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MASS MORTALITY IN NOAH'S ARK ARCA NOAE (LINNAEUS, 1758): A CASE STUDY FROM THE STRAIT OF MESSINA (MEDITERRANEAN SEA).

INTRODUCTION

Noah's Ark Arca noae (Linnaeus, 1758) is an edible clam that is widely distributed in hard and detrital subtidal bottoms in the eastern Atlantic and Mediterranean Seas and may reach densities of up to 13 individuals [m.sup.-2] in the Adriatic Sea (Peharda et al. 2002a). In the Mediterranean, Noah's Ark is widely exploited along the Adriatic eastern coasts (Benovic 1997), especially in Croatia, where the increased market demands tied to tourism have intensified the harvesting pressure on the natural stocks (Peharda et al. 2003, 2006). Although of minor interest in other Mediterranean localities (Batzios et al. 2003, Voultsiadou et al. 2010). if harvest increases then Noah's Ark might become a case of overexploited "niche products" (Hrs-Brenko 1980), similar to the cogeneric turkey-wing ark, Arca zebra in Venezuela (Miloslavich & Huck 2009) and other Arcidae worldwide (Stern-Pirlot & Wolff 2006).

The increased interest of the market toward this species has promoted investigations on the Adriatic populations, with a special focus on growth, age, and population structure (Peharda et al. 2002a, 2002b. 2003, 2009). as well as condition index (Peharda et al. 2003), reproductive cycle (Peharda et al. 2006), predation by gastropods (Morton et al. 2007). functional morphology (Morton & Peharda 2008), trophism (Peharda et al. 2012). and potential employment in aquaculture (Zupan et al. 2014). Sanitary risks linked to the consumption of ark mussels have been preliminarily investigated by Martinez Nazaret and 'Villalobos de Bastardo (2005) for the west Atlantic Arca zebra and by Topic Popovic et al. (2010) for Arca noae.

A catastrophic event of unknown origin caused the collapse of the Croatian ark fishery in the late 1940s (Hrs-Brenko 1980). After such a crucial event, mortalities of several taxa and Noah's Ark have been recorded in the Mediterranean Sea from 1981 to 1983 (Meinesz & Mercier 1983). Extensive mass mortality of rocky benthic macroinvertebrate species, including Arca noae. was observed in the northwestern Mediterranean region during the summer of 2003 after an exceptional heat wave (Garrabou et al. 2009).

In the Strait of Messina (central Mediterranean), mass mortalities of Arca noae have been recorded in the last decades (Giacobbe, unpublished data), together with some minor events, patch-distributed in the nearby Ionian and Tyrrhenian coasts. Such recurrent mass mortalities of A. noae, although occasionally reported, were never investigated in the past years because of their rapid and unforeseeable evolution (Table 1). In the spring of 2007, a large number of ark empty shells were observed and promptly sampled along the Sicilian coast of the Strait of Messina.

In this article, the population structure of such subtidal shell deposits are described and compared with living specimens from a nearby live population. The aims of the study were to understand if the sampled death assemblage is descriptive of the original population, if it may be traced to a mass mortality episode.

MATERIAL AND METHODS

Sampling and Morphometric Determinations

Periodic observations of mass mortalities in the Strait of Messina, revealed by a large amount of washed ashore clams, abalones, cowries, and Noah's arks (Giacobbe, unpublished data) led to undertaking a monitoring program that started in the summer of 2002. In the spring of 2007, large piles of empty shells were observed along the Sicily side of the Strait of Messina that allowed a timely documentation of a potential mass mortality event, which was preliminarily surveyed by SCUBA divers at 12 sites along 10 km of coast (Fig. 1). Sampling of dead Arca noae shells was haphazardly and manually collected on May 21st and 25th offshore from the villages of Ganzirri (Station A: 38.25802 N, 15.61913 E) and Torre Faro (Station B: 38.25995 N, 15.62915 E) at 4-5 m depths. No live animal was observed in these sites. The two samples of A. noae empty shells were compared with the nearest living population, found on November 30, 2007, almost 25 km westward in Tyrrhenian waters (Station C: 38.24444 N, 15,43371 E) (Fig. 1). From this population, live specimens were collected from concrete blocks, 1-3 m depth, by scraping all the arks from a 1-[m.sup.2] surface (18 [m.sup.2] total area). Once collected, the specimens were maintained in cooled and aerated water and transported rapidly to the laboratory.

