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Vulnerability of the paper nautilus (Argonauta nodosa) shell to a climate-change ocean: potential for extinction by dissolution.

Introduction

The effects of increasing temperature, elevated [rho][CO.sub.2], decreased pH, and reduced carbonate saturation on marine systems is a burgeoning field of research as we attempt to understand potential future outcomes for marine biota. Near-future predictions of increased temperature ( +4 [degrees]C), [rho][CO.sub.2] (>800 ppm) and acidification (-0.5 pH units) have been shown to have significant impacts on marine biota (Byrne, 2011). Increasing temperature is the most pervasive present-day impact of climate change on marine systems, with deleterious effects on physiology, reproduction, and calcification, and alteration in species' distributions (Brierley and Kingsford, 2009). The adverse effects of ocean warming will be further exacerbated when coupled with acidification (Byrne, 2011; Rodolfo-Metalpa et at., 2011).

Calcifying marine invertebrates with thin external shells may be particularly vulnerable to ocean change, as shown for abalone and oyster larvae (Gazeau et at., 2007; Byrne et at., 2011; Gattuso et at., 2011; Lischka et al., 2011). Abnormal calcification has been noted for many molluscs at pH [less than or equal to] 7.8, levels of ocean acidification predicted to occur by 2100 (IPCC, 2007; Nienhuis et al., 2010; Parker et at., 2011; Byrne, 2011; Byrne et al., 2011). Thus, it is expected that many marine calcifiers will fare poorly in a changing ocean (Orr et al., 2005; McClintock et at., 2009; Byrne, 2011). The effects of ocean acidification on marine calcifiers vary among species, influenced by the type of mineral produced (e.g., calcite, aragonite) and whether the skeleton has a protective cover (e.g., tissue, periostracum) (Nienhuis et al., 2010; Ries, 2011; Rodolfo-Metalpa et al., 2011).

Shell mineralogy is a key consideration in the context of ocean acidification (past and present) and with respect to invertebrate evolution (Smith et al., 2006). The inverse relationship between the solubility of Ca[CO.sub.3] and temperature is also well understood (Revelle and Fairbridge, 1957; Harper, 2000). The mineralogy of molluscs is best known for bivalves and gastropods (Lowenstam and Weiner, 1989; Dauphin, 2006; Weiss, 2010). Biomineralization in cephalopods, the taxon investigated here, has received less attention. To date, about 10 different minerals are reported for cephalopod shells, cuttlebones, and beaks, making them some of the most complex mineralizers in the ocean (Lowenstam and Weiner, 1989). The internal skeletons of cuttlefish and squids are aragonitic (Radtke, 1983; Bettencourt and Guerra, 2000).

The thin shell of the female argonaut (Cephalopoda; Octopoda) is a magnesium-calcite structure (Revelle and Fairbridge, 1957; Mitchell et al., 1994; Nixon and Young, 2003; Saul and Stadum, 2005), a mineral form vulnerable to dissolution at decreased pH (McClintock et al., 2011; Reis, 2011). Only female argonauts produce a shell, which is used as a brood chamber for developing young in the pelagic realm (Nixon and Young, 2003; Finn and Norman, 2010). The argonaut shell is a unique structure secreted by glands on specially adapted dorsal arms. Mineralization of molluscan shells is typically highly organized, attributed to the tight control of calcification by mantle tissue (Dauphin et al., 2003; Checa et al., 2009). Because the paper nautilus shell is secreted by glands on the dorsal arms rather than by the mantle as in most molluscs (Saul and Stadum, 2005; Finn and Norman, 2010), its organization is likely to differ from other molluscs, and this is examined here.

