Marine Pollution Bulletin 79 (2014) 348–353

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Baseline

Essential, trace and toxic element concentrations in the liver of the world’s largest bony fish, the ocean sunfish (Mola mola) Justin R. Perrault a,⇑, John P. Buchweitz b, Andreas F. Lehner b a b

Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236-1004, United States Diagnostic Center for Population and Animal Health, Michigan State University, 4125 Beaumont Road, Lansing, MI 48910-8104, United States

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Keywords: Ocean sunfish Mola mola Essential elements Trace elements Toxic elements Liver

a b s t r a c t No studies document essential (calcium, magnesium, phosphorus, potassium, sodium), trace (barium, boron, chromium, cobalt, copper, iron, manganese, molybdenum, selenium, zinc) or toxic element (antimony, arsenic, cadmium, lead, mercury, thallium) concentrations in any members of the family Molidae, including the world’s largest bony fish, the ocean sunfish (Mola mola). Here, we analyzed 21 elements in the liver of one M. mola. These values were compared to liver concentrations in multiple species with spatial and dietary overlap. Concentrations of calcium (3339 ppm wet weight) and iron (2311 ppm wet weight) were extremely elevated in comparison to a number of other fish species, indicating that calcium and/or iron toxicity may have occurred in this animal. Concentrations of toxic elements were generally low, with the exception of cadmium (3.5 ppm). This study represents the first report of essential, trace and toxic elements in this species. Ó 2013 Elsevier Ltd. All rights reserved.

The biology and ecology of the world’s largest marine bony fish, the ocean sunfish (Mola mola), remain poorly understood (Pope et al., 2010). Like other large bony fishes, the ocean sunfish makes long distance migrations (Potter et al., 2011; Potter and Howell, 2011). This species is unique in that they are known to forage on gelatinous organisms including jellyfishes, pyrosomes and salps (Fraser-Brunner, 1951; Thys, 1994); however, they are most likely not dietary specialists, with other prey items including leptocephali, sponges, annelids, crustaceans, mollusks and algae, among others (Desjardin, 2005; Syväranta et al., 2012). Some studies have documented trace element loads in potential gelatinous prey items of M. mola (Cimino et al., 1983; Templeman and Kingsford, 2012). Because members of this family may be long-lived (>20 years of age, Liu et al., 2009) and are extremely large in size (Pope et al., 2010), toxic element loads, including those that are detrimental to health and survival (antimony, arsenic, cadmium, lead, mercury, thallium), may accumulate in the body to concentrations that are harmful to physiologic processes. A number of other marine organisms, including chum salmon (Oncorhynchus keta), spiny dogfish (Squalus acanthias) and the leatherback sea turtle (Dermochelys coriacea) are known to prey on pelagic coelenterates (Bjorndal, 1997; Arai, 2005). Due to their resource overlap, the ocean sunfish and other organisms that prey on jellyfishes, pyrosomes and salps should be exposed to similar concentrations of essential, trace and toxic elements. Here, we ⇑ Corresponding author. Tel.: +1 941 388 4441x213; fax: +1 941 388 4312. E-mail address: [email protected] (J.R. Perrault). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.11.026

chose to analyze the liver of one M. mola for essential (calcium, magnesium, phosphorus, potassium, sodium), trace (barium, boron, chromium, cobalt, copper, iron, manganese, molybdenum, selenium, zinc) and toxic (antimony, arsenic, cadmium, lead, mercury, thallium) element concentrations and compare those concentrations to liver concentrations of fishes and leatherback turtles from the literature. On August 22, 2011, one freshly dead, stranded ocean sunfish was found on Juno Beach, Florida USA (26°530 300 0 N, 80°030 2100 W; Fig. 1). The organism was washing out to sea during the time of sampling, therefore morphometric data could not be collected; however, this organism was estimated at around 1.4 m in length. The ocean sunfish was necropsied on the beach in the surf zone and the liver was collected. The sample was stored at 15 °C until analyses could be conducted. The liver sample was processed at Michigan State University’s Diagnostic Center for Population and Animal Health (MSU DCPAH, Lansing, Michigan USA). Total mercury was analyzed by cold vapor atomic absorption spectrometry (Cetac M-6000A, Cetac Technologies Inc., Omaha, Nebraska USA). Total selenium was analyzed using inductively coupled plasma (ICP) mass spectrometry (Agilent ICP-MS 7500ce, Agilent Technologies, Santa Clara, California USA). All other elements (antimony, arsenic, barium, boron, cadmium, calcium, chromium, cobalt, copper, iron, lead, magnesium, manganese, molybdenum, phosphorus, potassium, sodium, thallium and zinc) were analyzed using ICP-atomic emission spectrometry (Varian Vista Pro with axial aligned torch, Agilent Technologies). One g of sample was used in analyses. The sample was digested overnight

