Ecotoxicology and Environmental Safety 102 (2014) 179–186
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Review
Trace element concentrations in the top predator jumbo squid (Dosidicus gigas) from the Gulf of California Joana Raimundo a,n, Carlos Vale a, Rui Rosa b a b
IPMA, Portuguese Institute of Sea and Atmosphere, Avenida de Brasília, 1449-006 Lisbon, Portugal Guia Marine Laboratory, Oceanography Center, Faculty of Sciences University of Lisbon, Av. Nossa Senhora do Cabo, 939, 2750-374 Cascais, Portugal
art ic l e i nf o
a b s t r a c t
Article history: Received 16 August 2013 Received in revised form 23 December 2013 Accepted 22 January 2014 Available online 14 February 2014
Jumbo (or Humboldt) squid, Dosidicus gigas, is a large jet-propelled top oceanic predator off the Eastern Pacific. The present study reports, for the first time, concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb in gills, mantle and digestive gland of this powerful pelagic squid in the Gulf of California. Zinc and Cu were the most abundant elements. All elements, with the exception of As, were largely stored in digestive gland; particularly Cd that reached concentrations between 57 and 509 mg g 1. Significant relationships between tissues were found for Co (digestive gland–gills), As (gills–mantle) and Cd (digestive gland–mantle). Proportionality of Cd concentrations between mantle and digestive gland suggested that detoxification capacity by digestive gland was insufficient to avoid the transfer of this element to mantle and other tissues. Nonetheless, Cd concentrations in the mantle were always below the regulatory limit and, therefore lack of constraints for human consumption. On the basis of the fishery landings, one may estimate that up to 1 t of Cd can be annually removed by jumbo squid fisheries. & 2014 Elsevier Inc. All rights reserved.
Keywords: Trace elements Jumbo squid Dosidicus gigas Gulf of California
Contents 1. 2. 3. 4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Material and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Trace element partitioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Relations of trace element accumulation between tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Vehicle of cadmium transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Trace element concentrations in cephalopods have received increasing interest in the last decade due to the recognition of species being able to accumulate high levels of essential and nonessential elements in key tissues (e.g. Martin and Flegal, 1975; Miramand and Guary, 1980; Finger and Smith, 1987; Miramand and Bentley, 1992; Bustamante et al., 2000; Kojadinovica et al., 2011). Digestive gland, which plays a key function in the digestive process (Mangold, 1983) is the major storage site of trace elements
n
Corresponding author. E-mail address: [email protected] (J. Raimundo).
0147-6513/$ - see front matter & 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2014.01.026
179 180 181 181 183 183 185 185 185
(Martin and Flegal, 1975; Miramand and Guary, 1980). For example, Cd in digestive gland of some cephalopod species may reach 98% of the total body burden (Bustamante et al., 2002a). Such high retention of this potentially toxic element is predictably associated with detoxification mechanisms minimizing the Cd mobility among key tissues (Simkiss and Taylor, 1982; Phillips and Rainbow, 1989; Bustamante et al., 2002a, b; Raimundo et al., 2008, 2010a, b). Besides this retention ability, environmental and biological factors, such as availability in water and food, exposure period, temperature, size, sex, and maturity stage may also influence the bioaccumulation values (e.g. Barghigiani et al., 2000; Miramand and Bentley, 1992; Pierce et al., 2008; Raimundo et al., 2004, 2005; Pereira et al., 2009; Pernice et al., 2009). High accumulation of trace elements
180
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associated with the short life span led several authors to consider cephalopod species as potential indicators of environmental contamination (Miramand and Bentley, 1992; Bustamante et al., 2002a). The jumbo (or Humboldt) squid, Dosidicus gigas, is a large and powerful jet-propelled predator, that reaches more than 2 m total length and 50 kg in mass (Nesis, 1983). This species is endemic of the Eastern Tropical Pacific (ETP) and with a longevity generally assumed to be no more than 12–24 months (Nigmatullin et al., 2001). Besides supporting a large fishery, it also plays a critical role in the ETP ecosystem both as prey and predator (Rosa et al., 2013). Interestingly, in the last ten years, this squid has greatly extended its tropical/subtropical range polewards in both hemispheres, where it is exerting a significant top–down control on commercial fish stocks (Zeidberg and Robison, 2007; Keyl et al., 2008). This species can easily remove more than 4 million t of food per year (mainly myctophid fishes) from the ETP pelagic food web (Rosa and Seibel, 2010). In terms of behavioral ecology, the jumbo squid undergoes diel vertical migrations to intermediate depths where it encounters zones of low oxygen (Rosa and Seibel, 2008, 2010). These oxygen minimum zones greatly limit the vertical distribution and ecology of many marine animals (Prince and Goodyear, 2006), but the jumbo squid thrive in such harsh environment by managing hypoxia via metabolic suppression (Trübenbach et al., 2013a, b). Because jumbo squid is large and abundant, it transfers large amounts of energy from lower trophic levels to top vertebrate predators. Despite of the ecological (and economical) importance, the capability of jumbo squids to concentrate metals in their tissues has not been documented, and it is not known if they constitute a significant vector of contaminants to top predator
species that feed on them, namely blue marlins, swordfish, sail fish, sharks and marine mammals (Rosa et al., 2013). The aim of the present study is to inventory, for the first time, the concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb in the gills, mantle and digestive gland of the jumbo squid, D. gigas capture in the Gulf of California, one of marine ecosystems with the highest productivity and biodiversity in the world.
2. Material and methods Sixteen adult jumbo squids (Dosidicus gigas) were collected, with dip-nets and hand-lines with jigs, in the Gulf of California, between Santa Rosalia, Guyamas and San Rafael basin (271N, 1111W; 281N, 1131W) (Fig. 1), in June 2011, aboard the RV New Horizon (Scripps Institute, California). Specimens were weighted, measured (mantle length), sex determined, dissected, and gills, mantle (without skin) and digestive gland separated. Maturity stages were assigned according to the classification of Markaida and Sosa-Nishizaki (2001), more specifically: I and II, immature; III, maturing; IV and V, mature and VI, spent. The individual samples were immediately frozen in liquid nitrogen onboard, and then transferred to 80 1C in the lab. Afterwards, the tissue samples were freeze-dried, grounded and homogenized for the analytical procedures. Elements were determined in samples after digestion with a mixture of HNO3 (sp, 65 % v/v) and H2O2 (sp, 30 % v/v) at different temperatures according to the method described in Ferreira et al. (1990). All lab ware was cleaned with HNO3 (20 %) for two days and rinsed with Milli-Q water to avoid contamination. Three procedural blanks were prepared using the same analytical procedure and reagents, and included within each batch of samples. Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb were determined by a quadrupole ICP-MS (Thermo Elemental, X-Series). The accuracy of these analytical methods was assessed by the analysis of international certificate standards (DORM-2, dogfish muscle, DORM-3, fish protein; DOLT-3 and 4, fish liver and TORT-2, lobster hepatopancreas). The results obtained did not differ significantly (p o 0.05) from the certified values (Table 1). Procedural blanks always
Fig. 1. Sampling location of Dosidicus gigas in the Gulf of California.