In the laboratory, after removing the encrusting organisms, the shells were treated with 3% hydrogen peroxide to eliminate any residues of organic matter and dried at 40[degrees]C. Living specimens from C station have been preliminarily frozen to facilitate soft tissue removing. The shell length (SL), shell height (SH), and shell width (SW) were measured by caliper (Palmer, [+ or -]0.5 mm) according to Peharda et al. (2003). Individual shell dry weight (SWt, 0.1 g) was measured using the Pioneer PA4102C electronic balance (Table 2).

The specimen age was estimated from the number of pallial impressions on the inner shell surface (number of years) plus an eventual dark band on the edge (half year), according to Peharda et al. (2002a, 2002b).

Data Analysis

The shell length, height, width, and weight frequency distributions from each station were compared using the Kolmogorov--Smirnov test (Sokal & Rohlf 1995).

The relationship between the total SL and total SWt was determined for shells at each station. The linear regression assumptions were checked with the analysis of residuals. The relationships were determined according to the equation Y = a x [X.sup.b], where Y is the total SWt, X is the independent variable (total SL), a is the intercept, and b is the slope: a and b are estimated by the least squares method (Mystat software). The departure from the isometric condition ([H.sub.0]: b = 3, Sparre & Venema 1998) was tested using a Student's t-test. The differences between stations were tested by an analysis of covariance (using SL as the covariate).

The von Bertalanffy Growth Function (VBGF) was fit to the size-at-age data derived from the number of pallial impression as follows:

[SL.sub.t] = [SL.sub.[infinity]][1 - exp - K(t - [t.sub.0])],

where SL, is the length-at-age t, [SL.sub.[infinity]] is the asymptotic length, K is a measure of the growth rate (the rate at which [SL.sub.[infinity]] is approached), and [t.sub.0] is the theoretical age at L = 0. The growth performance index was calculated according to the following formula (Pauly & Munro 1984):

[phi]' = log(K[degrees]) + 21og([SL.sub.[infinity]]),

where K and [SL.sub.[infinity]] are the parameters of the VBGF.

RESULTS

Notable ark shell deposits in the Strait of Messina were recorded in May 2007 at all 12 surveyed stations along 10 km of coastline. A total of 445 specimens were collected (264 from station A and 181 from station B). All specimens had articulated valves with an elastic ligament. A total of 138 live specimens were obtained from station C (Tyrrhenian Sea), whose mean population density was estimated at 7.7 [+ or -] 4 individuals [m.sup.-2].

The descriptive statistics are included in Table 2. The SL, SH, SW, and SWt distributions for sites A and B were not significantly different (D: 0.11-0.13, 0.05); consequently, the data from both sites were pooled and considered a single population (dead population) to compare with the live specimens from site C. The SL frequency distributions (Fig. 2) showed multimodal trends for both dead (A + B) and living (C) populations and found to be significantly different between the combined dead and live samples (D = 0.35; P < 0.01).

The relationship between SWt and SL calculated for 442 specimens (two outliers of station A and one of station B were excluded via residual analysis), showed a slight difference between sites A and B (b = 2.703 and b = 2.713. Table 3). A significant difference (P < 0.01) was detected between dead and live (b = 2.441) populations. The Arca noae shells also showed a significant (P < 0.01) negative allometry (b < 3) for all sites (Table 3).

The number of pallial impressions on the inner shell surface suggested the identification of the six and seven age groups for dead and live specimens, respectively, with the age class 3.5 y most represented in both samples (Fig. 3).

The estimated parameters for the VBGF (Table 4) indicated that specimens from the Strait of Messina (sites A and B) might reach a theoretically greater SL with respect to the Tyrrhenian specimens (site C).

DISCUSSION

The occurrence of Noah's Ark mass mortalities, recorded in past years in the Strait of Messina, is supported by substantial deposits of empty shells whose multimodal distribution of shell size frequency is in accordance with those described for catastrophic mortality (Powell et al. 1986, 1989) and substantially reflected patterns observed among the living population. The mass mortality event, in fact, did not affect the nearby Tyrrhenian waters, which provided a comparison population whose density was slightly less than the maximum known for this species (Peharda et al. 2002b).

The population structure of death assemblages after a mass mortality has rarely been described in literature (Tsuchiya 1983). although it has been widely debated in the paleontological field (Kidwell & Bosence 1991). In the present case of sessile bivalves displaced from the natural hard substrate, the articulated valves indicated that sampling has been promptly performed before shell reworking and redistribution (Powell et al. 1989). Statistical analysis supports that the articulated shells sampled 1 km apart from each other were representative of a single widespread population. By contrast, live and dead specimens showed significant differences in shell morphology which might be related to the local wave exposure and hydrodynamic energy levels (Steffani & Branch 2003).

In both populations, the wide variability in size for each age group agreed with a multispawing phase, reported from April to August (Peharda et al. 2006) and it could also indicate a wide range of growth rate for individuals from a single recruitment.

The [SL.sub.[infinity]] (116 and 90 mm) reported here are higher than maximum observed length in the samples (58 and 68 mm) but lower than the maximum reported length of Arca noae (SL = 120 mm; Puljas et al. 2015). The difference between maximum observed and [SL.sub.[infinity]] may be explained by the high occurrence of young specimens in both populations (dead and living).

The lifespan of both (dead and living) populations was shorter than untouched (Puljas et al. 2015) as well as exploited ark clam beds (Peharda et al. 2006), which might be attributed to natural mortalities. Arca noae is confirmed be a relatively slow growing species. Values of growth constant obtained in the present study (0.9 and 0.11 [y.sup.-1]) are similar to those reported in the Adriatic Sea (0.15-0.17 [y.sup.-1]; Peharda et al. 2002b). The growth rate was about 9-7 mm [year.sup.-1] till 2-3 y of age after that it gradually decreased until 6-7 y (1.5 mm [year.sup.-1]).

Mass mortalities of benthic organisms have been reported in the Mediterranean both at regional and local scales. Episodes occurring at the scale of basins were generally attributed to climatic constraints, as those related to global warming processes (Bijma et al. 2013) and relative effects, as an increased onset of hypoxic-anoxic conditions (Diaz & Rosenberg 2008), and higher vulnerability to disease (Bally & Garrabou 2007). By contrast, local episodes have often been traced to direct anthropogenic disturbance (Moore et al. 1997). Nevertheless, patch-distributed episodes may be linked to regional events, as described for a partial mortality of gorgonians in the Strait of Messina that has been recognized as a local expression of events acting at regional and global scales (Mistri & Ceccherelli 1994). Similarly, the recorded mass mortality of Noah's Ark, without any evident anthropogenic causes, might be viewed in the context of a generalized but irregularly documented phenomenon that affected the Mediterranean ark populations since 1980.

Moreover, a link with thermal anomalies can be excluded in this case because of the peculiar upwelling regime that cools the surface waters in the Strait of Messina, which consequently are poorly influenced by air temperature variations. In May 2007, however, temperatures ranged from 15 to 18[degrees]C, similar to the temperatures in 2006 and 2008 (Rosa et al. 2013).

Observational data about recurrent mass mortalities affecting sessile bivalves (i.e., Noah's ark) are supported by a quantitative analysis of the related empty shell assemblages. Such assemblages resulted in a well-documented description of actual Noah's ark population, thus representing a valuable case study of mass mortality.