J.R. Perrault et al. / Marine Pollution Bulletin 79 (2014) 348–353

Fig. 1. A stranded ocean sunfish (Mola mola) in Juno Beach, Florida USA. Anterior is to the left. The individual was estimated to be 1.4 m in length. Photo courtesy: K. Martin.

at 95 °C after addition of 2 mLs concentrated nitric acid (Avantor Performance Materials, Center Valley, Pennsylvania USA). Appropriate blanks and standards were used. The National Institute of Standards and Technology (NIST) Standard Reference MaterialsÒ 1577c Bovine Liver, 2976 Mussel Tissue and Alfa Aesar MultiElement Quality Control (QC)–21 (Ward Hill, Massachusetts USA) standard solutions were used as the quality controls. The limits of detection (LOD, ppm wet weight) were: mercury: 0.001 ppm; selenium: 0.01 ppm; barium, cadmium, copper, manganese, zinc: 0.05 ppm; cobalt, iron: 0.1 ppm; magnesium: 0.15 ppm; chromium, molybdenum: 0.2 ppm; arsenic, lead: 0.5 ppm; antimony, boron, calcium, phosphorus: 1.0 ppm; thallium: 2.5 ppm; potassium: 5 ppm; sodium: 10 ppm. Daily QC determination for each of the elements in QC materials typically shows them to be within one standard deviation of the expected mean concentration, with % confidence values as follows: (i) NIST Bovine Liver: calcium: 3.2%, copper: 0.94%, iron: 1.5%, magnesium: 1.5%, manganese: 1.3%, molybdenum: 1.8%, phosphorus: 2.0%, potassium: 2.7%, sodium: 1.5%, zinc: 1.3%; (ii) NIST Mussel Tissue: arsenic: 1.8%, barium: 4.6%, boron: 2.0%, lead: 4.9%, mercury: 3.7%, selenium: 2.1%; and (iii) Alfa Aesar Multi-Element: antimony: 1.3%, cadmium: 0.36%, chromium: 0.52%, cobalt: 0.72%, thallium: 1.1%. The results of essential, trace and toxic element analyses in the liver of the ocean sunfish are presented in Table 1. Essential elements were found at greater concentrations than toxic elements. The rank order concentrations were calcium > sodium > iron > phosphorus > potassium  magnesium  zinc  cadmium > copper > selenium > arsenic  manganese > mercury > cobalt = molybdenum > barium ( = difference of one order of magnitude). Antimony, boron, chromium, lead and thallium were all below the LOD. Comparisons to previously published reports of essential, trace and toxic element concentrations in a variety of fishes (Atlantic menhaden [Brevoortia tyrannus], chum salmon, grouper [Subfamily Epinephelinae], lake sturgeon [Acipenser fulvescens], pufferfish [Family Tetraodontidae], shark [Superorder Selachimorpha], shortfin mako [Isurus oxyrinchus], spiny dogfish and stingray [Family Myliobatidai]; from MSU DCPAH database; Hall et al., 1978; Scott and Latshaw, 1993) and leatherback turtle livers (Davenport et al., 1990; Edmonds et al., 1994; Godley et al., 1998; Caurant et al., 1999; Perrault, 2012; Poppi et al., 2012) are also presented in Table 1. The ocean sunfish had the highest liver concentrations of cadmium, calcium, cobalt, iron, magnesium and sodium compared to other fishes from the MSU DCPAH database and the literature (Table 1). This sample provided a unique opportunity to determine concentrations of essential, trace and toxic elements in the world’s

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largest bony fish, as encountering stranded individuals of this species is rare. Additionally, this study is unique as the majority of investigations regarding this organism focus on abundance, migrations and parasitology (Pope et al., 2010). Overall, the ocean sunfish had lower concentrations of toxic elements (arsenic, cadmium, mercury) in comparison to other large marine vertebrates, including cartilaginous sharks (Table 1, Hall et al., 1978; Wagemann and Muir, 1984; Edmonds et al., 1994; Dietz et al., 1996; Kubota et al., 2001). It is interesting to note that some concentrations of toxic elements are well below concentrations found to cause harm in other vertebrate species (Beyer et al., 1996). Concentrations of essential, trace and toxic elements are known to accumulate in the liver of bony fishes (Sorensen, 1991) and it was not unexpected that concentrations of essential elements were greater than toxic elements. Essential elements: The essential elements calcium (ranked 1st), magnesium (ranked 6th), phosphorus (ranked 4th), potassium (ranked 5th) and sodium (ranked 2nd) function in cellular metabolism and are known to bioconcentrate from water into fish tissues (Davis and Gatlin, 1996). In marine teleosts, it has been shown that calcium, phosphorus and sodium are more concentrated in the gills in comparison to other tissues (including liver), while potassium is least concentrated in the gills (Scott and Latshaw, 1993). While we did not measure concentrations of essential elements in gill tissue, our results indicate that this may also be true for the ocean sunfish, as potassium was the lowest in concentration (1350 ppm) in the liver in comparison to calcium (3339 ppm), sodium (3093 ppm) and phosphorus (1488 ppm). Magnesium was lowest in concentration of the essential elements (772 ppm), yet was still elevated in comparison to other fishes (Table 1) and may be at greater concentrations in bone compared to liver (Davis and Gatlin, 1996). Essential element concentrations in other fish species tended to be in the order potassium > sodium  phosphorus  magnesium > calcium, suggesting that interspecies differences occur with concentrations of essential elements (Table 1, MSU DCPAH database). Additionally, size, weight and seasonal factors may contribute to accumulation of essential elements in fish tissues (Ersoy and Çelik, 2010). We note that some essential elements (calcium, magnesium, sodium) were higher in the ocean sunfish in comparison to a number of other fish species (Table 1), with liver calcium concentrations being the highest of all elements. Additionally, potassium was ranked 4th among essential elements (and 5th among all elements), while it normally ranks highest in fishes (Table 1). In regards to liver calcium, members of the Chondrichthyes, Cyprinidae, Perciformes and Salmonidae families tend to have concentrations in the range of 32–197 ppm (in specimens submitted to DCPAH). Terrestrial species (e.g., cattle, horse, pig, and poultry) have a similar distribution (Puls, 1994). It is difficult to accept the high liver calcium concentration in the specimen reported here as representing the normal situation in this species, given that its value is as much as 100 times greater than that of other species. Values above 1000 ppm are typically considered toxic in cattle (i.e., may reflect exposure to calcium–oxalate or oxalic acid precursors such as ethylene glycol). The calcium:phosphorus ratio on a weight basis in cattle should be kept within tight tolerances of 1.8–2.1 in bone, reflected as roughly 0.05–0.10 in liver (Puls, 1994). The calcium:phosphorus ratio in this specimen’s liver was 2.24, which is elevated, about 20-fold to 40-fold greater than might be expected (the liver calcium:phosphorus ratio in Atlantic menhaden = 0.062; Scott and Latshaw, 1993). Additionally, ratios of calcium:phosphorus in whole fish range from 0.7 to 1.6 (Lall, 2002), which are still below the liver calcium:phosphorus ratio in the ocean sunfish. This suggests significant calcium mineralization of the liver as a result of toxic exposure. In mammals, elevated concentrations of calcium (and magnesium) may be due to renal failure (Ferguson and Hoenig, 2011), and it is possible that this organism died from a

350 Table 1 Essential, trace and toxic element concentrations (ppm wet weight) in the liver of an ocean sunfish and other species from the literature. Bolded items in each column represent the highest reported concentration(s) of that element. Reference

Location

Antimony

Arsenic

Barium

Boron

Cadmium

Calcium

Chromium

Cobalt

Copper

Ocean sunfish Atlantic menhadena Chum salmon Grouperb Lake Sturgeonb Leatherback turtle Pufferfishb Sharkb Shortfin mako Spiny dogfish Stingrayb

This study 1 2 MSU DCPAH MSU DCPAH 3–8 MSU DCPAH MSU DCPAH 2 2 MSU DCPAH

Florida Chesapeake Bay Alaska Not reported Great lakes Worldwide Not reported Not reported N. Atlantic N. Atlantic Not Reported

Essential, trace and toxic element concentrations in the liver of the world's largest bony fish, the ocean sunfish (Mola mola).

No studies document essential (calcium, magnesium, phosphorus, potassium, sodium), trace (barium, boron, chromium, cobalt, copper, iron, manganese, mo...
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