0.045 7 0.035 0.065 7 0.007 – – – – – – 0.43 70.27 0.357 0.13 0.0377 0.008 0.043 7 0.008 0.26 70.026 0.290 70.020 18.2 7 1.0 19.4 7 0.6 – – 277 1.9 26.7 70.6 6.0 77.0 1.4 7 0.09 3.5 70.28 3.3 6.3 71.2 7.06 7 0.48 7.5 7 0.99 8.3 71.3 – – 16.3 7 4.8 18.17 1.1 6.0 71.0 6.88 70.30 – – – – – – 21.4 7 4.0 25.6 7 2.3 477 7.0 51.3 7 3.1 82 79.6 86.6 7 2.4 1117 6.1 1167 6 1727 22 1807 6 – – – – 28 74.5 31.2 7 1.0 28 72.3 31.2 7 1.1 – – – – 1.05 70.12 1.28 70.24 2.62 7 0.36 2.727 0.35 – – 2.0 7 0.34 2.50 7 0.19 0.26 7 0.38 0.1827 0.031 1.39 71.0 1.89 70.19 – – – – 0.43 7 0.044 0.517 0.09 – – 1.75 7 0.35 1.89 7 0.17 – – – – 0.65 7 0.12 0.777 0.15
2.63 7 2.2 3.66 7 0.34 – – – – – – 9.9 7 12 13.6 7 1.2
Pb (mg g 1, dw) Cd (mg g 1, dw) Se (mg g 1, dw) As (mg g 1, dw) Zn (mg g 1, dw) Cu (mg g 1, dw) Ni (mg g 1, dw) Co (mg g 1, dw)
– – – – – – – – 1.8 7 0.30 1.64 70.19 TORT-2
DOLT-4
DOLT-3
DORM-3
Obtained Certified Obtained Certified Obtained Certified Obtained Certified Obtained Certified
For the number of specimens used in this study (n¼ 16) trace element concentrations in the analyzed tissues did not varied significantly with mantle size, total weight or gender of D. gigas. Despite the limited number of specimens, to the best of our knowledge, this is the first attempt to assess the effect of biological parameters on trace element bioaccumulation in D. gigas. Therefore comparison to previous works can only be done to other species. The similar element composition observed for male and female is in line with findings for the squids Todarodes filippovae and Illex argentinus (Gerpe et al., 2000; Kojadinovica et al., 2011). However, the effect of this biological factor on the trace element
DORM-2
4. Discussion
Mn (mg g 1, dw)
The proportion female:male of the collected specimens was 9:7, being all in the maturation stages III and V. The mantle length and total weight of jumbo squids ranged within the intervals 32–73 cm and 0.9–13 kg, respectively. Total weight (TW) was correlated to mantle length (ML) through the exponential equation TW¼ 0.085 ML0.070. Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb concentrations in gills, mantle and digestive gland showed no significant differences (KW-H, po0.05) with total weight, mantle length or gender of D. gigas. Trace element concentrations of both genders and all sizes were thus treated together. Fig. 2 presents the median, the percentile 25th and 75th, minimum and maximum concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb concentrations in gills, mantle and digestive gland of D. gigas specimens captured in the Gulf of California. Outliers and extreme points were not plotted to better visualize differences among tissues within smaller scales. Zinc and Cu were the most abundant elements. Although being considered as essential elements to organisms, concentration medians in the digestive gland ranged one order of magnitude for Zn (22– 238 mg g 1) and two for Cu (6.8–560 mg g 1). Narrower intervals were observed in gills (82–107 mg g 1 for Zn and 154–363 mg g 1 for Cu) and mantle (71–98 mg g 1 for Zn and 3.7–13 mg g 1 for Cu). Partitioning among the three tissues varied with the element, medians decreasing from: 161 mg g 1 (Cd) to 0.25 mg g 1 (Pb) in digestive gland, 21 mg g 1 (As) to 0.065 mg g 1 (Pb) in mantle, and 18 mg g 1 (As) to 0.090 mg g 1 (Pb) in gills. In general, digestive gland presented higher variability than gills and mantle. Manganese and Cr were more abundant in gills differing significantly (U, p o0.05) from the other two tissues. Vanadium, Co, Ni, Se, Cd and Pb exhibited significantly (U, p o0.05) higher concentrations in digestive gland than in gills and mantle. Arsenic was significantly (U, p o0.05) lower in digestive gland. Copper concentrations were similar in gills and digestive gland, and Zn in the three tissues. Despite most trace elements being largely stored in the digestive gland, linear and positive relations were found for Co, As and Cd among mantle, gills and digestive gland (Fig. 3). These relations may elucidate element pathway in the analyzed species and redistribution among these tissues.
Cr (mg g 1, dw)
3. Results
181
V (mg g 1, dw)
accounted for less than 1 % of the total metal in the samples. All the results are given as medians and ranges in microgram per gram of tissue dry weight (mg g 1, dw). Prior to statistical analyses, metal concentrations were tested for normality and equality of variances. Non-compliance with parametric ANOVA assumptions led to employment of the Kruskal-Wallis H (KW-H) and Mann-Whitney (U) nonparametric tests to evaluate the existing differences between element concentrations in tissues and between genders. The significance for statistical analyses used was always p o0.05. The statistical analyses were performed using STATISTICA (Statsoft).
Table 1 Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb (mg g 1, dry weight) in fish muscle and protein (DORM-2 and DORM-3, respectively), fish liver (DOLT-3 and DOLT-4) and lobster hepatopancreas (TORT-2) obtained in the present study and certified values.
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
5
1.2
4
1.0 Cr (µg g -1)
V (µg g -1)
182
3 2
0.2
0
0.0
Mantle Digestive gland
4
8
3
6
Co (µg g -1)
Mn (µg g -1)
Gill
2 1
Gill
Mantle
Mantle
Gill
Mantle Digestive gland
Digestive gland
500 Cu (µg g -1)
Ni (µg g -1)
Gill
600
6 4 2
400 300 200 100
Gill
0
Mantle Digestive gland
40
As (µg g -1)
300
200
100
0
Mantle Digestive gland
4
0
Digestive gland
8
0
Gill
2
0
Zn (µg g -1)
0.6 0.4
1
30 20 10 0
Gill
Mantle
Digestive gland
Gill
Mantle Digestive gland
300
20 Cd (µg g -1)
15 Se (µg g -1)
0.8
10
200
100 5 0
0 Gill
Mantle Digestive gland
Gill
Mantle Digestive gland
Gill
Mantle Digestive gland
Pb (µg g -1)
0.6
0.4
0.2
0.0
Fig. 2. Median, percentile 25th and 75th, minimum and maximum concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb (mg g 1, dry weight) in the gills, mantle and digestive gland of Dosidicus gigas captured in the Gulf of California.
