td><td>(x̄ ± sd)</td><td>(25.4 ± 5.3)</td><td>(22.2 ± 7.8)</td></tr></tbody></table>

Shells used in chronology were of similar size and age compared with those for which only age was estimated. An exception was the case of several younger shells (n=5; <16 years) that were omitted from chronology development. All shells older than 40 were included in our analysis. Pronounced variation was noted in the estimated age of similar sized shells; for example, shells with length from 70 to 80 mm had an estimated age from 20 to more than 40
years (Supplementary Material; Figure S2). The mean correlation between each detrended time series and the average of others (series intercorrelation) for shells from Gulf of Venice was 0.542. The average mean sensitivity which expresses the year-to-year variability of the values in a time series was 0.256. For shells from Pag Bay, the series intercorrelation was 0.579 and mean sensitivity was 0.279, while for the Pašman Channel samples, the series intercorrelation was 0.543 and mean sensitivity was 0.263.

During the first few years of life, shell growth is very rapid and often the annual growth lines are not sufficiently clear, so it is not possible to accurately measure the distances between them. Therefore, the widths of annual growth increments during the earlier ontogeny (~first 5 years) were not measured. Similarly, in samples collected in periods before late summer/early autumn when the annual growth line is formed, last year at the very edge was not measured. Also, due to very narrow growth increments, the positions of annual growth lines at the very edge (late ontogeny) were not sufficiently clear in some specimens and in such cases were not measured.

Data on the width of annual growth increments for *C. chione* specimens collected at the three localities were obtained for the periods showed in Table 2.

Table 2. Overview of the periods of measured annual growth increments for *Callista chione* specimens and constructed master chronologies per localities.

<table><thead><tr><th>Locality</th><th>Measured annual growth increments</th><th>Master chronology period</th></tr></thead><tbody><tr><td>Gulf of Venice</td><td>1997 - 2018</td><td>1986 - 2018</td></tr><tr><td>Pag Bay</td><td>1984 - 2019</td><td>1994 - 2019</td></tr><tr><td>Pašman Channel</td><td>1982 - 2015</td><td>1994 - 2015</td></tr></tbody></table>

**Figure 3.** Individual detrended growth time series of *Callista chione* from; A. The Gulf of Venice (1979-2018), B. Pag Bay (1984-2019), and C. The Pašman Channel (1982-2015). Solid black line represents standard chronology. The growth index varies around 1, with higher values indicating positive wider and lower values indicating negative narrower growth than expected by the model. Sample depth (denoting number of samples, grey shading area), 0.85 EPS threshold (straight dashed line) and calculated EPS (black line) are shown for each sampling locality below corresponding chronology data.
Comparison of the three residual master chronologies obtained for *C.chione* individuals collected from the three localities in the Adriatic Sea was made for the time periods over which each chronology was determined to be suitable for environmental comparison based on EPS~>0.85. A statistically significant correlation was obtained only between the Gulf of Venice and Pag Bay chronologies from 1994 to 2018 (r = 0.607; p <0.001). The correlation between these two localities is supported by the synchrony found in years 2004, 2007, 2014, and 2018 that were characterized by higher growth indexes (wider increments). Likewise, coincidences were also found in the years 2006, 2008, 2012, and 2017 that showed lower growth indexes (narrower increments; Fig. 5). Interestingly, the years 2002, 2006, and 2012 were characterized by low growth for all three localities (Fig. 4).

<figure><img src="image_5.png" /><figcaption>**Figure 4.** Comparison of *Callista chione* residual shell master chronologies from the three sampling localities. The growth index varies around 1, with higher values indicating **wider** growth and lower values indicating **narrower** growth than expected by the model.</figcaption></figure>
<figure><img src="image_6.png" /><figcaption>**Figure 5.** Acetate peels of shells collected in **A. Gulf of Venice, (ITA2)**, and **B. Pag Bay** (PAG39). Full circles indicate wide growth increments, open circles indicate narrow growth increments. Scale bar 100 mm.</figcaption></figure>

No significant correlations were found between the Gulf of Venice shell growth chronology and chlorophyll *a* concentrations in the nearby area of the Northern Adriatic, however, some areas of positive and negative correlation were observed further south of this locality. Pearson's *r* correlations at a 90% significance level (or higher) were observed between the shell master chronologies and chlorophyll concentration for March and April. Positive correlations were observed between shell data for Pag Bay and chlorophyll values at nearby sites for the same months, while for shells from the Pašman Channel significant positive correlation was only found for March (Fig. 6). Comparisons between shell growth chronologies and sea surface temperatures (not shown) showed no significant correlations in any area of the Adriatic for any of the three master chronologies.