Evolution of the argonaut shell was the key adaptation for a holopelagic life cycle independent of the requirement to lay benthic egg masses, as in other cephalopods (Nixon and Young, 2003). Egg masses are reared inside the female shell until juveniles are ready to hatch into the plankton (Nixon and Young, 2003). Shell-less juveniles and miniature males are typically associated with shallow sites of upwelling (<100 m; Vidal et al., 2010), but the requirement of gas-mediated buoyancy of the female shell at the sea surface limits females to shallower depths, potentially less than 10 In (Finn and Norman, 2010). Despite this, argonauts are rarely encountered alive, but their frequency in the stomachs of apex predators and reports of mass strandings suggest they are abundant (Norman, 2003; Rosa and Seibel, 2010; Vidal et al., 2010). Sometimes in thousands (Okutani and Kawaguchi, 1983), mass strandings of Argonauta sp. provide material of an otherwise largely unobtainable organism.

The general morphology of the shell of Argonauta nodosa (Lightfoot, 1786) is described by Mitchell et at. (1994), and the terminology used here for shell features follows this description. X-ray diffractometry (XRD) and scanning electron microscopy (SEM) were used to characterize the mineralogy and unique microstructure of the shell of Argonauta nodosa, and to examine the mineral and structural response following exposure to climate-change stressors. We immersed fragments of A. nodosa shells in control (19 [degrees]C/pH 8.1), near-future (ca. 2100; 24 [degrees]C/pH 7.6-7.8), and more extreme pH treatments (pH 7.4-7.2) to determine trends in the relationship between shell mineralogy, dissolution, and low pH. On the basis of its lack of an outer protective periostracum-like cover (exposing it directly to the chemistry of surrounding seawater on both the inner and outer surfaces), its thin profile, and its magnesium-calcite construction, we expected to see changes in the shell structure in low-pH treatments, as documented in ocean acidification studies of living molluscs and isolated shells (Orr et al., 2005; Gazeau et al., 2007; Marshall et at., 2008; McClintock et at., 2009; Nienhuis et al., 2010; Welladsen et al., 2010; Ries, 2011; Rodolfo-Metalpa et at., 2011). We further predicted that the adverse effects of acidification would be exacerbated when coupled with warming (Byrne, 2011; Rodolfo-Metalpa et at., 2011). The shell is a vital feature of the life history of A. nodosa. Negative effects of ocean warming and acidification on this brood chamber would have serious implications for reproductive success and persistence of this species in a changing ocean.

Materials and Methods

Specimen collection and preparation

Specimens of Argonauta nodosa were collected by hand from a surface aggregation of this species at Batemans Bay, NSW (35[degrees]44'S, 150[degrees]11'E), in December 2010. The shells were transported to the University of Sydney, where they were cleaned using distilled water to remove any organic material, and air-dried under a fume hood. Four fragments were prepared from nine A. nodosa shells (36 fragments; n = 9) by breaking equally sized pieces (ca. 1-2 [cm.sub.2]) from the side of the shell (Fig. la). Each fragment was weighed on an analytical balance to 0.0001 g, which was used as the starting weight in 2-week incubation experiments. The fragments were placed in individual treatment containers (100-ml jars) of experimental filtered seawater (FSW; 1 gm; salinity 35.5 ppt) in all temperature-pH combinations.

Shell dissolution

Temperature was maintained in water baths and monitored using a temperature-compensating pH probe (WTW Multiline). The 19 [degrees]C treatment approximated the average ambient sea surface temperature (SST) in the Bateman s area (IMOS NSW Moorings BMP090 and BMP120; http://imosmest.aodn.org.au/geonetwork), and 24 [degrees]C represented the upper threshold for near-future (20702100) warming of SST in southeastern Australia, an ocean warming hot spot (IPCC, 2007; Hobday and Lough 2011). Three [pH.sub.NIST] treatments were used, pH 8.1 (control), 7.8, and 7.6, to represent current and near-future acidification predictions (-0.4-0.6 units; IPCC, 2007). Lower pH levels (pH 7.4 and 7.2) were used to determine potential tipping points for shell dissolution. Experimental pH treatments were achieved by bubbling [CO.sub.2] and [0.sub.2] into FSW until the desired pH level was reached ([+ or -]-0.13 units; Table 1), monitored using the WTW Multiline probe. The probe was calibrated for each use with NIST buffers pH 7 and 10 (ProSciTech). The treatment containers were filled with no headspace and capped to avoid outgassing of [CO.sub.2].

