Annual shell growth increment formation in the deep water Patagonian scallop Zygochlamys patagonica.

ABSTRACT The Patagonian scallop Zygochlamys patagonica occurs on the SW Atlantic shelf of South America between 36[degrees]S to 55[degrees]S in beds at depths around 100 m. Stable oxygen and carbon isotope ratio analysis in scallops from four large beds (Uruguay, 36[degrees]17'S, Reclutas, 39[degrees]20'S, Tango B, 42[degrees]30'S, and Beagle, 55[degrees]10'S) in combination with condition indexes and oceanography date strongly suggest that shell growth increments in this species are formed annually. Most translucent growth bands coincide with low values of both [[delta].sup.13]C and[[delta].sup.18]O (i.e., they are formed at times of high remineralization activity and of higher water temperature). This pattern is consistent throughout the distributional range. Given the specific Argentinean shelf oceanography, higher temperatures at this depth occur during austral autumn--beginning winter in the region of Reclutas and Tango B bur during summer-autumn at the northern and southern limit of the distributional range. Year- round investigations at Reclutas beds indicate that translucent shell growth bands coincide with a pause in somatic growth during austral winter, when energy investment is shifted from somatic growth to gonad development.

KEY WORDS: Zygochlamys patagonica, scallops, stable isotope analysis, shell growth increments, age

INTRODUCTION

Individual age and growth are key parameters in stock assessment and thus in sustainable management of commercially important shellfish (Orensanz et al. 2006). The reliability of many size-at-age keys presently used, however, is questionable owing to (i) inconsistent and/or inappropriate ageing techniques, (ii) no validation of the key, or (iii) the untested application to populations living under different environmental conditions (Roy et al. 1998).

In ecosystems with seasonal oscillation in temperature and/ or in primary production, stable oxygen and carbon isotope ratios ([[delta].sup.18], [[delta].sup.13]C) can be used to confirm growth seasonality in calcareous species such as molluscs (see Forester et al. 1973, Krantz et al. 1987, Wefer & Berger 1991). Carbonates are precipitated under oxygen isotope equilibrium with ambient water in most mollusc species (Epstein et al. 1953, Grossman & Ku 1986, Tanabe & Oba 1988, Owen et al. 2002), i.e., shell [[delta].sup.18]O values and water temperature are linearly correlated and hence shell [[delta].sup.18]O is a proxy of water temperature at shell formation, see paleotemperature equations of Epstein et al. (1953) or Owen et al. (2002). [[delta].sup.18]O shell profiles have been used to validate the annual formation of growth bands in a number of bivalve species, such as Eurhomalea exalbida (Lomovasky et al. 2002), Laternula elliptica (Brey & Mackensen 1997), Adamussium colbecki (Heilmayer et al. 2003), Phacosoma japonicum (Schone et al. 2003) and Arctica islandica (Schone et al. 2004). The variation of [[delta].sup.13]C in shell carbonate is more difficult to interpret because of the interaction of physico-chemical and biological processes (McConnaughey et al. 1997, Owen et al. 2002). The major signal generator in shell carbonate [[delta].sup.13]C is the stable carbon isotope composition of dissolved inorganic carbon (DIC) that, on its part, reflects the annual cycle of phytoplank ton production and degradation (Wefer & Berger 1991, McConnaughey et al. 1997). Water temperature (Rubinson & Clayton 1969, Romanek et al. 1992) and biological effects (kinetic fractionation) associated with the metabolically produced C[O.sub.2] (Tanaka et al. 1986, Khim et al. 2000, Owen et al. 2002) are of significance, too.

