International Literature Review

This Appendix presents the data from international literature on contamination of marine mammals.

Metals

Trace elements and heavy metals are common in the marine environment, especially in heavily industrialized regions. Cetaceans appear to accumulate these chemicals in their tissues, primarily through ingestion of prey, in proportion to their representation in the local environment (Johnston et al., 1996). There have been almost no specific studies of the toxicological effects of trace elements and metals on cetaceans, and most of what is known comes from inferences made from studies on humans (Johnston et al., 1996; Bowles, 1999).

Mercury

Marine mammals, particularly odontocete (toothed) cetaceans contain some of the highest concentrations known in the animal kingdom of Mercury in their livers. Indo-Pacific Humpback Dolphins from Hong Kong contain up to 906 mg kg^-1 dry weight total Mercury in their livers (Table C1-1). Concentrations in the kidneys are lower, with a maximum value of 35.8 mg kg^-1 (Parsons 1999). Several other species of cetaceans from elsewhere in the world contain similar or higher concentrations of liver Mercury. The highest concentration from the recent scientific literature is 13,270 mg kg^-1 in liver of a bottlenose dolphin, Tursiops truncatus, from Italy (Nigro and Leonzio, 1996). Finless porpoises Neophocaena phocaenoides, from Hong Kong and the adjacent East China Sea also contain elevated concentrations of Mercury in their livers, though not as high as in Indo-Pacific Humpback Dolphins.

Table C1-1 Concentration ranges of total Mercury in liver of cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Mercury	Reference
Sousa chinensis	Hong Kong	<0.36 - 906	Parsons, 1999
Sousa chinensis	Hong Kong	<0.01 – 630	Jefferson, 1998
Neophocaena phocaenoides	Hong Kong	<0.37 – 385	Parsons, 1999
Neophocaena phocaenoides	E. China Sea	0.21 – 33.4	Zhou et al 1994
Tursiops truncatus	Australia	0.48 – 35.1	Kemper et al 1994
Tursiops truncatus	Italy	13,270	Nigro & Leonzio, 1996
Tursiops truncatus	South Carolina	<1.7 – 505	Beck et al 1997
Tursiops truncatus	Great Britain	38.0 – 93.0	Law et al 1992
Tursiops truncatus	Texas	8.3 – 1404	Meador et al 1999
Tursiops truncatus	Florida	18.0 – 1312	Meador et al 1999
Tursiops truncatus	Florida	<0.03 – 1528	Rawson et al 1993
Tursiops truncatus	Irish Sea	69 – 72	Law et al 1992
Grampus griseus	Italy	3828	Nigro & Leonzio, 1996
Stenella coeruleoalba	Italy	592	Monaci et al 1998
Stenella coeruleoalba	Spain	1043	Monaci et al 1998
Stenella coeruleoalba	Mediterranean	1.20 – 1544	Andre et al 1991
Stenella coeruleoalba	Atlantic	1.20 – 87.0	Andre et al 1991
Stenella coeruleoalba	Irish Sea	19.7 – 38.0	Law et al 1992
Delphinus delphis	Irish Sea	1.7 – 228	Law et al 1992
Delphinus delphis	Australia	114 – 249	Kemper et al 1994
Lagenorhynchus albirostris	Irish Sea	93	Law et al 1992
Lagenorhynchus acutus	Cape Cod Bay, MA	3.45 – 49.7	Mackey et al 1995
Monodon monoceros	E. Canadian Arctic	1.1 – 128	Wagemann et al 1998
Phocoena phocoena	North Sea	0.6 – 449	Siebert et al 1999
Phocoena phocoena	Norway	2.9 – 18.7	Teigen et al 1993
Phocoena phocoena	Great Britain	2.1 – 518	Law et al 1992
Phocoena phocoena	Irish Sea	1.7 – 656	Law et al 1992
Phocoena phocoena	Gulf of Maine	1.93 – 53.1	Mackey et al 1995
Delphinapterus leucas	W. Canadian Arctic	1.1 – 402	Wagemann et al 1998
Delphinapterus leucas	E. Canadian Arctic	4.3 – 133	Wagemann et al 1998
Delphinapterus leucas	St Lawrence R.	1.42 – 756	Béland et al 1993
Delphinapterus leucas	Alaska	4.8 – 252	Mackey et al 1995
Delphinapterus leucas	Point Hope, AK	4.8 – 35.2	Becker et al 1995
Delphinapterus leucas	Point Lay, AK	61.0 – 252	Becker et al 1995
Delphinapterus leucas	Massachusetts	3.6 – 386	Becker et al 1995
Globicephala melas	Massachusetts	1.9 – 626	Meador et al 1993
Globicephala melas	Feroe Islands	7.8 – 557	Schintu et al 1992
Globicephala melas	Feroe Islands	50.4 – 735	Caurant et al 1996
Globicephala melas	Massachusetts	3.6 – 386	Mackey et al 1995
Orcinus orca	Great Britain	304	Law et al 1997
Mesoplodon densirostris	Great Britain	856	Law et al 1997
Physeter macrocephalus	S. North Sea	8.7 – 132	Holsbeek et al 1999
Physeter macrocephalus	S. North Sea	108	Law et al 1996
Balaena mysticetus	Alaska	0.09 – 1.0	Mackey et al 1996
Balaena mysticetus	Alaska	0.09 – 0.42	Krone et al 1999
Balaenoptera acutorostrata	Irish Sea	6.2	Law et al 1992
Balaenoptera physalus	Spain	0.56 – 5.4	Sanpera et al 1993
Balaenoptera physalus	Iceland	1.4 – 2.9	Sanpera et al 1993
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Parsons (1999) concluded that concentrations of Mercury in the liver of some individual Indo-Pacific Humpback Dolphins from Hong Kong were high enough to represent a poisoning threat to the dolphins. Odontocete cetaceans are able to detoxify Mercury in their livers. Most of the Mercury in their food is methylmerury, which is absorbed efficiently from food (Nichols et al 1999). In the liver, methylmercury is demethylated and reacted with selenium to form an insoluble mercury-selenium complex (Palmisano et al 1995; Nigro and Leonzio, 1996).