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TERESA BOTTARI, (1) GIUSEPPA SCARFI (2*) AND SALVATORE GIACOBBE (2)

(1) Institute for Coastal Marine Environment (IAMC), National Research Council (CNR), Spianata S. Raineri 86. 98122 Messina, Italy; (2) Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale F. Stagno d' Alcontres 31, 98166 Messina, Italy

(*) Corresponding author. E-mail: gscarfi@unime.it

DOI: 10.2983/035.036.0324
TABLE 1.
Mortality events Area noae recorded in the Strait of Messina (and
neighboring areas).

Year    Site                         Notes

1977    The Strait of Messina        Mass mortality and stranding of
                                     bivalves and gastropods
1983    The Strait of Messina        Mass mortality of A. noae
1985    Tyrrhenian Sea (Sicily)      Patch-distributed mortality of
                                     bivalves and sea urchins
1987    Messina Strait and close     Mass mortality of A. noae and other
        Ionian Sea                   bivalves
1992    Messina Strait and close     Mass mortality of A. noae and other
        Tyrrhenian Sea               bivalves
1997    Tyrrhenian Sea (Sicily)      Patch-distributed mortality of
                                     bivalves, crabs, and sea urchins
2007    The Strait of Messina        Mass mortality of A. noae and other
                                     bivalves
2009    Tyrrhenian Sea (Sicily       Patch-distributed mortality of
        and Calabrian)               bivalves, crabs, and sea urchins
2015    Tyrrhenian Sea (Sicily)      Patch-distributed mortality of
                                     bivalves, crabs, and sea urchins

TABLE 2.
Descriptive statistics of the empty shell samples of Ana noae used in
the present study.

                               SL (mm)                  SW (mm)
Station   Status   N      Range     Mean    SD     Range    Mean    SD

A         Dead     264   12    52   32.6     8.1   5   26   15.1    3.7
B         Dead     181   10    58   31.8    10.0   5   27   15.1    4.9
C         Live     138   12    68   41.0    10.4   6   35   23.0    5.6

                    SH (mm)                 SWt (g)
Station    Range    Mean   SD      Range      Mean    SD

A          5   22   13.4   2.8   0.1    9.5   2.5     1.6
B          4   20   13.2   3.8   0.1    8.8   2.6     2.0
C          6   31   19.0   4.4   0.2   19     6.9     4.1

SL, shell length; SW, shell width; SH, shell height; SWt, shell weight.

TABLE 3.
Relationships between SL and SWt of Arca noae.

Station    Status    N       SL range    SWt range     a         b
                             (mm)        (g)

A          Dead      262    12   52      0.1    9.5    -8.664    2.703
B          Dead      180    10   58      0.1    8.8    -8.622    2.713
C          Live      138    12   68      0.2   18.6    -7.233    2.441

Station    SE (b)    [R.sup.2]    t-test        ANCOVA
                                  (isometry)

A          0.036     0.956        0.01          0.01
B          0.036     0.970        0.01
C          0.075     0.884        0.01

N, number of specimens; a. intercept; b, allometry coefficient; SE,
standard error; [R.sup.2]. determination coefficient; probability of
Student's t-test for differences between allometry coefficient b and
"3" (i.e., isometric condition): ANCOVA, analysis of covariance.

TABLE 4.
Estimated parameters of the VBGF for Arca noae in the Strait of Messina
and Tyrrhenian Sea.

Station    Status     N      [SL.sub.[infinity]]    K ([y.sup.-1])

A-B        Dead       445        116                  0.09
C          Live       138         90                  0.11

Station    -[t.sub.0](y)    MSE      [phi]'

A-B          -0.76          22.5     3.083
C            -1.56          52.8     2.950

N, number; [L.sub.[infinity]], theoretical maximum (asymptotic) total
shell length; K, growth coefficient; -[t.sub.0] theoretical age at zero
length; MSE, mean square error; [phi]', growth performance index.
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Author:Bottari, Teresa; Scarfi, Giuseppa; Giacobbe, Salvatore
Publication:Journal of Shellfish Research
Article Type:Case study
Geographic Code:0MEDI
Date:Dec 1, 2017
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