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<figure><img src="image_7.png" /><figcaption>**Figure 6.** Correlation maps between shell master chronology and chlorophyll concentration for the Gulf of Venice (1999-2018), Pag Bay (2002-2019) and the Pašman Channel (1996-2015) in March and April. Red circle represents locality of shell collection.</figcaption></figure>

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4. Discussion

4.1. *Callista chione* age estimation

Growth rate and age are widely used biological parameters for the management and conservation of living marine resources. The age of a bivalve can be estimated using surface growth rings or checks that can be clearly seen on the external shell surface (Richardson 2001). They are particularly clear in *C.chione* during early ontogeny, when the rings are widely spaced and easy to identify (Forster, 1981). However, later in ontogeny (>20 years) they are deposited more closely together at the shell margin and are not always easily discernible. Results of this study show that age of individuals of in this species can pronouncedly vary with respect to length, as estimated age of specimens measuring ~ 75 mm shell length ranged from 22 to 45 years (Supplementary Material; Figure S2). Slow growth during late ontogeny and high intraspecies variation in shell growth rates were previously noted for *C.chione* (Ezgeta- Balić *et al.*, 2011), as well as for a number of other bivalves species including for example *Arctica islandica* (e.g. Witbaard *et al.*, 1999, Schöne, 2013), and *Lithophaga lithophaga* (Peharda *et al.*, 2015). Therefore, it is more appropriate to use acetate peel replicas examined under magnification to estimate the age of larger sized *C.chione* individuals, as opposed to size-age relationships, suggested by Ezgeta-Balić *et al.* (2011).

*Callista chione* is a moderately long-lived bivalve that can attain an age of >40 years (Forster, 1981; Ezgeta-Balić *et al.*, 2011). However, according to previous studies it is more common to find populations with individuals showing a maximum age of 16 years (Leontarakis and Richardson, 2005) or 17 years (Hall *et al.*, 1974; Metaxatos, 2004; Moura *et al.*, 2009) have been recorded in most of the studied populations. The population structure of *C.chione* in the Adriatic Sea has been documented by Ezgeta-Balić *et al.* (2011) at four localities along the eastern coast (Rab, Pag Bay, Kaštela Bay and the estuary of the Cetina River); individual ages ranged between 3 and 44 years, and contribution of older specimens in a given population varied pronouncedly with respect to locality. In this study, estimated age ranged from 14 to 46 years and 90% of analysed specimens were over 20 years old. It is important to note that for the purpose of chronology construction, larger individuals with >60 mm in length were chosen. Maximal longevity of 46 years estimated in this study is two years longer than previous estimates for specimens from Rab (Ezgeta-Balić *et al.* 2011). Due to the commercial importance of this species, it is highly likely that larger sized and older specimens have already been selectively removed from the Adriatic populations. Age data is a prerequisite to generate
330 the information on population structure, longevity, mortality, recruitment and fluctuations in fishery, which could contribute to the improvement of the national management plans of the species stock (Pauly *et al.*, 2002).