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
0.05
6
CoMantle (µg g-1)
CoDig gland (µg g-1)
8
y = 50.46x + 0.060 R2 = 0.80
4 2 0 0.00
0.02
0.04
0.06
0.08
y = 50.46x + 0.060 R2 = 0.80
0.04 0.03 0.02 0.01 0.00
0.10
0
-1
CdMantle (µg g-1)
AsMantle (µg g-1)
10
0
10
20
6
8
4
20
0
4 CoDig gland (µg g )
y = 1.007x -1.859 R2 = 0.90
30
2
-1
CoGills (µg g ) 40
183
30
40
Asgills (µg g-1)
3
y = 165.8x + 63.82 R2 = 0.86
2 1 0
0
200
400
600
CdDig gland (µg g-1)
Fig. 3. Relationships between gills, mantle and digestive gland for Co, As and Cd concentrations (mg g 1, dry weight) in Dosidicus gigas from the Gulf of California.
accumulation in cephalopods is far from being consensual (e.g. Barghigiani et al., 2000; Bustamante et al., 1998; Seixas and Pierce, 2005; Bustamante et al., 2006; Raimundo et al., 2010a). Presumably, other biologic or environmental factors mitigate the effect of gender on trace element accumulation. It is documented that females mature later than males in the Gulf of California (Markaida et al., 2004). Individuals used in the current work presenting maturation stage between III and V limited the conclusion on trace element concentrations being influenced by the maturation. 4.1. Trace element partitioning Digestive gland was the preferential organ of the jumbo squid for the accumulation of V, Co, Ni, Se, Cd and Pb, like reported for Architeuthis dux and Todarodes filippovae (e.g. Bustamante et al., 2008; Kojadinovica et al., 2011). High retention of potentially toxic elements is admittedly associated with detoxification mechanisms existing in the digestive gland, like metallothioneins and high molecular weight proteins (Simkiss and Taylor, 1982; Phillips and Rainbow, 1989; Bustamante et al., 2002b; Raimundo et al., 2010a, c). As observed for various cephalopod species, Cd concentrations in the jumbo squid were elevated (57–509 mg g 1). The comparison with the literature (Table 2) shows that those registered values were one order of magnitude above the ones obtained for Todaropsis eblanae, Todarodes sagittatus, Nototodarus gouldi, A. dux, Loligo opalescens, Loligo forbesi and Alloteuthis sp., comparable to Ommastrephes bartrami and Sthenoteuthis oualaniensis, and lower than in T. filippovae. That broad interval of concentrations, like observed for other species, is in line with the hypothesis of accumulation being linked to detoxification mechanisms preventing the toxicity effect of such high Cd accumulation. Similar mechanisms are considered in the digestive gland of the various cephalopod species (Bustamante et al., 2002b; Raimundo et al., 2010a, c). Concentration of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se and Pb were compared to values found in other species (Table 2). Narrow intervals suggest that accumulated values primarily reflect the ingested food composition rather than retention mechanisms in response to toxicity. Gills presented significantly higher concentrations of Cr and Mn than the other analyzed tissues. Enhanced values of Mn and As in gills were also registered in the squid T. filippovae (Kojadinovica
et al., 2011). Association of Cr, Mn, Zn and As with the gills of jumbo squid may be interpreted as direct uptake of these elements from seawater. This interpretation has been invoked to Cr, Ni, Cd and Zn in other cephalopod species (Koyama et al., 2000; Miramand et al., 2006; Bustamante et al., 2002a, 2008). Contrarily to all the determined elements in this work, As concentrations in gills were similar to the values registered in mantle and significantly higher than in digestive gland. A similar distribution pattern was observed for As in A. dux captured in Spanish waters (Bustamante et al., 2008) and in T. filippovae from Tasmania and southern Indian Ocean (Kojadinovica et al., 2011). This partitioning has been attributed to different mobility of As chemical forms (Francesconi, 2010). Copper in gills is probably linked to the presence of the heamocyanin (respiratory pigment), in which this element is one of the main components (Soldevilla, 1987; Villanueva and Bustamante, 2006; Craig and Overnell, 2003). Cadmium concentrations were similar to the ones found in T. sagittatus and higher than in L. forbesi captured in the UK waters (Pierce et al., 2008). The enhancement of Cd concentrations in ommastrephids (D. gigas and T. sagittatus) in comparison to loliginids (L. forbesi) was already reported by Pierce et al. (2008) and attributed to differences in feeding and physiological characteristics of the digestive gland. Mantle of D. gigas presented low element concentrations, as found in other cephalopods, (Miramand and Guary, 1980; Miramand and Bentley, 1992; Raimundo et al., 2004, 2008; Pierce et al., 2008). The contrasting difference of Cd concentrations between mantle and digestive gland is remarkable in the jumbo squid, as well as in other cephalopods. Presumably the detoxification mechanism existing in the digestive gland prevents the partitioning of this potential toxic element for other tissues, namely mantle (Bustamante et al., 2002b; Raimundo et al., 2008, 2010a). However, Cd concentrations in the mantle of D. gigas were two to three orders of magnitude higher than in T. sagittatus, L. forbesi and Alloteuthis sp., although similar to T. filippovae and T. eblanae. Concentrations of As in the mantle of D. gigas were comparable to the ones found in T. filippovae (Table 2). 4.2. Relations of trace element accumulation between tissues Despite the storage of several trace elements in the digestive gland, the linear and positive relations of Co (digestive gland–gills and digestive gland–mantle) and Cd (digestive gland–mantle)
184
Table 2 Comparison of element concentrations (mg g 1, dw) in gills, mantle and digestive gland of Dosidicus gigas from the present study with squid data from the literature. Tissue
V (mg g 1, dw)
Cr (mg g 1, dw)
Mn (mg g 1, dw)
Co (mg g 1, dw)
Ni (mg g 1, dw)
Cu (mg g 1, dw)
Zn (mg g 1, dw)
As (mg g 1, dw)
Se (mg g 1, dw)
Cd (mg g 1, dw)
Pb (mg g 1, dw)
Ref.