The Patagonian scallop Zygochlamys patagonica (King & Broderip 1832) is an important economic resource in the SW Atlantic (Lasta & Bremec 1998, Lasta & Bremec 1999). It inhabits the shelf (40-200 m; Waloszek & Waloszek 1986, Lasta & Zampatti 1981, Defeo & Brazeiro 1994, Gutierrez & Defeo 2003; occasionally down to 960 m, Waloszek 1991) throughout southern coastal South America. It occurs from the southern tip of South America to the island of Chiloe (42[degrees]S) along the Pacific coast (Valladares & Stotz 1996), and to Uruguayan waters (36[degrees]S) along the Atlantic coast (Defeo & Brazeiro 1994, Gutierrez & Defeo 2003). On the Pacific shelf, beds occur in shallow waters above 25 m (Andrade et al. 1991), whereas on the Atlantic shelf the large beds are situated along the 100 m isobath (Defeo & Brazeiro 1994, Lasta & Bremec 1998), matching the location of three major oceanic frontal systems of this region (Bogazzi et al. 2005). These frontal zones resemble high productivity areas with maxim in nutrients, phytoplankton and chlorophyll-a (Carreto et al. 1995, Brown & Podesta 1997), and coincide spatially with aggregations of zooplankton, fish and scallops (Podesta 1990, Brunetti et al. 1998, Brunetti et al. 2000, Thomson et al. 2001, Acha et al. 2004, Bogazzi et al. 2005, Ciocco et al. 2006).

Present size-at-age keys for Z. patagonica are quite different and thus inconclusive, most likely owing to differences in the methods used, such as growth increment identification on the shell surface (Waloszek & Waloszek 1986, Lasta et al. 2001, Defeo & Gutierrez 2003), internal growth increments (Waloszek & Waloszek 1986, Bizikov & Middleton 2002, Lomovasky et al. 2004b, Lomovasky et al. 2005) and growth increment validation using monthly sampling of terminal growth stage or stable isotope analysis ([[delta].sup.18]O, Lasta et al. 2001). Thus, the purpose of our study is to provide reliable estimates of Z. patagonica age and growth to facilitate the management of the Atlantic populations. We combine up-to-date techniques of ageing and age validation with oceanography data to analyze and validate individual age and growth patterns in this species from four large beds across its SW Atlantic distributional range.

MATERIALS AND METHODS

Sampling

Zygochlamys patagonica was sampled from the 4 scallop beds "Uruguay" (36[degrees]17'S 53[degrees]49'W, 108-109 m water depth), "Reclutas" (39[degrees]25'S-55[degrees]56'W, 101-110 m), "Tango B" (42[degrees]30'S-59[degrees]05'W, 96-118 m) and "Beagle" (55[degrees]10'S66[degrees]05'W, 112 m; Fig. 1). Samples were collected with a 2.5 m wide dredge except at Beagle, where a bottom otter trawl (foot rope 22 m, net and cod-end 10 cm mesh size) was applied. The initial and final positions of each trawl were registered (using GPS; precision: [+ or -] 60 m). Depth was recorded by an echo sounder (precision: [+ or -] 1 m). Scallops were collected and frozen at -20[degrees]C until further examination. In the laboratory, epibionts were gently brushed off the shell surface. We measured shell height (SH, umbo to the ventral margin), and determined gonadal mass (GM) and adductor muscle mass (AMM; all parameters with precision [+ or -] 0.01).

[FIGURE 1 OMITTED]

Growth Increment Reading and Stable Isotope Analysis

The shell surface of Z. patagonica displays "external" growth increments separated by narrow growth "lines". They correspond to an "internal" pattern of alternating wide opaque and narrow translucent growth bands visible in shell cross sections (see Lomovasky et al. 2004b, Lomovasky et al. 2005). These bands represent periods of fast (opaque) and slow or even halted shell growth (translucent), see Rhoads & Lutz 1980. The number of "external" growth lines visible on the shell surface was determined by stereomicroscope.

We used shell carbonate [[delta].sup.18]O and [[delta].sup.13]C to test whether shell growth increments were formed annually in Z. patagonica after previous attempts of Jones et al. (1983), Krantz et al. (1984), Donner & Nord (1986), Brey & Mackensen (1997) and others. For isotope analysis, we drilled carbonate samples of [+ or -] 50 [micro]g each from the outer shell surface along the axis of maximum growth in shell height of three individuals from each bed (five from Reclutas; all mature individuals) in an equally spaced dorsal-to-ventral series using small dental drills (bit size 500 [micro]m or 300 [micro]m). To determine the spatial position of each carbonate sample with respect to the growth band pattern, subsequently each valve was sectioned along the isotope sample transect. Both the growth band pattern and the drill dents were visible on acetate peels replicates prepared from the cut surface (following Rhoads & Lutz 1980).

Stable oxygen and carbon isotope composition was determined with a Finnigan MAT251 mass spectrometer coupled to an automatic carbonate preparation device. The precision of measurements was better than [+ or -] 0.08 [per thousand ]for [[delta].sup.18]O, and [+ or -]0.06 [per thousand] for [[delta].sup.13]C based on routine measurements of a laboratory working standard. Data are related to the Pee Dee belemnite (PDB) standard through repeated analyses of National Bureau of Standard (NBS) isotopic reference material 19 (Hut 1987) by

[delta] = [([R.sub.sample]/[R.sub.standard]) - 1] x 1,000

where [R.sub.sample] and [R.sub.standard] are the isotopic relationship of the sample and of the standard, respectively.

Timing of Growth Band Formation

To examine whether translucent growth bands are formed annually and within one certain period during the annual cycle of temperature and primary production, we analyzed whether band position corresponds to a particularly high or low stable isotope ratio. The position of each isotope sample was determined as either on a growth band ("on-line," 1) or between growth bands ("off-line," 0). To enable statistical analysis across the 14 individuals, both individual differences in average stable isotope ratio and trends in individual data series were removed by fitting a flexible polynomial model (cubic spline fit) to each individual isotope ratio series (software JMP 5.1 by SAS Institute Inc. 2003) and the residuals ([R.sub.[delta]]O and [R.sub.[delta]]C, respectively) were used for further analysis.

Given the decrease of annual growth increment with age, growth increments become more and more narrowly spaced towards the shell edge (see Lomovasky et al. 2004b, Lomovasky et al. 2005). In 8 of the 14 shells this caused a sample resolution problem: two or three adjacent isotope samples were situated on adjacent translucent growth bands with no "off-line'" samples in between (i.e., each of these samples may also include shell mate rial from in between opaque areas). Thus we excluded all those "on-line" samples from statistical analysis, which were not separated from the next "on-line" sample by at least one "off-line" sample. A total of 291 isotope samples was obtained from the 14 shells (Table 1), 174 samples were situated "off-line" and 89 samples were situated "on-line" 26 "on-line" samples had to be excluded from further analysis as they were directly neighbored to another "on-line" sample.

We applied analysis of variance (two-way ANOVA) to evaluate differences in [[delta].sup.18]O and [[delta].sup.13]C, respectively, between "on-line" samples on growth increments and samples off growth increments, and for potential effects of scallop bank and of individual on this pattern (Zar 1999).

The intraannual [[delta].sup.18]O range was computed as the difference between the maximum and the minimum value in the series of [[delta].sup.18]O collected from one growth increment (i.e., between one growth line and the next) but only for such increments with >2 subsequent samples. The null hypothesis of no differences in intraannua1 [[delta].sup.18]O between beds was tested by one-way ANOVA (Zar 1999).

Condition Indexes

Monthly scallop samples from "Reclutas" (Jan. to Dec. 2000, n = 1,346, Fig. 1) were used to establish the annual cycle of gonad and adductor muscle development. Individual gonad and muscle condition indices (CI) were computed from shell height (SH), gonad mass (GM) and adductor muscle mass (AMM) of adult individuals (>45 mm SH, n = 962; Campodonico et al. 2001). Individual CI was computed by the relationship Mass/[Height.sup.b], where b is the exponent of the corresponding overall size-mass relation, and normalized to a relative condition index (RCI) = (CI - mean CI)/S.D. of CI (see Lasta et al. 2001, for details). Month-to-month differences in gonad and adductor muscle RCI were analyzed by one-way ANOVA and subsequent posthoc test to identify differences between means (Tukey HSD; Zar 1999).

Physical Parameters

From the INIDEP (Instituto Nacional de Investigacion y Desarrollo Pesquero) oceanographic database and the NODC's World Ocean Database 2001 (WOD01) we extracted those oceanographic data profiles situated within geographical boxes of 0.4[degrees] latitude x 0.4[degrees] longitude around the center of each of the four scallop beds and sampled between 1955 and 2005. A total of 229 hydrographic profiles were available, 192 of these were provided by the INIDEP database. 179 stations were sampled by calibrated CTD (conductivity, temperature, depth), 37 by BT (bathythermograph) and 16 stations by discrete water bottles. Within each box we computed the monthly average temperature in the 90-120 m depth layer from all corresponding data to obtain the annual bottom water temperature cycle at the site of each scallop bed. Seasonal development of water column stratification was described by vertical temperature profiles (0-100 m depth) computed for summer (January to March), autumn (April to June), winter (July to September) and spring (October to December) in each box. Vertical resolution was 5 m at Beagle and 1 m at the other three sites.

RESULTS

Stable Isotope Analysis and Timing of Growth Increment Formation

Two-way ANOVA (dependent variable versus on/off-line and scallop individual; and versus on/off-line and scallop bed, respectively) revealed no significant effect of individual scallops or scallop bed on either [R.sub.[delta]O] or [R.sub.[delta]C] (P > 0.05). "On- line" samples exhibited significantly lower values in both [R.sub.[delta]O] (-0.081 versus 0.032, P < 0.001) and [R.sub.[delta]C] (-0.030 versus 0.011, P = 0.021) compared with "off-line" samples (Fig. 2). Hence, translucent growth bands are formed when temperature is comparatively high ([[delta].sup.18]O is low) and the lighter carbon isotope [sup.12]C is over-represented in the near bottom carbonate system ([[delta].sup.13]C is low).

[FIGURE 2 OMITTED]

According to the paleotemperature equation of Epstein (1953), temperature amplitude of 1[degrees]C to 3[degrees]C causes an amplitude in [[delta].sup.18]O of about 0.25-0.77 [per thousand]. This corresponds well to the observed intraannual [[delta].sup.18]O range measured in shells from all beds, 0.2-0.7 (Fig. 3). No difference in the intraannual [[delta].sup.18]O range was observed between beds (one-way ANOVA, P = 0.57).

Condition Indexes

Both gonad and adductor muscle relative condition index at Reclutas show distinct albeit out-of-phase annual cycles (Fig. 4). July to September (austral winter) is the time of highest gonad RCI, and December to April (summer, early autumn) is the time of lowest gonad RCI (Fig. 4a). Adductor muscle RCI shows just the opposite picture, July to September is the time of lowest, and November to April is the time of highest values (Fig. 4b; Tukey HSD, P < 0.05).

Physical Parameters

Annual average temperature in 90-120 m water depth decreases from north to south (8.3[degrees]C at Uruguay, 6.2[degrees]C at Reclutas and Tango B, 7.5[degrees]C at Beagle). The annual temperature amplitude is 2[degrees] to 3[degrees]C at the 3 northern sites and about 4.5[degrees]C at Beagle. Maximum bottom water temperatures are attained in autumn (March to June, 8.85 [+ or -] 0.76[degrees]C) in Uruguay, in autumn and early winter (May to July, 6.57 [+ or -] 0.41[degrees]C) in Reclutas and Tango B, and in summer (January to May, 8.5 [+ or -] 0.43[degrees]C) in Beagle (Fig. 5). Minimum temperatures are attained in winter end-beginning of spring at all 4 sites (September to November, Uruguay: 5.85 [+ or -] 0.3[degrees]C, Reclutas and Tango B: 7.5 [+ or -] 0.37[degrees]C and Beagle: 5.7 + or -] 0.7[degrees]C).

[FIGURE 3 OMITTED]

Water column stratification (Fig. 5, profiles) shows a distinct north-south gradient: The seasonal change in stratification is very distinct at Uruguay and nonexistent at Beagle. Strength of summer stratification decreases from north to south, too, as indicated by the summer temperature gradient between zero and 100 m that is 14[degrees]C at Uruguay and nil at Beagle.

DISCUSSION

Stable oxygen and carbon isotope ratio analysis in combination with condition indexes and oceanographic date demonstrate that in Zygochlamys patagonica translucent shell growth bands are formed annually (Fig. 2). Against the background of shell growth patterns in many temperate bivalve species, however, it appears to be quite uncommon that growth ceases during the time of highest water temperature. Temperature itself is known to be one major controlling factor of metabolism and thus of shell growth (Grizzle & Lutz 1988, Jones et al. 1990). Metabolic rate and shell growth decrease both towards the lower and the upper physiological temperature limit (e.g., Ansell 1968), most likely owing to oxygen limitation at the cellular level (Portner & Knust 2007). So, is the maximum water temperature (<10[degrees]C across all four sites, Fig. 5) experienced by Z. patagonica already within the physiologically critical range? Heilmayer (2004) found that standard metabolic rates of Z. patagonica from Reclutas were slightly (albeit insignificantly) higher at 9[degrees]C compared with 6[degrees]C (i.e., there is evidence that the observed maximum temperature is below the critical range and thus unlikely to be the trigger for shell growth cessation.

Besides temperature, food availability and differential energy allocation are the major determinants of growth. Seasonal oscillation in food supply can cause seasonal oscillation in growth with very slow or even no growth at rimes of lowest food availability (Green 1973, Beukema & Desprez 1986, Beukema & Cadee 1991, Kube et al. 1996, Arneri et al. 1998). Differential energy allocation in somatlc (including shell) and gonad production is another common source of seasonal oscillation in shell growth of bivalves (e.g., MacDonald & Thompson 1986a, Thompson 1986b, Thompson 1988, Lomovasky et al. 2004a, Thompson & MacDonald 2006). The out-of-phase annual cycles of both gonad and adductor muscle relative condition index in Z. patagonica at Reclutas (Fig. 4; see also Lasta et al. 2001) point in this direction. Soma is built in summer and early autumn (November to March), whereas gonads are produced in late autumn and winter (July to September), as confirmed by monthly histological analysis (Campodonico et al. 2001). Such out-of-phase cycles in gonadal and somatic growth appear to be common in pectinids (e.g., Argopecten irradians, Barber & Blake 1981, Bricelj et al. 1987a, Bricelj et al. 1987b; A. purpuratus, Martinez & Mettifogo 1998; Chlamys opercularis, Taylor & Venn 1979; C. septemradiata, Ansell 1974; Euvola (Pecten) ziczac, Lodeiros & Himmelman 2000; Patinopecten caurinus, MacDonald & Bourne 1987; Placopecten magellanicus, Robinson et al. 1981, MacDonald & Thompson 1988; Pecten maximus, Comely 1974). Moreover, the simultaneous increase in gonad condition and decrease in soma condition, as observed between May and August in Z. patagonica (Fig. 4), indicate a reallocation of energy from soma to gonad. Thus, the formation of the translucent shell growth band in Z. patagonica indicates a slow down in shell growth corresponding to the shift from somatic to gonad growth, as observed in other pectinids, too (e.g., Richardson et al. 1982, Bricelj & Shumway 1991).

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

How is this biological seasonality of Z. patagonica coupled to environmental seasonality? Chl a concentrations and corresponding phytoplankton production (Bianchi et al. 2005) on the south western Atlantic shelf-break are closely coupled to water column stratification (Romero et al. 2006). First plankton blooms develop when the seasonal thermocline is formed (see Fig. 5) (i.e., north of about 45[degrees]S in early austral spring (September to October) and further south somewhat later (November to January). The pelagic primary production season ends in late June when the stratification of the water column is broken off (Baldoni & Guerrero 2000, Rivas & Piola 2002). Hence, maximum somatic growth in Z. patagonica at Reclutas is directly coupled to spring summer primary production (the accumulation of reserves in tissues is likely caused by phytoplankton blooms, see Barber & Blake 1991, Thompson & MacDonald 2006), as indicated by the rapid increase in adductor muscle RCI from September onwards (Fig. 4) and by the fact that shells start to grow after the late autumn and winter maximum in temperature (Fig. 2) (i.e., not earlier than August to September (Fig. 5). Zygochlamyspatagonica switches from somatic to gonad production around May to June (Fig. 4), exactly at the time when primary production and thus food supply cease. The distinct "on-line" [[delta].sup.13]C signal indicates a strong near-bottom demineralization activity around this time, which is expected after the breakup of the thermocline and the accompanying sedimentation event. Subsequently, gonads grow during the time of--most likely--negligible primary production until August to September (Fig. 4), when they must be ready for spawning (Campodonico et al. 2001) to match larval development with the spring bloom. Some reallocation of energy from soma to gonad, as observed in other pectinid species (Bricelj et al. 1987a, Bricelj et al. 1987b, Bricelj & Shumway 1991) appears to be inevitable to meet energy demand of gonad development in Z. patagonica, albeit we cannot provide more evidence than the condition index cycles (Fig. 4).