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<table>
  <tr>
    <td>363</td>
    <td>Sea was estimated at impressive 97 years (Peharda et al., 2019). In our study, the lengths of the constructed master chronologies of C.chione were 32 years for the Gulf of Venice, 25 years for Pag Bay, and 21 years for the Pašman Channel.</td>
  </tr>
  <tr>
    <td>1</td>
    <td></td>
  </tr>
  <tr>
    <td>2</td>
    <td></td>
  </tr>
  <tr>
    <td>3</td>
    <td></td>
  </tr>
  <tr>
    <td>4</td>
    <td></td>
  </tr>
  <tr>
    <td>5</td>
    <td></td>
  </tr>
  <tr>
    <td>6</td>
    <td></td>
  </tr>
  <tr>
    <td>7</td>
    <td></td>
  </tr>
  <tr>
    <td>8</td>
    <td></td>
  </tr>
  <tr>
    <td>9</td>
    <td></td>
  </tr>
  <tr>
    <td>10</td>
    <td></td>
  </tr>
  <tr>
    <td>11</td>
    <td></td>
  </tr>
  <tr>
    <td>12</td>
    <td></td>
  </tr>
  <tr>
    <td>13</td>
    <td></td>
  </tr>
  <tr>
    <td>14</td>
    <td></td>
  </tr>
  <tr>
    <td>15</td>
    <td></td>
  </tr>
  <tr>
    <td>16</td>
    <td></td>
  </tr>
  <tr>
    <td>17</td>
    <td></td>
  </tr>
  <tr>
    <td>18</td>
    <td></td>
  </tr>
  <tr>
    <td>19</td>
    <td></td>
  </tr>
  <tr>
    <td>20</td>
    <td></td>
  </tr>
  <tr>
    <td>21</td>
    <td></td>
  </tr>
  <tr>
    <td>22</td>
    <td></td>
  </tr>
  <tr>
    <td>23</td>
    <td></td>
  </tr>
  <tr>
    <td>24</td>
    <td></td>
  </tr>
  <tr>
    <td>25</td>
    <td></td>
  </tr>
  <tr>
    <td>26</td>
    <td></td>
  </tr>
  <tr>
    <td>27</td>
    <td></td>
  </tr>
  <tr>
    <td>28</td>
    <td></td>
  </tr>
  <tr>
    <td>29</td>
    <td></td>
  </tr>
  <tr>
    <td>30</td>
    <td></td>
  </tr>
  <tr>
    <td>31</td>
    <td></td>
  </tr>
  <tr>
    <td>32</td>
    <td></td>
  </tr>
  <tr>
    <td>33</td>
    <td></td>
  </tr>
  <tr>
    <td>34</td>
    <td></td>
  </tr>
  <tr>
    <td>35</td>
    <td></td>
  </tr>
  <tr>
    <td>36</td>
    <td></td>
  </tr>
  <tr>
    <td>37</td>
    <td></td>
  </tr>
  <tr>
    <td>38</td>
    <td></td>
  </tr>
  <tr>
    <td>39</td>
    <td></td>
  </tr>
  <tr>
    <td>40</td>
    <td></td>
  </tr>
  <tr>
    <td>41</td>
    <td></td>
  </tr>
  <tr>
    <td>42</td>
    <td></td>
  </tr>
  <tr>
    <td>43</td>
    <td></td>
  </tr>
  <tr>
    <td>44</td>
    <td></td>
  </tr>
  <tr>
    <td>45</td>
    <td></td>
  </tr>
  <tr>
    <td>46</td>
    <td></td>
  </tr>
  <tr>
    <td>47</td>
    <td></td>
  </tr>
  <tr>
    <td>48</td>
    <td></td>
  </tr>
  <tr>
    <td>49</td>
    <td></td>
  </tr>
  <tr>
    <td>50</td>
    <td></td>
  </tr>
  <tr>
    <td>51</td>
    <td></td>
  </tr>
  <tr>
    <td>52</td>
    <td></td>
  </tr>
  <tr>
    <td>53</td>
    <td></td>
  </tr>
  <tr>
    <td>54</td>
    <td></td>
  </tr>
  <tr>
    <td>55</td>
    <td></td>
  </tr>
  <tr>
    <td>56</td>
    <td></td>
  </tr>
  <tr>
    <td>57</td>
    <td></td>
  </tr>
  <tr>
    <td>58</td>
    <td></td>
  </tr>
  <tr>
    <td>59</td>
    <td></td>
  </tr>
  <tr>
    <td>60</td>
    <td></td>
  </tr>
  <tr>
    <td>61</td>
    <td></td>
  </tr>
  <tr>
    <td>62</td>
    <td></td>
  </tr>
  <tr>
    <td>63</td>
    <td></td>
  </tr>
  <tr>
    <td>64</td>
    <td></td>
  </tr>
  <tr>
    <td>65</td>
    <td></td>
  </tr>
</table>
and a south-eastward current along the western coast (Western Adriatic Current – WAC, Fig. 1A). The Pašman Channel sampling site is therefore more affected by the inflow of warmer and saline waters coming from the south than the two other sites, as Pag Bay and the Gulf of Venice sampling sites are located in somewhat geographically and hydrographically isolated Adriatic areas. Pag Bay is a part of the deeply indented north-eastern Adriatic coastline, strongly influenced by the severe wintertime outbreaks of cold and dry Bora wind (Grisogono and Belušić, 2009) and local fresh water sources (Zrmanja River and submarine fresh water springs, e.g., Novosel et al., 2002; Šupraha et al., 2011). The oceanographic properties of the northernmost part of the Adriatic are strongly dependent on the Po River discharges and characteristics of the air-sea fluxes, particularly those related to the strong Bora outbreaks, which excite the cyclonic gyres encompassing the area of the sampling site (Orlić et al., 1994; Kuzmić et al., 2006). Additionally, a persistent thermohaline front positioned to the south and southwest of the Istrian peninsula (Istrian Front), separating colder and less saline waters of the northernmost part of the northern Adriatic from the warmer and more saline southern waters, was reported during oceanographic surveys and in model simulations (e.g., Kokkini et al., 2017 and references therein).