Dense concretions and sometimes associated liver disease have been observed in livers of bottlenose dolphins, Tursiops truncatus (Rawson et al 1993). These lesions were associated with liver total Mercury concentrations higher than 61 mg kg^-1 wet wt (210 mg kg^-1 dry wt). Siebert et al (1999) reported a statistical correlation between Mercury concentrations in livers of cetaceans from the North and Baltic Seas and the severity of pathological lesions, mostly associated with nutritional state.

Mercury may cause systemic toxicity when it is accumulated to concentrations that exceed the mercury-complexing capacity of the liver and kidney. This information indicates that the Indo-Pacific Humpback Dolphins in Hong Kong may be potentially at risk of harm from bioaccumulated mercury in marine prey species. However, it should be noted that the concentrations reported in this Study from the data review of prey species were low and either close to or below analytical detection limits.

Arsenic

Concentrations of Arsenic are low (compared to concentrations in potential prey) in liver and kidney of most cetaceans, including Indo-Pacific Humpback Dolphins. The highest concentration of Arsenic measured in Indo-Pacific Humpback Dolphin liver is 12.9 mg kg^-1 dry wt (Table C1-2). The highest Arsenic concentration measured in other cetaceans was in the liver of a narwal, Monodon monoceros, from Greenland (49 mg kg^-1) (Dietz et al 1996). Concentrations of Arsenic in cetacean tissues usually are lower than those in their prey (Neff, 1997; Parsons, 1997). Most of the Arsenic in dolphin prey is in organic forms, particularly arsenobetaine, which is excreted unmetabolized in the urine by most mammals.

Table C1-2 Concentration ranges of Arsenic in liver of cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Arsenic	Reference
Sousa chinensis	Hong Kong	<0.36 - 12.94	Parsons, 1999
Neophocaena phocaenoides	Hong Kong	<0.76 – 40.25	Parsons, 1999
Tursiops truncatus	Texas	1.6 – 2.0	Meador et al 1999
Tursiops truncatus	Florida	1.7 – 3.1	Meador et al 1999
Tursiops truncatus	S. Carolina	<0.34 – 5.5	Beck et al 1997
Lagerorhynchus acutus	Cape Cod Bay	0.62 – 1.43	Mackey et al 1995
Phocoena phocoena	Gulf of Maine	0.63 – 2.0	Mackey et al 1995
Phocoena phocoena	Gulf of Maine	1.76 – 2.38	Tilbuty et al 1997
Globicephala melas	Massachusetts	1.3 – 2.6	Meador et al 1993
Globicephala melas	Massachusetts	0.11 – 4.0	Mackey et al 1995
Delphinapterus leucas	Greenland	2.9 – 9.3	Dietz et al 1996
Monodon monoceros	Greenland	0.14 – 49.0	Dietz et al 1996
Orcinus orca	Great Britain	2.14	Law et al 1997
Mesoplodon densirostris	Great Britain	8.62	Law et al 1997
Balaena mysticetus	Alaska	0.75 – 1.79	Krone et al 1999
Balaenoptera acutorostrata	Greenland	2.9	Dietz et al 1996
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Cadmium

Cadmium may accumulate to high concentrations in liver and kidney of cetaceans (Tables C1-3 and C1-4). Cadmium concentrations in liver and kidney of Indo-Pacific Humpback Dolphins from Hong Kong are in the lower part of the range reported for several other species of cetaceans from throughout the world. Caurant and Amiard-Triquet (1995) could find no correlation between elevated Cadmium concentrations in liver, kidney, and blood of pilot whales, Globicephala melas, and any pathological conditions. They concluded that the whales had a remarkable tolerance to Cadmium in their diet. Much of the Cadmium in tissues of cetaceans seems to be derived from consumption of cephalopods, many species of which contain very high concentrations of Cadmium.

Table C1-3 Concentration ranges of Cadmium in liver of cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Cadmium	Reference
Sousa chinensis	Hong Kong	<0.36 - 23.17	Parsons, 1999
Neophocaena phocaenoides	Hong Kong	<0.37 – 2.86	Parsons, 1999
Neophocaena phocaenoides	E. China Sea	ND – 21.5	Zhou et al 1994
Tursiops truncatus	Texas	0.03 – 0.7	Meador et al 1999
Tursiops truncatus	Texas	0.03 – 4.62	Kuehl & Haebler, 1995
Tursiops truncatus	Florida	1.6	Meador et al 1999
Tursiops truncatus	S. Carolina	<0.34 – 5.5	Beck et al 1997
Tursiops truncatus	Australia	ND – 34.5	Kemper et al 1994
Delphinus delphis	Australia	ND – 38.0	Kemper et al 1994
Phocoena phocoena	Gulf of Maine	<0.17 – 1.77	Mackey et al 1997
Phocoena phocoena	Gulf of Maine	0.23 – 1.04	Tilbury et al 1997
Lagerorhynchus acutus	Cape Cod Bay	0.84 – 27.8	Mackey et al 1995
Orcinus orca	Great Britain	12.8	Law et al 1997
Mesoplodon densirostris	Great Britain	21.4	Law et al 1997
Globicephala melas	Massachusetts	1.3 – 2.6	Meador et al 1993
Globicephala melas	Massachusetts	9.6 – 49.3	Mackey et al 1995
Monodon monoceros	E. Canadian Arctic	7.62 – 473	Wagemann et al 1996
Delphinapterus leucas	Greenland	2.9 – 9.3	Dietz et al 1996
Delphinapterus leucas	Canadian Arctic	0.03 – 97	Béland et al 1993
Delphinapterus leucas	Hudson Bay	3.47 – 39.6	Béland et al 1993
Delphinapterus leucas	St. Lawrence R.	<0.005 – 1.5	Béland et al 1993
Monodon monoceros	Greenland	0.14 – 49.0	Dietz et al 1996
Balaena mysticetus	Alaska	0.75 – 1.79	Krone et al 1999
Balaenoptera acutorostrata	Greenland	2.9	Dietz et al 1996
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Table C1-4 Concentration ranges of Cadmium in kidney of cetaceans throughout the world compared to concentrations in kidneys of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Cadmium	Reference
Sousa chinensis	Hong Kong	<0.7 - 84.10	Parsons, 1999
Neophocaena phocaenoides	Hong Kong	<0.63 – 19.57	Parsons, 1999
Neophocaena phocaenoides	E. China Sea	0.05 – 81.4	Zhou et al 1994
Tursiops truncatus	Texas	1.1 – 4.2	Meador et al 1999
Tursiops truncatus	Florida	1.0 – 5.2	Meador et al 1999
Tursiops truncatus	Florida	ND – 6.4	Wood & van Vleet, 1996
Tursiops truncatus	Australia	ND – 122	Kemper et al 1994
Delphinus delphis	Australia	ND – 155	Kemper et al 1994
Stenella coeruleoalba	Italy	27.51	Monaci et al 1998
Stenella coeruleoalba	Spain	8.38	Monaci et al 1998
Globicephala melas	Massachusetts	119 – 425	Meador et al 1993
Platanista gangetica	Ganges River	<0.04 – 6.4	Kannan et al 1993a
Monodon monoceros	E. Canadian Arctic	3.63 – 803	Wagemann et al 1996
Delphinapterus leucas	W. Canadian Arctic	3.01 – 109	Wagemann et al 1996
Delphinapterus leucas	E. Canadian Arctic	0.36 – 375	Wagemann et al 1996
Delphinapterus leucas	St. Lawrence R.	0.005 – 18.5	Wagemann et al 1996
Physeter macrocephalus	S. North Sea	133 – 426	Holsbeek et al 1999
Balaenoptera physalus	Spain	3.97 – 92.64	Sanpera et al 1996
Balaenoptera physalus	Iceland	20.1 – 209	Sanpera et al 1996
Note: Wet wt values were converted to dry wt by multiplying by 4.78 (Siebert et al 1999).