The observed connections between hydrography, primary production and pectinid seasonal growth cycles as observed at Reclutas should also apply to Tango B, as this scallop bed is governed by the same hydrographic pattern. However, it may be different at the northern Uruguay site and the southern Beagle site given that both are located in different, albeit opposite hydrographic regimes (Fig. 5, Piola et al. 2000, Sabatini et al. 2004). Uruguay is characterized by higher temperature, steeper thermocline and shifted seasonality (Fig. 5), owing to the influence of the Subtropical Shelf Front (Piola et al. 2000) and the Rio de Plata discharge (Piola et al. 2005). Beagle tends in the opposite direction, continuous vertical mixing and thus no thermocline (Fig. 5; Sabatini et al. 2004) and a higher amplitude in bottom water temperature (4.5[degrees]C). The intra-annual range in 5180, however, is the same in all beds (corresponding to l[degrees] to 3[degrees]C [i.e., the scallops may cease to grow during the time of highest temperature]) (compare Figs. 2 and 4), thus, the mechanism that produces the annual shell growth lines at Uruguay and Beagle beds remains unclear so far.

The annual periodicity of external growth lines of Z. patagonica validated by oxygen isotopes analyses in combination with condition indexes and oceanographic data provides a tool for future ageing approaches in this species. The seasonal shell growth pattern, however, may differ between beds owing to the interplay of environmental seasonality and intrinsic regulative mechanisms that govern the reproductive cycle.

ACKNOWLEDGMENTS

The authors thank Angel Marecos and Macarena Valinas (from INIDEP, Argentina) and, Kerstin Beyer (from Alfred Wegener Institute, Germany) for technical assistance and Dr. Bernd Schonc (from University of Mainz, Germany) for isotopes analysis. This project was supported by Glaciar Pesquera S.A. (by contract to the Universidad Nacional de Mar del Plata, OCA No. 320/04), INIDEP, Universidad Nacional de Mar del Plata, ANPCyT (PICT 13527), Conicet (PIP 5669) and Fundacion Antorchas (Grant 13900-13).

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BETINA J. LOMOVASKY,(1,2) * THOMAS BREY, (3) ANA BALDONI, (4) MARIO LASTA, (4) ANDREAS MACKENSEN, (3) SILVANA CAMPODONICO (4) AND OSCAR IRIBARNE (1,2)

(1) Laboratorio de Ecologia, Dpto. Biologia, FCEyN, Universidad Nacional de Mar del Plata, CC 573 Correo Central (B7600WAG) Mar del Plata, Bs. As. Argentina; (2) Consejo Nacional de Investigaciones Cientificas y Tecnicas ( CONICET), Argentina; (3) Alfred Wegener Institute for Polar and Marine Research, P.O. Box 120161, 27515 Bremerhaven, Germany; (4) Instituto Nacional de Investigacion y Desarrollo Pesquero (INIDEP). Paseo V. Ocampo No 1, (B7602HSA) Mar del Plata, Argentina

* Corresponding author. E-mail: [e-mail]

TABLE 1.
Zygochlamys patagonica sampling for stable
isotope analysis.

                                        Number of    Number of
              Scallop    Shell Height     Growth     Carbonate
Individual      Bed          (mm)       increments    Samples

  U1          Uruguay       53.54           7           18
  U2          Uruguay       53.69           7           18
  U3          Uruguay       58.67           9           23
  R1          Reclutas      45.99           8           16
  R2          Reclutas      53.94           8           l8
  R3          Reclutas      54.72           7           22
  R4          Reclutas      47.95           7           30
  R5          Reclutas      50.75           7           22
  TB1         Tango B       55.70           9           22
  TB2         Tango B       53.10           8           17
  TB3         Tango B       66.90          11           30
  B1          Beagle        44.40           5           13
  B2          Beagle        43.23           5           17
  B3          Beagle        63.21           7           27