Table 1
Average daily change of p[H.sub.NIST] in experimental replicates
based on measurements taken before daily water changes throughout
the 2-week experimental period

Treatment                pH NIST*      pH NIST           pH
                                       Change*        Total*[dagger]

8.1        19[degrees]C  8.11 (0.010)    -0.03(0.01)      8.03(0.01)

           24[degrees]C  8.11 (0.010)    -0.04(0.01)      8.03(0.01)

7.8        19[degrees]C   7.80(0.002)    -0.01(0.01)      7.71(0.02)

           24[degrees]C   7.80(0.003)    -0.03(0.01)      7.73(0.01)

7.6        19[degrees]C   7.59(0.003)     0.03(0.02)      7.51(0.02)

           24[degrees]C   7.60(0.005)     0.01(0.01)      7.55(0.08)

7.4        19[degrees]C   7.39(0.002)     0.06(0.01)      7.32(0.02)

           24[degrees]C   7.40(0.005)     0.06(0.01)      7.35(0.02)

7.2        19[degrees]C   7.20(0.003)  0.13 [+ or -]      7.15(0.01)
                                               0.008

           24[degrees]C   7.20(0.004)  0.13 [+ or -]      7.17(0.25)
                                               0.009

Treatment  P[co.sub.2]  [[ohm].sub.Calcite]
           [dagger]     [dagger]

8.1               419                   4.23

                  412                   4.87

7.8               932                   2.36

                  993                   2.72

7.6              1524                   1.55

                 1525                   1.82

7.4              2469                   1.01

                 2454                   1.20

7.2              3853     0.67[double dagger]


                 3882     0.79[double dagger]

* Values are means with standard error given in
parentheses (n = 14).

[dagger] Average p[H.sub.T] p[CO.sub.2] and[[ohm].sub.Calcite]
calculated from CO2SYS (see Methods).

[double dagger] undersaturated.


Treatment water in the containers was renewed daily with fresh experimental FSW. Before each change, the pH of treatment water was checked (Table 1). This also provided some agitation of the specimens in the treatment water. [pH.sub.T], [rho][CO.sub.2], and [[ohm].sub.Calcite] were calculated using CO2SYS [Pierrot et al. (2006); using the dissociation constants of Mehrbach et al., (1973) as refitted by Dickson and Millero (1987)] from measures of salinity, temperature, [pH.sub.NIST], and total alkalinity (TA) (Table 1). As expected, [pH.sub.T] was~0.10 units lower than [pH.sub.NIST], but general trends in shell dissolution on the NIST and total scale will be similar (Zeebe and Wolf-Gladrow, 2001; Nguyen et al., 2012). Water samples were collected from an open-ocean site (Long Bay, Sydney), fixed with saturated HgC1, and filtered (0.2 [micro]m). Average TA (2301 [micro]mol [kg.sub.-1] seawater; n = 15; SE = 3.14) was determined by potentiometric titration (CSIRO Laboratory, Hobart) using standards (Dickson et al., 2007). Calcite was undersaturated at pH 7.2, and aragonite from pH 7.4 (Table 1).

After 14 days, the shell fragments were removed, rinsed in deionized water (to remove excess salt), air-dried in a fume hood overnight, and weighed. The change in dry weight from the start to day 14 was used as an indication of the relative dissolution under warming and acidification treatments. Percentage weight-change was calculated to normalize data as the fragments were not exactly the same weight. Average weight-change was calculated from four fragments per shell, and then the average was calculated between shells for each treatment (n = 9).