### 4.3. Environmental influence on the growth of *Callista chione*

Growth synchrony among *C.chione* specimens collected from the same locality suggests that a common environmental parameter influences individual growth. However, relationships between shell growth and external factors can be complex, especially in shallow coastal environments in semi-enclosed seas such as the Adriatic Sea (Epple et al., 2006). In these areas, local processes, including precipitation, riverine input and terrestrial runoff, may be highly localised (Gillanders, 2005). Some previous sclerochronological studies have identified seawater temperature as one of the main drivers of shell growth. Positive correlations between seawater temperature and bivalve growth have been observed for several bivalve species including *Arctica islandica* (e.g., Marali and Schöne, 2015), *Glycymeris glycymeris* (Reynolds et al., 2013; Royer et al., 2013), and *Glycymeris bimaculata* (Bušelić et al., 2015). Negative correlation between seawater temperature and bivalve growth have also been observed in the case of master chronologies of species *Ciliatocardium ciliatum* in the northwest Barents Sea (Carroll et al., 2014) and species *A. islandica* in the southern Barents Sea (Mette et al., 2016). Some of the studies found very low (e.g., Butler et al., 2013) or time-unstable (e.g., Marali and Schöne, 2015) correlation between seawater temperature and shell growth thus further highlighting the complexity in growth-temperature relationships among and even within
428

species. In the case of *C. chione* master chronologies, no correlations were observed with seawater temperature in the Adriatic Sea.

1

429

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3

430

4

5

Previous studies of *G. pilosa* in the Adriatic Sea have identified the impact of decadal (5

6

431

- 10 years) oscillation of water masses referred to as the Adriatic - Ionian Bimodal Oscillating

7

432

System (BiOS), on populations at the Barbariga and Pašman Channel localities (Peharda *et al*., 2019). BIOS is known to be the dominant driver of the thermohaline and biogeochemical

8

9

oscillations across most of the basin, including southern and middle Adriatic and the shallow

10

433

11

434

northern areas (Civitarese *et al*., 2010; Vilibić *et al*., 2012; Batistić *et al*., 2014; Dautović *et

12

435

13

al*., 2017). However, in the same study, at two southern localities Živogošće and Drače, growth

14

436

of *G. pilosa* was influenced more by the local factors. In this study, no correlations of *C. chione*

15

437

16

master chronologies and parameters describing BIOS were observed.

17

438

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19

439

20

In this study, positive and negative correlations between shell growth chronologies and

21

440

22

nearby chl a values were observed for the three different locations. Although satellite

23

441

24

chlorophyll a data provide insights into state of phytoplankton communities in an area, this

25

442

26

does not monitor sudden changes of conditions in enclosed bays or straight channels between

27

443

28

islands (Kirk, 2011). A previous study of trophic ecology of the *C. chione* conducted in Pag

29

444

30

Bay and the Cetina River estuary showed that the diet differs between localities (Purroy *et al*., 2018a). According to Purroy *et al*.

31

445

32

2018a). According to Purroy *et al* (2018a), for the bivalves in Pag Bay the most important

33

446

34

food source are particles deposited on sediment, while in the estuary of the Cetina River the

35

447

36

most important food source is suspended particulate matter. Correlation maps obtained in our

37

448

38

study indicate different relationships between the shell master chronology and chlorophyll a

39

449

40

concentration in the region. Significant correlations were mostly limited to March and April

41

450

and showed spatial variations. However, the environmental variables that influence bivalve

42

451

43

growth can vary over fine spatial scales, especially in coastal environments in semi enclosed

44

452

seas where local processes can be highly localized (Gillanders, 2005). While no direct influence

45

453

45

of environmental data on the growth of bivalve *C. chione* were observed, results in this study

46

454

47

highlight the need to combine sclochronological analyses with ecological studies and in situ

48

455

49

measurements of parameters such as food availability and quality to understand life history

50

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51

traits of bivalves as archives of environmental variables.

52

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53

Acknowledgments

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65
458 The authors are grateful to Mario Zokić, Cristina Breggion, Filip Bukša, Ivica Matijaca and Ariadna Purroy for their help with collection of samples. Research has been supported by the Croatian Science Foundation under the project BivACME (IP-2019-04-8542).

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Adriatic Sea. Helgol. Mar. Res. 65(4), 457–465. https://doi.org/10.1007/s10152-010-

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France. *PLoS One*. 12(12), e0189782. https://doi.org/10.1371/journal.pone.0189782

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CREDIT author statement

Hana Uvanović, Melita Peharda: Conceptualization

Hana Uvanović, Melita Peharda, Nicole Pavin, Julien Thébault, Carlotta Mazzoldi, Hrvoje Mihanović
and Ivan Župan: Methodology

Hana Uvanović, Melita Peharda: Writing- Original draft preparation

Hana Uvanović, Julien Thébault: Visualization

Hana Uvanović, Melita Peharda, Nicole Pavin, Julien Thébault, Carlotta Mazzoldi, Hrvoje Mihanović
and Ivan Župan: Writing- Review & Editing
**Declaration of interests**

[x] The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

[ ] The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: