Marine Pollution Bulletin xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Baseline
Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast Efrat Shoham-Frider a,⇑, Dan Kerem b, Mia Roditi-Elasar b, Oz Goffman b, Danny Morick b,c, Olga Yoffe d, Nurit Kress a a
Israel Oceanography and Limnological Research, National Institute of Oceanography, Tel-Shikmona, P.O. Box 8030, Haifa 31080, Israel Israel Marine Mammal Research and Assistance Center, The Leon Recanati Institute for Maritime Studies and Department for Maritime Civilizations, The University of Haifa, Mt. Carmel, Haifa 31905, Israel c Department of Pathology, The Hebrew University Hadassah Medical School, Jerusalem 91120, Israel d Geological Survey of Israel, 30 Malkhe Israel St., Jerusalem 95501, Israel b
a r t i c l e
i n f o
Keywords: Dolphins Whales Stranding Eastern Mediterranean Trace elements
a b s t r a c t In this paper we present the concentrations of Hg, Cd, Se, Pb, Cu, Mn, Zn and Fe in organs of 6 noncommon specimens of cetaceans that were stranded along the Israeli Mediterranean coast (IMC), during 2002–2010: two fin whales, one minke whale, one Cuvier’s beaked whale, one rough-toothed dolphin, and one Risso’s dolphin. Most of the specimens were calves stranded by accident. Concentrations of Hg and Cd were low in tissues of the baleen whales and higher in the toothed whales, with maximum concentrations of 1067 mg kg 1 Hg in the liver of the Risso’s dolphin and 29 mg kg 1 Cd in the kidney of the Cuvier’s beaked whale. As far as we are aware, this is the first report of trace elements in baleen whales in the Eastern Mediterranean, and the first report of trace elements in minke whale and rough-toothed dolphin in the Mediterranean. Ó 2014 Elsevier Ltd. All rights reserved.
Six specimens of rarely stranded cetacean species were collected by IMMRAC (Israel Marine Mammal Research and Assistance Center) along the Israeli Mediterranean coast (IMC), during 2000–2010: Two specimens of fin whale (Balaenoptera physalus – Bp), one specimen of minke whale (Balaenoptera acutorostrata – Ba), one specimen of Cuvier’s beaked whale (Ziphius cavirostris – Zc), one rough-toothed dolphin (Steno bredanensis – Sb) – all males, and one female specimen of Risso’s dolphin (Grampus griseus – Gg). Despite the fact that three of these species (Sb, Zc and Gg) are defined as ‘regular’ and two (Ba and Bp) are defined as ‘visitors’ to the Levantine Basin (Kerem et al., 2012), all of the above species rarely strand along the IMC, compared to other regular species. During 1993–2009, stranding records included 4 specimens each of the species Ba and Bp and 6, 7 and 8 specimens of the species Gg, Zc and Sb, respectively (ibid). During the same period, strandings of 104 specimens of the common bottlenose dolphin Tursiops truncatus (IMMRAC, unpublished data), and of 15 specimens of striped dolphin Stenella coeruleoalba (Kerem et al., 2012) were recorded. ⇑ Corresponding author. Tel.: +972 544797500; fax: +972 48511911. E-mail addresses: [email protected] (E. Shoham-Frider), dankerem@research. haifa.ac.il (D. Kerem), [email protected] (M. Roditi-Elasar), ogoffman@gmail. com (O. Goffman), [email protected] (D. Morick), [email protected] (O. Yoffe), [email protected] (N. Kress).
Sighting records of these species are relatively rare too. For example, during a research cruise carried out in the summer of 2008 in the international waters of the Eastern Mediterranean Sea as well as in Turkish, Lebanese and Syrian territorial waters, the recorded specimens were 53 striped dolphins, 27 common bottlenose dolphins, 5 sperm whales (Physeter macrocephalus), 2 short-beaked common dolphins (Delphinus delphis) and 2 Risso’s dolphins (Dede et al., 2012). Data on tissue pollutant levels in cetaceans from the Levantine Basin of the Eastern Mediterranean are generally rare, and more so among non-common species. Our group reported on trace elements (TE) and organic pollutants concentrations in key-tissues of the common bottlenose dolphin, striped dolphin and Risso’s dolphin, collected along the IMC between 1993 and 2007 (Roditi-Elasar et al., 2003; Shoham-Frider et al., 2002, 2009). Published data on TE concentrations in non-common cetaceans from more western regions of the Mediterranean Sea are also scarce and mainly include data for Risso’s dolphin and Cuvier’s Beaked whale (Storelli et al., 1999; Frodello et al., 2002; Capelli et al., 2008; Bellante et al., 2009; Bilandzic’ et al., 2012). In this paper we present tissue TE concentrations in representatives of 6 regionally non-common species of cetaceans. As far as we are aware, this is the first report of TE concentrations in tissues of baleen whales (mysticeti) in the Eastern Mediterranean and the
http://dx.doi.org/10.1016/j.marpolbul.2014.03.017 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Shoham-Frider, E., et al. Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.017
2
E. Shoham-Frider et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
first report of TE concentrations in tissues of minke whale and rough-toothed dolphin in the Mediterranean. The whales and dolphins were found along the IMC from Akko in the north to Ashqelon in the south (Fig. 1). On May 08, 2000, a male calf minke whale (#97, Fig. 2a) was found dead in the early morning, entangled in a gill net, in 14 m seawater depth off Akko. The fresh carcass was stored in the freezer by fishermen and delivered to IMMRAC’s crew for autopsy within a few hours. The whale weighed 340 kg, was 355 cm long and seemed to be in good body condition. External inspection revealed net cut marks on the gums. Video-monitored endoscopy (Pentax) disclosed milk in the oesophagus and first stomach. Upon dissection, milk at various digestive stages was found along the entire GI tract with no evidence of other intakes other than small pieces of plastics (12 cm) in the third stomach. No gross pathology could be detected other than clear signs of drowning. On February 16, 2002, the very fresh mutilated body of a 1.6 m long (without the tail) male calf rough-toothed dolphin (#122), was found on the beach north of Atlit. All protruding appendages (dorsal fin, flippers and tail fluke) were amputated, the usual landmarks of gill-net entanglement, probably performed by the fishermen in an attempt to minimize damage to the net upon disentanglement. A large piece of the abdominal wall was cut off, probably to serve as bait (Fig. 2b). Cut marks from the net’s nylon mesh were observed on the head and some ribs were broken. The
Fig. 1. The locations and species (in brackets) of rare cetaceans found along the Israeli Mediterranean coast during 2000–2010.
dolphin either did not eat from the net, or else regurgitated whatever it did during its attempt to disentangle itself, as the stomach contained one large and several small squid beaks, and a few large, clean fish bones. Apart from froth in the airways, no gross pathology of the internal organs could be observed. Due to the obvious cause of death, it was deemed unnecessary to perform a detailed pathological investigation. On July 15, 2002, a severely emaciated Cuvier’s beaked whale (#130) was spotted by lifeguards in shallow water north of Herzliya. Attempts of swimmers to redirect it to the open sea failed, it was lifted on a stretcher and held in the water, but by the time of arrival of IMMRAC’s veterinarian, it had already succumbed. It was a 4.2 m long juvenile male, with an estimated weight of 400 kg. Four and a half kg of plastic waste were found in the fore-stomach, with few squid beaks. On February 15, 2007, the slightly decomposed body of a fin whale (#204) drifted into Haifa Port and was hoisted onto a truck for interment (Fig. 2c). It turned out to be an extremely emaciated male calf, 4500 kg in weight and 11.5 m in length, with no external signs of injury. A year later, on February 3, 2008, another fin whale male calve (#218) swam into the anchorage of the Eilat-Ashqelon Oil Pipeline installation in Ashqelon. Attempts to redirect it to open water failed and later on it rammed its head into the quay and soon succumbed. External inspection revealed a well-healed amputation of half of its left fluke by a ship’s propeller (Fig. 2d). It weighted 14,000 kg and was 13.4 m long. On April 18, 2010, the fresh carcass of a 294 cm long and 300 kg estimated weight, juvenile Risso’s dolphin female (#244) was found on the Ashdod’s shore (southern Israel, Fig. 2e). It was transported to the Koret School of Veterinary Medicine, where it was kept refrigerated (4 °C) and was autopsied 21 h later. Autopsy Findings of this specimen were detailed in Elad et al. (2010). Tissue samples (muscle, liver, kidney and blubber) for trace element determinations (Hg, Cd, Cu, Zn, Fe, Mn, Pb and Se) were sampled into plastic containers and kept frozen at 20 °C until analysis. Wet samples were digested in duplicates, with concentrated nitric acid in Teflon-lined, high pressure decomposition vessels as described by Hornung et al. (1989). The solutions were analyzed specifically for Cd, Cu, Zn, Mn, Fe and Pb by atomic absorption spectrophotometry with flame and graphite furnace, on a Varian A220 and AA880 spectrophotometer equipped with a deuterium-arc background corrector. Hg analyses were performed by cold vapour atomic fluorescence spectrometry (CVAFS) with a Merlin Millenium system (PS Analytical, UK), after SnCl2 reduction and purging with high purity argon. Selenium was measured by inductively-coupled plasma mass spectrometry (Perkin–Elmer, Elan-DRC-a). Detection limits for Se, Cd, Cu, Zn, Fe, Mn, Pb and Hg were 0.001, 0.001, 0.08, 0.06, 0.5, 0.08, 0.01 and 5 * 10 6 mg kg 1 wet weight, respectively. Chemical blanks that were run during the analysis presented no evidence of contamination. Quality control and quality assurance of tissue trace element determinations were performed on certified standard reference material from the National Research Council of Canada (NRCC – DORM 3 – fish protein certified reference material for trace metals). The standards were digested and analyzed in the same manner as the samples with each analytical run and gave results within 5% of the certified values. All presented results are averages of duplicate assays and are expressed on a tissue wet weight basis. The concentrations of Hg, Se, Cd, Pb, Cu, Zn, Mn and Fe in tissues of the six specimens analyzed are presented in Tables 1 and 2, together with previously published data for the same species from other areas. To enable comparison, data reported in dry weight was transformed to wet weight assuming 25% dry matter content (Becker et al., 1995). The comparison to other studies on same species discussed below is qualitative rather than statistically-based, because of the small number of specimens analyzed in this study.
Please cite this article in press as: Shoham-Frider, E., et al. Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.017
E. Shoham-Frider et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
3
Fig. 2. The male calf minke whale, by-caught off Akko (a), the by-caught rough-toothed dolphin calf found off Atlit (b), the two fin whale calves, one of which drifted dead into Haifa port (c) and the other that live-stranded in Ashqelon (d) and the Risso’s dolphin female stranded off Ashdod (e).
Mercury and Selenium in baleen whales: Concentrations of Hg were low (
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Baseline
Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast Efrat Shoham-Frider a,⇑, Dan Kerem b, Mia Roditi-Elasar b, Oz Goffman b, Danny Morick b,c, Olga Yoffe d, Nurit Kress a a
Israel Oceanography and Limnological Research, National Institute of Oceanography, Tel-Shikmona, P.O. Box 8030, Haifa 31080, Israel Israel Marine Mammal Research and Assistance Center, The Leon Recanati Institute for Maritime Studies and Department for Maritime Civilizations, The University of Haifa, Mt. Carmel, Haifa 31905, Israel c Department of Pathology, The Hebrew University Hadassah Medical School, Jerusalem 91120, Israel d Geological Survey of Israel, 30 Malkhe Israel St., Jerusalem 95501, Israel b
a r t i c l e
i n f o
Keywords: Dolphins Whales Stranding Eastern Mediterranean Trace elements
a b s t r a c t In this paper we present the concentrations of Hg, Cd, Se, Pb, Cu, Mn, Zn and Fe in organs of 6 noncommon specimens of cetaceans that were stranded along the Israeli Mediterranean coast (IMC), during 2002–2010: two fin whales, one minke whale, one Cuvier’s beaked whale, one rough-toothed dolphin, and one Risso’s dolphin. Most of the specimens were calves stranded by accident. Concentrations of Hg and Cd were low in tissues of the baleen whales and higher in the toothed whales, with maximum concentrations of 1067 mg kg 1 Hg in the liver of the Risso’s dolphin and 29 mg kg 1 Cd in the kidney of the Cuvier’s beaked whale. As far as we are aware, this is the first report of trace elements in baleen whales in the Eastern Mediterranean, and the first report of trace elements in minke whale and rough-toothed dolphin in the Mediterranean. Ó 2014 Elsevier Ltd. All rights reserved.
Six specimens of rarely stranded cetacean species were collected by IMMRAC (Israel Marine Mammal Research and Assistance Center) along the Israeli Mediterranean coast (IMC), during 2000–2010: Two specimens of fin whale (Balaenoptera physalus – Bp), one specimen of minke whale (Balaenoptera acutorostrata – Ba), one specimen of Cuvier’s beaked whale (Ziphius cavirostris – Zc), one rough-toothed dolphin (Steno bredanensis – Sb) – all males, and one female specimen of Risso’s dolphin (Grampus griseus – Gg). Despite the fact that three of these species (Sb, Zc and Gg) are defined as ‘regular’ and two (Ba and Bp) are defined as ‘visitors’ to the Levantine Basin (Kerem et al., 2012), all of the above species rarely strand along the IMC, compared to other regular species. During 1993–2009, stranding records included 4 specimens each of the species Ba and Bp and 6, 7 and 8 specimens of the species Gg, Zc and Sb, respectively (ibid). During the same period, strandings of 104 specimens of the common bottlenose dolphin Tursiops truncatus (IMMRAC, unpublished data), and of 15 specimens of striped dolphin Stenella coeruleoalba (Kerem et al., 2012) were recorded. ⇑ Corresponding author. Tel.: +972 544797500; fax: +972 48511911. E-mail addresses: [email protected] (E. Shoham-Frider), dankerem@research. haifa.ac.il (D. Kerem), [email protected] (M. Roditi-Elasar), ogoffman@gmail. com (O. Goffman), [email protected] (D. Morick), [email protected] (O. Yoffe), [email protected] (N. Kress).
Sighting records of these species are relatively rare too. For example, during a research cruise carried out in the summer of 2008 in the international waters of the Eastern Mediterranean Sea as well as in Turkish, Lebanese and Syrian territorial waters, the recorded specimens were 53 striped dolphins, 27 common bottlenose dolphins, 5 sperm whales (Physeter macrocephalus), 2 short-beaked common dolphins (Delphinus delphis) and 2 Risso’s dolphins (Dede et al., 2012). Data on tissue pollutant levels in cetaceans from the Levantine Basin of the Eastern Mediterranean are generally rare, and more so among non-common species. Our group reported on trace elements (TE) and organic pollutants concentrations in key-tissues of the common bottlenose dolphin, striped dolphin and Risso’s dolphin, collected along the IMC between 1993 and 2007 (Roditi-Elasar et al., 2003; Shoham-Frider et al., 2002, 2009). Published data on TE concentrations in non-common cetaceans from more western regions of the Mediterranean Sea are also scarce and mainly include data for Risso’s dolphin and Cuvier’s Beaked whale (Storelli et al., 1999; Frodello et al., 2002; Capelli et al., 2008; Bellante et al., 2009; Bilandzic’ et al., 2012). In this paper we present tissue TE concentrations in representatives of 6 regionally non-common species of cetaceans. As far as we are aware, this is the first report of TE concentrations in tissues of baleen whales (mysticeti) in the Eastern Mediterranean and the
http://dx.doi.org/10.1016/j.marpolbul.2014.03.017 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Shoham-Frider, E., et al. Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.017
2
E. Shoham-Frider et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
first report of TE concentrations in tissues of minke whale and rough-toothed dolphin in the Mediterranean. The whales and dolphins were found along the IMC from Akko in the north to Ashqelon in the south (Fig. 1). On May 08, 2000, a male calf minke whale (#97, Fig. 2a) was found dead in the early morning, entangled in a gill net, in 14 m seawater depth off Akko. The fresh carcass was stored in the freezer by fishermen and delivered to IMMRAC’s crew for autopsy within a few hours. The whale weighed 340 kg, was 355 cm long and seemed to be in good body condition. External inspection revealed net cut marks on the gums. Video-monitored endoscopy (Pentax) disclosed milk in the oesophagus and first stomach. Upon dissection, milk at various digestive stages was found along the entire GI tract with no evidence of other intakes other than small pieces of plastics (12 cm) in the third stomach. No gross pathology could be detected other than clear signs of drowning. On February 16, 2002, the very fresh mutilated body of a 1.6 m long (without the tail) male calf rough-toothed dolphin (#122), was found on the beach north of Atlit. All protruding appendages (dorsal fin, flippers and tail fluke) were amputated, the usual landmarks of gill-net entanglement, probably performed by the fishermen in an attempt to minimize damage to the net upon disentanglement. A large piece of the abdominal wall was cut off, probably to serve as bait (Fig. 2b). Cut marks from the net’s nylon mesh were observed on the head and some ribs were broken. The
Fig. 1. The locations and species (in brackets) of rare cetaceans found along the Israeli Mediterranean coast during 2000–2010.
dolphin either did not eat from the net, or else regurgitated whatever it did during its attempt to disentangle itself, as the stomach contained one large and several small squid beaks, and a few large, clean fish bones. Apart from froth in the airways, no gross pathology of the internal organs could be observed. Due to the obvious cause of death, it was deemed unnecessary to perform a detailed pathological investigation. On July 15, 2002, a severely emaciated Cuvier’s beaked whale (#130) was spotted by lifeguards in shallow water north of Herzliya. Attempts of swimmers to redirect it to the open sea failed, it was lifted on a stretcher and held in the water, but by the time of arrival of IMMRAC’s veterinarian, it had already succumbed. It was a 4.2 m long juvenile male, with an estimated weight of 400 kg. Four and a half kg of plastic waste were found in the fore-stomach, with few squid beaks. On February 15, 2007, the slightly decomposed body of a fin whale (#204) drifted into Haifa Port and was hoisted onto a truck for interment (Fig. 2c). It turned out to be an extremely emaciated male calf, 4500 kg in weight and 11.5 m in length, with no external signs of injury. A year later, on February 3, 2008, another fin whale male calve (#218) swam into the anchorage of the Eilat-Ashqelon Oil Pipeline installation in Ashqelon. Attempts to redirect it to open water failed and later on it rammed its head into the quay and soon succumbed. External inspection revealed a well-healed amputation of half of its left fluke by a ship’s propeller (Fig. 2d). It weighted 14,000 kg and was 13.4 m long. On April 18, 2010, the fresh carcass of a 294 cm long and 300 kg estimated weight, juvenile Risso’s dolphin female (#244) was found on the Ashdod’s shore (southern Israel, Fig. 2e). It was transported to the Koret School of Veterinary Medicine, where it was kept refrigerated (4 °C) and was autopsied 21 h later. Autopsy Findings of this specimen were detailed in Elad et al. (2010). Tissue samples (muscle, liver, kidney and blubber) for trace element determinations (Hg, Cd, Cu, Zn, Fe, Mn, Pb and Se) were sampled into plastic containers and kept frozen at 20 °C until analysis. Wet samples were digested in duplicates, with concentrated nitric acid in Teflon-lined, high pressure decomposition vessels as described by Hornung et al. (1989). The solutions were analyzed specifically for Cd, Cu, Zn, Mn, Fe and Pb by atomic absorption spectrophotometry with flame and graphite furnace, on a Varian A220 and AA880 spectrophotometer equipped with a deuterium-arc background corrector. Hg analyses were performed by cold vapour atomic fluorescence spectrometry (CVAFS) with a Merlin Millenium system (PS Analytical, UK), after SnCl2 reduction and purging with high purity argon. Selenium was measured by inductively-coupled plasma mass spectrometry (Perkin–Elmer, Elan-DRC-a). Detection limits for Se, Cd, Cu, Zn, Fe, Mn, Pb and Hg were 0.001, 0.001, 0.08, 0.06, 0.5, 0.08, 0.01 and 5 * 10 6 mg kg 1 wet weight, respectively. Chemical blanks that were run during the analysis presented no evidence of contamination. Quality control and quality assurance of tissue trace element determinations were performed on certified standard reference material from the National Research Council of Canada (NRCC – DORM 3 – fish protein certified reference material for trace metals). The standards were digested and analyzed in the same manner as the samples with each analytical run and gave results within 5% of the certified values. All presented results are averages of duplicate assays and are expressed on a tissue wet weight basis. The concentrations of Hg, Se, Cd, Pb, Cu, Zn, Mn and Fe in tissues of the six specimens analyzed are presented in Tables 1 and 2, together with previously published data for the same species from other areas. To enable comparison, data reported in dry weight was transformed to wet weight assuming 25% dry matter content (Becker et al., 1995). The comparison to other studies on same species discussed below is qualitative rather than statistically-based, because of the small number of specimens analyzed in this study.
Please cite this article in press as: Shoham-Frider, E., et al. Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.017
E. Shoham-Frider et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx
3
Fig. 2. The male calf minke whale, by-caught off Akko (a), the by-caught rough-toothed dolphin calf found off Atlit (b), the two fin whale calves, one of which drifted dead into Haifa port (c) and the other that live-stranded in Ashqelon (d) and the Risso’s dolphin female stranded off Ashdod (e).
Mercury and Selenium in baleen whales: Concentrations of Hg were low (