Mineralogy--x-ray diffractometry

Fragments of Argonauta nodosa shells (2-4 [cm.sub.2]) were ground to a fine powder with 0.1 g NaCl and examined using XRD for carbonate mineralogy as described by Smith et (1998, 2006). Analyses were conducted on untreated shells (n = 11) and on shells incubated for 2 weeks in all temperature-pH combinations (n = 5 per treatment). Calcite: aragonite ratio and weight-percent (Wt%) Mg[CO.sub.3] in calcite were determined for each fragment using computerized peak-identification measurements (precision ca. 0.1 Wt%) (calibration equations as in Gray and Smith, 2004). Magnesium content was classified to place the mineral within categorical bounds (Smith et at., 2006).

Shell structure--scanning electron microscopy

The surfaces of shells from control and experimental pH treatments were examined by scanning electron microscopy (SEM) to determine microstructural change. SEM was performed at the Australian Centre for Microscopy and Microanalysis. Specimens were mounted in a slow-curing epoxy resin to provide a cross-section for analysis, polished in a series of silicon and diamond polishes, and finished with a 5-min polish of colloidal silica (Struers OPS). The organic component to the central core was dissolved during this process. The mounts were then coated with about 2-3 nm of gold and analyzed using a Zeiss-Ultra Plus field emission scanning electron microscope. All images are presented as cross-sections showing the inner and outer surfaces of control and experimental shells. Analyses were carried out in a high-vacuum mode using an accelerating voltage of 10-15 kV.

Data analysis

The mean weight change in four fragments was calculated for nine shells and used as the data point for analyses (n = 9). Weight change and weight-percent (Wt%) Mg[CO.sub.3] data were analyzed by two-way analysis of variances (ANOVA). Temperature and pH were considered fixed orthogonal factors, and percent weight loss and Wt% Mg[CO.sub.3] were the dependent variables. Percent data were arcsine-transformed before analysis. As required for ANOVA, homogeneity of variance and normality were checked and confirmed for all data (Quinn and Keough, 2002). Post hoc Tukey HSD tests were used to identify significant differences within and between treatments. All analyses were done using JMP ver. 5.0.1.

Results

Shell dissolution

Both temperature and pH had a significant effect on weight loss in shell fragments of Argonauta nodosa (temperature: [F.sub.1,80] = 5.6, P = 0.02; pH: [F.sub.4,80] = 108.5, P < 0.0001), with no interaction between factors ([F.sub.4,20 = 1.5, P = 0.2). Post hoc Tukey HSD tests indicated that shell dissolution increased with warming and low pH (Table 2). Dissolution was greatest in the most extreme treatment (+5 [degrees]C/pH 7.2), with 5.3% (SE = 0.34; n = 9) weight loss after 2 weeks incubation (Fig. 2). Though minimal, dissolution was evident in near-future pH treatments at control temperature, with a mean weight loss of 1.49% (SE = 0.41; n = 9) and 0.70% (SE = 0.33; n = 9) for pH 7.6 and pH 7.8, respectively (Fig. 2). Shell fragments incubated at control pH (pH 8.1) did not exhibit any weight loss (Fig. 2).

Table 2
Analysis of variance of weight loss data from Argonauta
nodosa shell fragments incubated in temperature/pH
treatments for 2 weeks; n = 9

Source       df   F      P value

Temperature   1   5.64     0.02

pH            4  108.5  <0.0001

Temp x pH     4   1.51   0.2063

Tukey HSP

Temp:        19 [degrees]C < 24 [degrees]C

pH:                    8.178 <7.6 <74 <7.2


Mineralogy--x-ray diffractometry

The A. nodosa shell is a calcitic construct, with no trace of other Ca[CO.susb.3] mineral polymorphs. The mean Mg content of untreated shell fragments was 5.05 Wt% (SE = 0.14; n = 11; Fig. 1). Thus the shell of A. nodosa is an intermediate Mg-calcite construct with no indication of an alternate mineral phase. Fragments incubated for 2 weeks in temperature and pH treatments exhibited no change in Wt% Mg (Fig. 1). Mg ranged from 4.2% to 6.5 Wt% (mean 5.4 Wt%, SE = 0.09; n = 50) across all treatments.