Dosidicus gigas
Gills Mantle Dig Gland Gills Muscle Dig Gland Gills Muscle Dig gland Gills Muscle Dig gland Dig Gland
0.49–0.70 0.20–0.38 0.50–12 0.04–0.38 o DL 0.21–2.7 – – – – – – –
0.58–1.2 0.43–2.0 0.36–5.0 0.19–4.0 o DL 0.070–0.87 – – – – – – –
1.9–3.0 0.26–0.67 0.76–2.2 1.5–14 o DL 0.94–3.7 – – – – – – –
0.020–0.21 0.0020–0.044 0.060–4.6 0.060–4.3 0.030–0.35 0.31-35 – – – – – – –
0.15–25 0.060–4.6 1.1–7.4 0.15–4.6 o DL 0.20–13 – – – – – – –
154–363 3.7–13 6.8–560 95–763 2.9–14 5.0–865 – – – – – – 363 7 238
82–107 71–98 22–333 71–97 49–84 1.2–307 – – – – – – 830 7 355
11–34 10–33 8.1–20 3.5–32 8.4–23 6.0–41 – – – – – – –
4.5–7.0 1.6–3.2 4.3–19 0.36–5.0 o DL 0.78–33 – – – – – – –
6.5–17 0.13–2.4 57–509 2.3–69 0.060–3.6 34–883 5.7 7 5.1 1.6 7 2.2 257 26 8.7 7 9.0 0.30 7 7 0.30 657 61 337 30
0.031–0.18 0.032–0.48 0.063–0.70 0.050–0.90 oDL 0.020–1.5 – – – – – – –
a
Dig Gland
–
–
4.2 71.1
–
–
246 7298
696 7 295
–
–
507 25
–
e
Dig Gland
–
–
–
–
–
195 7212
1637 55
–
–
287 7 202
–
f
Dig Gland Dig Gland Dig Gland Liver Liver Gills Muscle Dig gland Muscle Dig gland
– 2.2 71.9 1.7
– 0.93 7 0.41 0.49
– 2.7 72.1 2.3
– 3.3 7 1.8 4.8
– 0.62 7 0.54 1.4
17207 151 108 783 1218 5350 73210 83707 3130 – – – – –
5137 288 1037 51 219 2477 131 449 7 201 – – – – –
– 48 7 14 44
– – –
782 7 255 617 46 91 857 52 1227 58 0.25 7 0.32 0.093 7 0.15 127 10 0.80 7 0.20 9.5 7 2.3
– 0.417 0.33 0.85
Todarodes filippovae Todaropsis eblanae Todarodes sagittatus Nototodarus gouldi Nototodarus gouldi Ommastrephes bartrami Symplectoteuthis oualaniensis Architeuthis dux Loligo opalescens Loligo forbesi
Alloteuthis sp.
a
– – – – –
– – – – –
– – – – –
– – – – –
Present study. Kojadinovica et al. (2011). Ranges are the minimum and the maximum obtained for both sampled areas. c Pierce et al. (2008). d Finger and Smith (1987). e Smith et al. (1984). f Martin and Flegal (1975). g Bustamante et al. (2008). b
– – – – –
– – – – –
– – – – –
b
c
d
g
f
– – – – –
c
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
Species
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
suggest redistribution of these elements within the jumbo squid. Although ingested food has been appointed the main accumulation pathway for Co (Bustamante et al., 2004), the proportionality found among the three analyzed tissues indicates Co mobility as this element is uptake either through ingested food or water. Presumably, redistribution is induced by its essential role in the vitamin B12, which is important in cell division (Nolan et al., 1992). Despite this essentiality, values of Co in the digestive gland, gills and mantle of D. gigas were lower than in other species (Table 2). The digestive glandmantle relation observed for Cd suggests its uptake as ingested food, which is not entirely retained in the digestive gland. Whether detoxification capacity by this gland was surpassed cannot be clarified in this work. Linear relations between gills and mantle for As, which is not highly stored in the digestive gland, may be related to its preferential uptake through water, as proposed by Kojadinovica et al. (2011), followed by the transference to the mantle as arsenobetaine that may mimic the glycine betaine (Francesconi, 2010). However, a different pathway for As accumulation was proposed for Octopus vulgaris by Semedo et al. (2012). The distinct preferential via of As uptake in squids and octopus, is probably associated with the species life style, feeding habits and physiology. 4.3. Vehicle of cadmium transfer Trace element concentrations in the Gulf of California, where jumbo squids were captured, are generally attributed to natural factors related to upwelling and biogeochemistry of the region. Enhanced Cd concentrations in coastal waters could be associated with upwelling of bottom waters enriched by Cd diffused from the sediments (Segovia-Zavala et al., 1998). However, the potential contribution of anthropogenic sources like mining and urbanization cannot be dismissed (Shumilin et al., 2000, 2001). No constraints are predicted for human consumption of jumbo squids since Cd concentrations in the edible parts (mainly mantle, median of 0.11 mg g 1, wet weigh) are far below the regulatory limit established by the European Commission (1 mg g 1, wet weigh, Commission Regulation (EC) No. 629/2008). However, the noteworthy aspect comes mainly from the high Cd concentrations in digestive gland, and the size and abundance of jumbo squid in the Gulf of California. Together with the transference of large amounts of energy from lower trophic levels to top vertebrate predators, this specie appears to be a significant vector of Cd to top predator species that feed on them, namely blue marlins (AbitiaCardenas et al., 2010), swordfish (Markaida and Hochberg, 2005; Castillo et al., 2007), sail fish (Arizmendi-Rodriguez et al., 2006), sharks (Pardo-Gandarillas et al., 2007; Cabrera-Chavez-Costa et al., 2010) and marine mammals (Jaquet and Gendron, 2002; Ruiz-Cooley et al., 2004; Davis et al., 2007). In addition, a considerable amount of Cd should be accounted to be removed from the marine ecosystem by fishing. Assuming that the mantle accounts for 70‐80% of the body weight, and the digestive gland around 3%, and based on the fishery landings (SAGARPA, 2012; Rosa et al., 2013), one may estimate that up to 1 t of Cd can be annually removed by jumbo squid fisheries.
Acknowledgments The authors would like to thank Brad Seibel for making the participation in the research cruise aboard RV New Horizon possible and Unai Markaida for his assistance in collecting the specimens. Bárbara Anes for the ICP-MS analyses and the anonymous reviewers for the commentaries. The Portuguese Foundation for Science and Technology (FCT) supported this study through a Senior Research Position (Ciência 2007) to Rui Rosa and the Pos-doc grant (SFRH/BPD/91498/2012) to Joana Raimundo.
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Contents lists available at ScienceDirect
Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv
Review
Trace element concentrations in the top predator jumbo squid (Dosidicus gigas) from the Gulf of California Joana Raimundo a,n, Carlos Vale a, Rui Rosa b a b
IPMA, Portuguese Institute of Sea and Atmosphere, Avenida de Brasília, 1449-006 Lisbon, Portugal Guia Marine Laboratory, Oceanography Center, Faculty of Sciences University of Lisbon, Av. Nossa Senhora do Cabo, 939, 2750-374 Cascais, Portugal
art ic l e i nf o
a b s t r a c t
Article history: Received 16 August 2013 Received in revised form 23 December 2013 Accepted 22 January 2014 Available online 14 February 2014
Jumbo (or Humboldt) squid, Dosidicus gigas, is a large jet-propelled top oceanic predator off the Eastern Pacific. The present study reports, for the first time, concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb in gills, mantle and digestive gland of this powerful pelagic squid in the Gulf of California. Zinc and Cu were the most abundant elements. All elements, with the exception of As, were largely stored in digestive gland; particularly Cd that reached concentrations between 57 and 509 mg g 1. Significant relationships between tissues were found for Co (digestive gland–gills), As (gills–mantle) and Cd (digestive gland–mantle). Proportionality of Cd concentrations between mantle and digestive gland suggested that detoxification capacity by digestive gland was insufficient to avoid the transfer of this element to mantle and other tissues. Nonetheless, Cd concentrations in the mantle were always below the regulatory limit and, therefore lack of constraints for human consumption. On the basis of the fishery landings, one may estimate that up to 1 t of Cd can be annually removed by jumbo squid fisheries. & 2014 Elsevier Inc. All rights reserved.
Keywords: Trace elements Jumbo squid Dosidicus gigas Gulf of California
Contents 1. 2. 3. 4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Material and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Trace element partitioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Relations of trace element accumulation between tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Vehicle of cadmium transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Trace element concentrations in cephalopods have received increasing interest in the last decade due to the recognition of species being able to accumulate high levels of essential and nonessential elements in key tissues (e.g. Martin and Flegal, 1975; Miramand and Guary, 1980; Finger and Smith, 1987; Miramand and Bentley, 1992; Bustamante et al., 2000; Kojadinovica et al., 2011). Digestive gland, which plays a key function in the digestive process (Mangold, 1983) is the major storage site of trace elements
n
Corresponding author. E-mail address: [email protected] (J. Raimundo).
0147-6513/$ - see front matter & 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2014.01.026
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(Martin and Flegal, 1975; Miramand and Guary, 1980). For example, Cd in digestive gland of some cephalopod species may reach 98% of the total body burden (Bustamante et al., 2002a). Such high retention of this potentially toxic element is predictably associated with detoxification mechanisms minimizing the Cd mobility among key tissues (Simkiss and Taylor, 1982; Phillips and Rainbow, 1989; Bustamante et al., 2002a, b; Raimundo et al., 2008, 2010a, b). Besides this retention ability, environmental and biological factors, such as availability in water and food, exposure period, temperature, size, sex, and maturity stage may also influence the bioaccumulation values (e.g. Barghigiani et al., 2000; Miramand and Bentley, 1992; Pierce et al., 2008; Raimundo et al., 2004, 2005; Pereira et al., 2009; Pernice et al., 2009). High accumulation of trace elements
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associated with the short life span led several authors to consider cephalopod species as potential indicators of environmental contamination (Miramand and Bentley, 1992; Bustamante et al., 2002a). The jumbo (or Humboldt) squid, Dosidicus gigas, is a large and powerful jet-propelled predator, that reaches more than 2 m total length and 50 kg in mass (Nesis, 1983). This species is endemic of the Eastern Tropical Pacific (ETP) and with a longevity generally assumed to be no more than 12–24 months (Nigmatullin et al., 2001). Besides supporting a large fishery, it also plays a critical role in the ETP ecosystem both as prey and predator (Rosa et al., 2013). Interestingly, in the last ten years, this squid has greatly extended its tropical/subtropical range polewards in both hemispheres, where it is exerting a significant top–down control on commercial fish stocks (Zeidberg and Robison, 2007; Keyl et al., 2008). This species can easily remove more than 4 million t of food per year (mainly myctophid fishes) from the ETP pelagic food web (Rosa and Seibel, 2010). In terms of behavioral ecology, the jumbo squid undergoes diel vertical migrations to intermediate depths where it encounters zones of low oxygen (Rosa and Seibel, 2008, 2010). These oxygen minimum zones greatly limit the vertical distribution and ecology of many marine animals (Prince and Goodyear, 2006), but the jumbo squid thrive in such harsh environment by managing hypoxia via metabolic suppression (Trübenbach et al., 2013a, b). Because jumbo squid is large and abundant, it transfers large amounts of energy from lower trophic levels to top vertebrate predators. Despite of the ecological (and economical) importance, the capability of jumbo squids to concentrate metals in their tissues has not been documented, and it is not known if they constitute a significant vector of contaminants to top predator
species that feed on them, namely blue marlins, swordfish, sail fish, sharks and marine mammals (Rosa et al., 2013). The aim of the present study is to inventory, for the first time, the concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb in the gills, mantle and digestive gland of the jumbo squid, D. gigas capture in the Gulf of California, one of marine ecosystems with the highest productivity and biodiversity in the world.
2. Material and methods Sixteen adult jumbo squids (Dosidicus gigas) were collected, with dip-nets and hand-lines with jigs, in the Gulf of California, between Santa Rosalia, Guyamas and San Rafael basin (271N, 1111W; 281N, 1131W) (Fig. 1), in June 2011, aboard the RV New Horizon (Scripps Institute, California). Specimens were weighted, measured (mantle length), sex determined, dissected, and gills, mantle (without skin) and digestive gland separated. Maturity stages were assigned according to the classification of Markaida and Sosa-Nishizaki (2001), more specifically: I and II, immature; III, maturing; IV and V, mature and VI, spent. The individual samples were immediately frozen in liquid nitrogen onboard, and then transferred to 80 1C in the lab. Afterwards, the tissue samples were freeze-dried, grounded and homogenized for the analytical procedures. Elements were determined in samples after digestion with a mixture of HNO3 (sp, 65 % v/v) and H2O2 (sp, 30 % v/v) at different temperatures according to the method described in Ferreira et al. (1990). All lab ware was cleaned with HNO3 (20 %) for two days and rinsed with Milli-Q water to avoid contamination. Three procedural blanks were prepared using the same analytical procedure and reagents, and included within each batch of samples. Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb were determined by a quadrupole ICP-MS (Thermo Elemental, X-Series). The accuracy of these analytical methods was assessed by the analysis of international certificate standards (DORM-2, dogfish muscle, DORM-3, fish protein; DOLT-3 and 4, fish liver and TORT-2, lobster hepatopancreas). The results obtained did not differ significantly (p o 0.05) from the certified values (Table 1). Procedural blanks always
Fig. 1. Sampling location of Dosidicus gigas in the Gulf of California.
0.045 7 0.035 0.065 7 0.007 – – – – – – 0.43 70.27 0.357 0.13 0.0377 0.008 0.043 7 0.008 0.26 70.026 0.290 70.020 18.2 7 1.0 19.4 7 0.6 – – 277 1.9 26.7 70.6 6.0 77.0 1.4 7 0.09 3.5 70.28 3.3 6.3 71.2 7.06 7 0.48 7.5 7 0.99 8.3 71.3 – – 16.3 7 4.8 18.17 1.1 6.0 71.0 6.88 70.30 – – – – – – 21.4 7 4.0 25.6 7 2.3 477 7.0 51.3 7 3.1 82 79.6 86.6 7 2.4 1117 6.1 1167 6 1727 22 1807 6 – – – – 28 74.5 31.2 7 1.0 28 72.3 31.2 7 1.1 – – – – 1.05 70.12 1.28 70.24 2.62 7 0.36 2.727 0.35 – – 2.0 7 0.34 2.50 7 0.19 0.26 7 0.38 0.1827 0.031 1.39 71.0 1.89 70.19 – – – – 0.43 7 0.044 0.517 0.09 – – 1.75 7 0.35 1.89 7 0.17 – – – – 0.65 7 0.12 0.777 0.15
2.63 7 2.2 3.66 7 0.34 – – – – – – 9.9 7 12 13.6 7 1.2
Pb (mg g 1, dw) Cd (mg g 1, dw) Se (mg g 1, dw) As (mg g 1, dw) Zn (mg g 1, dw) Cu (mg g 1, dw) Ni (mg g 1, dw) Co (mg g 1, dw)
– – – – – – – – 1.8 7 0.30 1.64 70.19 TORT-2
DOLT-4
DOLT-3
DORM-3
Obtained Certified Obtained Certified Obtained Certified Obtained Certified Obtained Certified
For the number of specimens used in this study (n¼ 16) trace element concentrations in the analyzed tissues did not varied significantly with mantle size, total weight or gender of D. gigas. Despite the limited number of specimens, to the best of our knowledge, this is the first attempt to assess the effect of biological parameters on trace element bioaccumulation in D. gigas. Therefore comparison to previous works can only be done to other species. The similar element composition observed for male and female is in line with findings for the squids Todarodes filippovae and Illex argentinus (Gerpe et al., 2000; Kojadinovica et al., 2011). However, the effect of this biological factor on the trace element
DORM-2
4. Discussion
Mn (mg g 1, dw)
The proportion female:male of the collected specimens was 9:7, being all in the maturation stages III and V. The mantle length and total weight of jumbo squids ranged within the intervals 32–73 cm and 0.9–13 kg, respectively. Total weight (TW) was correlated to mantle length (ML) through the exponential equation TW¼ 0.085 ML0.070. Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb concentrations in gills, mantle and digestive gland showed no significant differences (KW-H, po0.05) with total weight, mantle length or gender of D. gigas. Trace element concentrations of both genders and all sizes were thus treated together. Fig. 2 presents the median, the percentile 25th and 75th, minimum and maximum concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb concentrations in gills, mantle and digestive gland of D. gigas specimens captured in the Gulf of California. Outliers and extreme points were not plotted to better visualize differences among tissues within smaller scales. Zinc and Cu were the most abundant elements. Although being considered as essential elements to organisms, concentration medians in the digestive gland ranged one order of magnitude for Zn (22– 238 mg g 1) and two for Cu (6.8–560 mg g 1). Narrower intervals were observed in gills (82–107 mg g 1 for Zn and 154–363 mg g 1 for Cu) and mantle (71–98 mg g 1 for Zn and 3.7–13 mg g 1 for Cu). Partitioning among the three tissues varied with the element, medians decreasing from: 161 mg g 1 (Cd) to 0.25 mg g 1 (Pb) in digestive gland, 21 mg g 1 (As) to 0.065 mg g 1 (Pb) in mantle, and 18 mg g 1 (As) to 0.090 mg g 1 (Pb) in gills. In general, digestive gland presented higher variability than gills and mantle. Manganese and Cr were more abundant in gills differing significantly (U, p o0.05) from the other two tissues. Vanadium, Co, Ni, Se, Cd and Pb exhibited significantly (U, p o0.05) higher concentrations in digestive gland than in gills and mantle. Arsenic was significantly (U, p o0.05) lower in digestive gland. Copper concentrations were similar in gills and digestive gland, and Zn in the three tissues. Despite most trace elements being largely stored in the digestive gland, linear and positive relations were found for Co, As and Cd among mantle, gills and digestive gland (Fig. 3). These relations may elucidate element pathway in the analyzed species and redistribution among these tissues.
Cr (mg g 1, dw)
3. Results
181
V (mg g 1, dw)
accounted for less than 1 % of the total metal in the samples. All the results are given as medians and ranges in microgram per gram of tissue dry weight (mg g 1, dw). Prior to statistical analyses, metal concentrations were tested for normality and equality of variances. Non-compliance with parametric ANOVA assumptions led to employment of the Kruskal-Wallis H (KW-H) and Mann-Whitney (U) nonparametric tests to evaluate the existing differences between element concentrations in tissues and between genders. The significance for statistical analyses used was always p o0.05. The statistical analyses were performed using STATISTICA (Statsoft).
Table 1 Concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb (mg g 1, dry weight) in fish muscle and protein (DORM-2 and DORM-3, respectively), fish liver (DOLT-3 and DOLT-4) and lobster hepatopancreas (TORT-2) obtained in the present study and certified values.
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
5
1.2
4
1.0 Cr (µg g -1)
V (µg g -1)
182
3 2
0.2
0
0.0
Mantle Digestive gland
4
8
3
6
Co (µg g -1)
Mn (µg g -1)
Gill
2 1
Gill
Mantle
Mantle
Gill
Mantle Digestive gland
Digestive gland
500 Cu (µg g -1)
Ni (µg g -1)
Gill
600
6 4 2
400 300 200 100
Gill
0
Mantle Digestive gland
40
As (µg g -1)
300
200
100
0
Mantle Digestive gland
4
0
Digestive gland
8
0
Gill
2
0
Zn (µg g -1)
0.6 0.4
1
30 20 10 0
Gill
Mantle
Digestive gland
Gill
Mantle Digestive gland
300
20 Cd (µg g -1)
15 Se (µg g -1)
0.8
10
200
100 5 0
0 Gill
Mantle Digestive gland
Gill
Mantle Digestive gland
Gill
Mantle Digestive gland
Pb (µg g -1)
0.6
0.4
0.2
0.0
Fig. 2. Median, percentile 25th and 75th, minimum and maximum concentrations of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Cd and Pb (mg g 1, dry weight) in the gills, mantle and digestive gland of Dosidicus gigas captured in the Gulf of California.
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
0.05
6
CoMantle (µg g-1)
CoDig gland (µg g-1)
8
y = 50.46x + 0.060 R2 = 0.80
4 2 0 0.00
0.02
0.04
0.06
0.08
y = 50.46x + 0.060 R2 = 0.80
0.04 0.03 0.02 0.01 0.00
0.10
0
-1
CdMantle (µg g-1)
AsMantle (µg g-1)
10
0
10
20
6
8
4
20
0
4 CoDig gland (µg g )
y = 1.007x -1.859 R2 = 0.90
30
2
-1
CoGills (µg g ) 40
183
30
40
Asgills (µg g-1)
3
y = 165.8x + 63.82 R2 = 0.86
2 1 0
0
200
400
600
CdDig gland (µg g-1)
Fig. 3. Relationships between gills, mantle and digestive gland for Co, As and Cd concentrations (mg g 1, dry weight) in Dosidicus gigas from the Gulf of California.
accumulation in cephalopods is far from being consensual (e.g. Barghigiani et al., 2000; Bustamante et al., 1998; Seixas and Pierce, 2005; Bustamante et al., 2006; Raimundo et al., 2010a). Presumably, other biologic or environmental factors mitigate the effect of gender on trace element accumulation. It is documented that females mature later than males in the Gulf of California (Markaida et al., 2004). Individuals used in the current work presenting maturation stage between III and V limited the conclusion on trace element concentrations being influenced by the maturation. 4.1. Trace element partitioning Digestive gland was the preferential organ of the jumbo squid for the accumulation of V, Co, Ni, Se, Cd and Pb, like reported for Architeuthis dux and Todarodes filippovae (e.g. Bustamante et al., 2008; Kojadinovica et al., 2011). High retention of potentially toxic elements is admittedly associated with detoxification mechanisms existing in the digestive gland, like metallothioneins and high molecular weight proteins (Simkiss and Taylor, 1982; Phillips and Rainbow, 1989; Bustamante et al., 2002b; Raimundo et al., 2010a, c). As observed for various cephalopod species, Cd concentrations in the jumbo squid were elevated (57–509 mg g 1). The comparison with the literature (Table 2) shows that those registered values were one order of magnitude above the ones obtained for Todaropsis eblanae, Todarodes sagittatus, Nototodarus gouldi, A. dux, Loligo opalescens, Loligo forbesi and Alloteuthis sp., comparable to Ommastrephes bartrami and Sthenoteuthis oualaniensis, and lower than in T. filippovae. That broad interval of concentrations, like observed for other species, is in line with the hypothesis of accumulation being linked to detoxification mechanisms preventing the toxicity effect of such high Cd accumulation. Similar mechanisms are considered in the digestive gland of the various cephalopod species (Bustamante et al., 2002b; Raimundo et al., 2010a, c). Concentration of V, Cr, Mn, Co, Ni, Cu, Zn, As, Se and Pb were compared to values found in other species (Table 2). Narrow intervals suggest that accumulated values primarily reflect the ingested food composition rather than retention mechanisms in response to toxicity. Gills presented significantly higher concentrations of Cr and Mn than the other analyzed tissues. Enhanced values of Mn and As in gills were also registered in the squid T. filippovae (Kojadinovica
et al., 2011). Association of Cr, Mn, Zn and As with the gills of jumbo squid may be interpreted as direct uptake of these elements from seawater. This interpretation has been invoked to Cr, Ni, Cd and Zn in other cephalopod species (Koyama et al., 2000; Miramand et al., 2006; Bustamante et al., 2002a, 2008). Contrarily to all the determined elements in this work, As concentrations in gills were similar to the values registered in mantle and significantly higher than in digestive gland. A similar distribution pattern was observed for As in A. dux captured in Spanish waters (Bustamante et al., 2008) and in T. filippovae from Tasmania and southern Indian Ocean (Kojadinovica et al., 2011). This partitioning has been attributed to different mobility of As chemical forms (Francesconi, 2010). Copper in gills is probably linked to the presence of the heamocyanin (respiratory pigment), in which this element is one of the main components (Soldevilla, 1987; Villanueva and Bustamante, 2006; Craig and Overnell, 2003). Cadmium concentrations were similar to the ones found in T. sagittatus and higher than in L. forbesi captured in the UK waters (Pierce et al., 2008). The enhancement of Cd concentrations in ommastrephids (D. gigas and T. sagittatus) in comparison to loliginids (L. forbesi) was already reported by Pierce et al. (2008) and attributed to differences in feeding and physiological characteristics of the digestive gland. Mantle of D. gigas presented low element concentrations, as found in other cephalopods, (Miramand and Guary, 1980; Miramand and Bentley, 1992; Raimundo et al., 2004, 2008; Pierce et al., 2008). The contrasting difference of Cd concentrations between mantle and digestive gland is remarkable in the jumbo squid, as well as in other cephalopods. Presumably the detoxification mechanism existing in the digestive gland prevents the partitioning of this potential toxic element for other tissues, namely mantle (Bustamante et al., 2002b; Raimundo et al., 2008, 2010a). However, Cd concentrations in the mantle of D. gigas were two to three orders of magnitude higher than in T. sagittatus, L. forbesi and Alloteuthis sp., although similar to T. filippovae and T. eblanae. Concentrations of As in the mantle of D. gigas were comparable to the ones found in T. filippovae (Table 2). 4.2. Relations of trace element accumulation between tissues Despite the storage of several trace elements in the digestive gland, the linear and positive relations of Co (digestive gland–gills and digestive gland–mantle) and Cd (digestive gland–mantle)
184
Table 2 Comparison of element concentrations (mg g 1, dw) in gills, mantle and digestive gland of Dosidicus gigas from the present study with squid data from the literature. Tissue
V (mg g 1, dw)
Cr (mg g 1, dw)
Mn (mg g 1, dw)
Co (mg g 1, dw)
Ni (mg g 1, dw)
Cu (mg g 1, dw)
Zn (mg g 1, dw)
As (mg g 1, dw)
Se (mg g 1, dw)
Cd (mg g 1, dw)
Pb (mg g 1, dw)
Ref.
Dosidicus gigas
Gills Mantle Dig Gland Gills Muscle Dig Gland Gills Muscle Dig gland Gills Muscle Dig gland Dig Gland
0.49–0.70 0.20–0.38 0.50–12 0.04–0.38 o DL 0.21–2.7 – – – – – – –
0.58–1.2 0.43–2.0 0.36–5.0 0.19–4.0 o DL 0.070–0.87 – – – – – – –
1.9–3.0 0.26–0.67 0.76–2.2 1.5–14 o DL 0.94–3.7 – – – – – – –
0.020–0.21 0.0020–0.044 0.060–4.6 0.060–4.3 0.030–0.35 0.31-35 – – – – – – –
0.15–25 0.060–4.6 1.1–7.4 0.15–4.6 o DL 0.20–13 – – – – – – –
154–363 3.7–13 6.8–560 95–763 2.9–14 5.0–865 – – – – – – 363 7 238
82–107 71–98 22–333 71–97 49–84 1.2–307 – – – – – – 830 7 355
11–34 10–33 8.1–20 3.5–32 8.4–23 6.0–41 – – – – – – –
4.5–7.0 1.6–3.2 4.3–19 0.36–5.0 o DL 0.78–33 – – – – – – –
6.5–17 0.13–2.4 57–509 2.3–69 0.060–3.6 34–883 5.7 7 5.1 1.6 7 2.2 257 26 8.7 7 9.0 0.30 7 7 0.30 657 61 337 30
0.031–0.18 0.032–0.48 0.063–0.70 0.050–0.90 oDL 0.020–1.5 – – – – – – –
a
Dig Gland
–
–
4.2 71.1
–
–
246 7298
696 7 295
–
–
507 25
–
e
Dig Gland
–
–
–
–
–
195 7212
1637 55
–
–
287 7 202
–
f
Dig Gland Dig Gland Dig Gland Liver Liver Gills Muscle Dig gland Muscle Dig gland
– 2.2 71.9 1.7
– 0.93 7 0.41 0.49
– 2.7 72.1 2.3
– 3.3 7 1.8 4.8
– 0.62 7 0.54 1.4
17207 151 108 783 1218 5350 73210 83707 3130 – – – – –
5137 288 1037 51 219 2477 131 449 7 201 – – – – –
– 48 7 14 44
– – –
782 7 255 617 46 91 857 52 1227 58 0.25 7 0.32 0.093 7 0.15 127 10 0.80 7 0.20 9.5 7 2.3
– 0.417 0.33 0.85
Todarodes filippovae Todaropsis eblanae Todarodes sagittatus Nototodarus gouldi Nototodarus gouldi Ommastrephes bartrami Symplectoteuthis oualaniensis Architeuthis dux Loligo opalescens Loligo forbesi
Alloteuthis sp.
a
– – – – –
– – – – –
– – – – –
– – – – –
Present study. Kojadinovica et al. (2011). Ranges are the minimum and the maximum obtained for both sampled areas. c Pierce et al. (2008). d Finger and Smith (1987). e Smith et al. (1984). f Martin and Flegal (1975). g Bustamante et al. (2008). b
– – – – –
– – – – –
– – – – –
b
c
d
g
f
– – – – –
c
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
Species
J. Raimundo et al. / Ecotoxicology and Environmental Safety 102 (2014) 179–186
suggest redistribution of these elements within the jumbo squid. Although ingested food has been appointed the main accumulation pathway for Co (Bustamante et al., 2004), the proportionality found among the three analyzed tissues indicates Co mobility as this element is uptake either through ingested food or water. Presumably, redistribution is induced by its essential role in the vitamin B12, which is important in cell division (Nolan et al., 1992). Despite this essentiality, values of Co in the digestive gland, gills and mantle of D. gigas were lower than in other species (Table 2). The digestive glandmantle relation observed for Cd suggests its uptake as ingested food, which is not entirely retained in the digestive gland. Whether detoxification capacity by this gland was surpassed cannot be clarified in this work. Linear relations between gills and mantle for As, which is not highly stored in the digestive gland, may be related to its preferential uptake through water, as proposed by Kojadinovica et al. (2011), followed by the transference to the mantle as arsenobetaine that may mimic the glycine betaine (Francesconi, 2010). However, a different pathway for As accumulation was proposed for Octopus vulgaris by Semedo et al. (2012). The distinct preferential via of As uptake in squids and octopus, is probably associated with the species life style, feeding habits and physiology. 4.3. Vehicle of cadmium transfer Trace element concentrations in the Gulf of California, where jumbo squids were captured, are generally attributed to natural factors related to upwelling and biogeochemistry of the region. Enhanced Cd concentrations in coastal waters could be associated with upwelling of bottom waters enriched by Cd diffused from the sediments (Segovia-Zavala et al., 1998). However, the potential contribution of anthropogenic sources like mining and urbanization cannot be dismissed (Shumilin et al., 2000, 2001). No constraints are predicted for human consumption of jumbo squids since Cd concentrations in the edible parts (mainly mantle, median of 0.11 mg g 1, wet weigh) are far below the regulatory limit established by the European Commission (1 mg g 1, wet weigh, Commission Regulation (EC) No. 629/2008). However, the noteworthy aspect comes mainly from the high Cd concentrations in digestive gland, and the size and abundance of jumbo squid in the Gulf of California. Together with the transference of large amounts of energy from lower trophic levels to top vertebrate predators, this specie appears to be a significant vector of Cd to top predator species that feed on them, namely blue marlins (AbitiaCardenas et al., 2010), swordfish (Markaida and Hochberg, 2005; Castillo et al., 2007), sail fish (Arizmendi-Rodriguez et al., 2006), sharks (Pardo-Gandarillas et al., 2007; Cabrera-Chavez-Costa et al., 2010) and marine mammals (Jaquet and Gendron, 2002; Ruiz-Cooley et al., 2004; Davis et al., 2007). In addition, a considerable amount of Cd should be accounted to be removed from the marine ecosystem by fishing. Assuming that the mantle accounts for 70‐80% of the body weight, and the digestive gland around 3%, and based on the fishery landings (SAGARPA, 2012; Rosa et al., 2013), one may estimate that up to 1 t of Cd can be annually removed by jumbo squid fisheries.
Acknowledgments The authors would like to thank Brad Seibel for making the participation in the research cruise aboard RV New Horizon possible and Unai Markaida for his assistance in collecting the specimens. Bárbara Anes for the ICP-MS analyses and the anonymous reviewers for the commentaries. The Portuguese Foundation for Science and Technology (FCT) supported this study through a Senior Research Position (Ciência 2007) to Rui Rosa and the Pos-doc grant (SFRH/BPD/91498/2012) to Joana Raimundo.
185
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