Shell structure--scanning electron microscopy

The A. nodosa shell is a thin, hollow structure with rugose surface features consisting of semilinear rows of nodules and ribs (Fig. 3a, b). These surface features radiate from the central spiral to the upper keel, where two rows of large nodules are constructed (Fig. 3a, b). Opposing nodules along the keel are asymmetrical, constructed in a zigzag-like sequence (Fig. 3b). Although the shell appears bilaterally symmetrical, the nodules and ribs are disjointed and inconsistent (Fig. 3a, b).

At the level of mineral, A. nodosa calcifies crystals hidi-rectionally from a central organic core, which is the nucleating point for crystal formation (Fig. 3c, d). Disordered crystallite grains radiate outward from the central core in fanlike units perpendicular to the inner and outer shell surfaces (Figs. 3c, d; 4a). In places, this perpendicular radiation was interrupted by a fracture zone (Fig. 4b). Crystallites extend right to the shell surface, with no evidence of a protective outer layer (e.g., tissue, periostracum) (Fig. 3d; 4a, b). Within individual units, crystallites vary in size and shape, appearing largely unstructured in regard to layering and organization (Figs. 3c, d; 4a, b).

Signs of surface etching, where marked dissolution occurs at the shell edge, were evident after 14 days incubation in low pH treatments (pH [less than or equal to] 7.4) at control temperature (19 [degrees]C) (Fig. 4d--f). Shell dissolution occurred at the exposed shell surface at boundaries between individual crystallites (Fig. 4d--f). The gaps formed by surface dissolution were often in-filled by epoxy resin under pressure in the SEM chamber (Fig. 4d-1). No surface etching was evident in control and near-future pH treatments (pH [greater than or equal to] 7.6) (Fig. 4a--c).

Discussion

The thin shell produced by the female argonaut is unique among the Mollusca, including other cephalopods. Mineralization by molluscs is typically highly organized, nucleating from the inner mantle and radiating unidirectionally in systematic bricklike layers to the outer periostracum (Dauphin et at., 2003; Checa et at., 2009). The argonaut shell is radically different, with a central core as the site of bidirectional nucleation toward the inner and outer shell surfaces, which lack an organic cover (Mitchell et at., 1994). Calcification by argonauts occurs by periodic mineral deposition by specialized glands on the dorsal arm, alternating between the inner and outer shell surfaces (Mitchell et at., 1994). The distinctive shell structure of argonauts has been directly attributed to this unique mode of calcification, in contrast to calcification by the mantle as in other molluscs (Saul and Stadum, 2005; Finn and Norman, 2010).

The Argonauta nodosa shell appears roughly bilaterally symmetrical; however, the surface features (nodules, ribs) are not fully aligned. At the level of mineral, individual crystallites also seem largely unstructured, radiating outward in no obvious layers from the site of nucleation. The notable imperfections of the A. nodosa shell are likely a result of periodic and alternating (therefore interrupted) calcification between the inner and outer shell surfaces, as suggested by Mitchell et al. (1994). The fracture zones in crystallite radiation indicate restart points during this interrupted calcification, dividing separate periods of mineral secretion. The zipperlike arrangement of nodules along the keel also suggests that secretion of mineral is focused on one side of the shell before alternating to the other. Overall, SEM here supports the suggestion that interrupted calcification by argonauts attributes to a disordered shell structure compared to most other molluscs (Mitchell et at., 1994). The fanlike units of crystallites, however, imply systematic and sequential layers of mineral during forward growth of the shell from the aperture.

Shell mineralogy was confirmed to be 100% calcite, as determined by Mitchell et al. (1994). The intermediate Mgcalcite concentration (5.05 Wt%) is higher than that reported for the skeletons of other cephalopods (1%-4%) and differs from the carbonate structures produced by most molluscs (Revelle and Fairbridge, 1957; Taylor and Reid, 1990; Mitchell et al., 1994; Harper, 2000; Saul and Stadum, 2005; Dauphin, 2006). High Mg-calcite is more susceptible to dissolution than other skeletal mineral forms at lower pH (McClintock et al., 2011; Ries, 2011), and the inverse relationship between the solubility of Ca[CO.sub.3] and increased temperature is well known (Revelle and Fairbridge, 1957; Harper, 2000). As a result, the argonaut shell may be among the most vulnerable adult mollusc shells to future changes in ocean conditions, a suggestion supported by the dissolution we observed.

The organic layer (e.g., tissue, periostracum) shielding the shells and skeletons of some invertebrates from the environment plays a major role in protecting them from the negative impacts of ocean acidification (Ries et al., 2009; Ries, 2011; Rodolfo-Metalpa et al., 2011). Dissolution and malformations of organic and nacreous layers may also decrease the structural integrity and strength of a shell (McClintock et al., 2009; WelIadsen et aL, 2010). Lacking a protective cover, the shell of A. nodosa is more vulnerable to changing seawater chemistry, as is also the case for the shells of bivalve and abalone veliger larvae (Byrne et al., 2011; Lischka et al., 2011). Unshelled larvae and corroded shells in response to near-future ocean acidification have been reported (Comeau et aL, 2010; Byrne et al., 2011; Lischka et al., 2011). The shells of adult serpulid worms and whelks are similarly affected by decreasing pH (Ries, 2011).

Dissolution of the shell of A. nodosa was observed after 2 weeks across all experimental temperature/pH treatments, including 0.8%-1.8% weight loss in treatments projected for coming decades (24 [degrees]C/pH 7.8-7.6 by 2100; IPCC, 2007). Significant change was evident at 24 [degrees]C and pH [less than or equal to] 7.6, supporting the suggestion that the adverse effects of ocean warming will be exacerbated when coupled with acidification (Rodolfo-Metalpa et al., 2011). In similar studies of isolated shells of Antarctic bivalves and Mediterranean gastropods, significant weight loss was evident following incubation (2-7 weeks) in pH [less than or equal to] 7.6 (2.7%-3.7% bivalves; 4.0% gastropod) (McClintock et al., 2009; Rodolfo-Metalpa et al., 2011). Although increased temperature exacerbated low pH-driven dissolution, in a warming ocean mineral saturation will increase, thus resulting in an antagonistic interaction with ocean acidification. This may facilitate shell production in the living argonaut.

Since we used shell fragments with a large ratio of surface area to volume, the dissolution we recorded may be greater than expected for whole A. nodosa shells. However, as a thin hollow structure where both the inside and outside of the shell is exposed, the argonaut shell has a naturally high surface area. In addition, the argonaut shell would be naturally exposed to much greater water movement, and so the shell loss observed here in relatively static incubations might actually underestimate what would occur in a warm low-pH ocean.

Although known to be abundant, argonauts are rarely encountered alive (Finn and Norman, 2010; Vidal et al., 2010). This study was thus limited to female brood chambers, which more commonly wash ashore in large numbers during mass stranding events (Norman, 2003). It is therefore unknown whether compensatory or repair calcification would occur in A. nodosa in response to an altered shell in a changing ocean. Glands on the arms of the female constantly secrete shell components (Mitchell et al., 1994; Saul and Stadum, 2005; Finn and Norman, 2010), and so A. nodosa may be able to respond behaviorally to actively reduce or compensate for shell loss, as has been suggested for pteropods (Lischka et al., 2011). Such compensatory shell secretion would depend on the rate of ocean acidification, and the rate by which A. nodosa can maintain suitable calcite production. The metabolic demands of maintaining the A. nodosa shell in a warm, high pCO2 ocean may reduce energy available for other processes. Studies on the brittle stars and a sea star documented increased growth and calcification in response to decreased pH, but with metabolic and energetic costs (Wood et al., 2008). Other studies on bivalves document reduced calcification rates in response to low pH (Gazeau et al., 2007; Ries et al., 2009).

In contrast to argonauts, other cephalopods (e.g., cuttlefish and squid) produce internal aragonitic skeletons that are protected from changes in seawater chemistry. The cuttlefish Sepia officinalis exhibits steady body and skeleton growth in both control and near-future ocean acidification conditions, and is capable of regulating the site of calcification with no effects evident to pH 7.2 (Gutowska et at., 2008). Metabolic processes of adult S. officinalis are also not compromised in a near-future ocean (Hu et at., 2011). Gutowska et al. (2010) suggests that ectothermic organisms with high metabolic rates, such as cephalopods, may have a pre-adaptive capacity for resilience in the face of decreasing ocean pH.

SEM revealed the mechanisms behind the dissolution caused by exposure to extreme pH treatments (pH [less than or equal to] 7.4). Preferential etching occurred at boundaries between crystalline grains at the exposed shell surfaces at low pH. This dissolution formed gaps between adjacent crystallites. Surface microstructure altered by dissolution would compromise the integrity and mechanical strength of the argonaut egg case, as noted for other molluscs exposed to ocean change conditions (McClintock et aL, 2009; Welladsen et al., 2010). Exposure to low pH during the alternating and interrupted calcification of A. nodosa could result in even greater disorganization of crystallites with a higher frequency of fracture zones throughout the shell, adding to reduced shell strength.

Dissolution was evident here after only 2 weeks' incubation in temperature/pH treatments. Greater dissolution would be expected with extended incubation, including in near-future ocean acidification levels (pH 7.6-7.8), which would result in a more fragile argonaut shell. Direct change to the argonaut egg case caused by ocean warming and acidification would have repercussions for shell architecture and calcification, and for the ability of females to protect embryos. The negative effects of ocean change on the female brood chamber would have deleterious effects on reproduction in A. nodosa, thereby compromising persistence of this species in a changing ocean. As A. nodosa is an important feature of pelagic and planktonic systems, its extinction by dissolution would have serious implications for food webs, especially for high-order apex predators (Vidal et al., 2010).

The integrity of the non-living argonaut shell aside, living shelled invertebrates may be at serious risk of shell weakening due to dissolution in an ocean simultaneously warming and decreasing in pH (McClintock et al., 2009; Wellad-sen et al., 2010). Dissolution is not restricted to the isolated shells of dead molluscs (Harper, 2000). The effects of ocean change on other life-history processes such as development are also of concern for A. nodosa. Shell-less argonauts (juveniles and minute males) may also be at risk in a changing ocean. Shell-less argonauts travel deeper into the pelagic zone, to depths of 200 m (Nixon and Young, 2003; Vidal et al., 2010). Ocean-change stressors including warming, acidification, and hypoxia will compress the habitable depth range of pelagic species (Portner, 2010). Further, it has been suggested that early cephalopod life stages may be the weak link in population success in response to future ocean conditions (Lacoue-Labarthe et al., 2009; Hu et al., 2011). The effects of future ocean change across all life-history stages of argonauts will be important to assess.

Acknowledgments

We thank Melinda Coleman and Brendan Kelaher for supplying argonaut shells. Thanks to Hong Nguyen for assistance in the laboratory and to Dr. Bronte Tilbrook and Kate Berry (CSIRO) for assistance with water chemistry. Supported by a grant from the ARC.

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Received 5 June 2012; accepted 7 August 2012.

* To whom correspondence should be addressed. E-mail: kennedy wo1fe90@gmail.com.

KENNEDY WOLFE (1). ABIGAIL M. SMITH (2). PATRICK TRIMBY (3), AND MARIA BYRNE (4)

(1) School of Medical Sciences, University of Sydney, New South Wales 2006, Australia; (2) Department of Marine Science, University of Otago, P.O. Box 56, Dunedin, New Zealand; (3) Australian Centre for Microscopy and Microanalysis, Madsen Building F09, University of Sydney, New South Wales 2006, Australia; and (4) School of Biological and Medical Sciences, University of Sydney, New South Wales 2006, Australia
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Author:Wolfe, Kennedy; Smith, Abigail M.; Trimby, Patrick; Byrne, Maria
Publication:The Biological Bulletin
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Geographic Code:8AUST
Date:Oct 1, 2012
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