Chromium, Copper and Nickel

Concentrations of Chromium, Copper, and Nickel in liver and kidney of Indo-Pacific Humpback Dolphins is in the lower to middle part of the range reported in the same tissues of other species of cetaceans world-wide (Parsons, 1999). Copper (an essential micronutrient) may reach 30 mg kg^-1 dry wt in the liver and kidneys of Indo-Pacific Humpback Dolphins from Hong Kong. Chromium and Nickel concentrations are below 1 mg kg^-1 dry wt. These concentrations are unlikely to be toxic to the dolphins.

Lead

Concentrations of Lead up to about 9 mg kg^-1 dry wt have been measured in the liver of Indo-Pacific Humpback Dolphins from Hong Kong (Parsons 1999). This concentration is in the higher part of the range of concentrations reported for Lead in livers of other species of cetaceans from throughout the world (Table C1-5).

Table C1-5 Concentration ranges of Lead in liver of cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Lead	Reference
Sousa chinensis	Hong Kong	<0.36 - 8.95	Parsons, 1999
Neophocaena phocaenoides	Hong Kong	<0.67 – 13.33	Parsons, 1999
Neophocaena phocaenoides	E. China Sea	0.38 – 3.0	Zhou et al 1994
Tursiops truncatus	Texas	0.12 – 2.6	Meador et al 1999
Tursiops truncatus	Texas	0.14 – 7.45	Kuehl & Haebler, 1995
Tursiops truncatus	Florida	0.14 – 0.20	Meador et al 1999
Tursiops truncatus	S. Carolina	<0.34	Beck et al 1997
Tursiops truncatus	Great Britain	<2.1 – 13.1	Law et al 1992
Tursiops truncatus	Australia	0.17 – 3.45	Kemper et al 1994
Delphinus delphis	Australia	ND – 10.3	Kemper et al 1994
Platanista gangetica	Ganges River	<0.7 – 1.7	Kannan et al 1993a
Phocoena phocoena	Great Britain	<2.1 – 14.6	Law et al 1992
Phocoena phocoena	Gulf of Maine	0.014 – 0.13	Tilbury et al 1997
Orcinus orca	Great Britain	<0.07	Law et al 1997
Mesoplodon densirostris	Great Britain	0.17	Law et al 1997
Monodon monoceros	E. Canadian Arctic	0.002 – 0.26	Wagemann et al 1996
Delphinapterus leucas	Canadian Arctic	<0.001 – 1.16	Béland et al 1993
Delphinapterus leucas	Hudson Bay	0.039 – 0.60	Béland et al 1993
Delphinapterus leucas	St. Lawrence R.	0.004 – 2.13	Béland et al 1993
Globicephala melas	Massachusetts	0.05 – 0.91	Meador et al 1993
Globicephala melas	Massachusetts	3.9 – 13.3	Mackey et al 1995
Physeter macrocephalus	S. North Sea	<1.0 – 2.2	Holsbeek et al 1999
Physeter macrocephalus	S. North Sea	0.38	Law et al 1996
Balaena mysticetus	Alaska	0.12 – 0.14	Krone et al 1999
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Zinc

Concentrations of Zinc often are quite high in soft tissues of marine animals, including dolphin prey. Concentrations of Zinc up to 243 mg kg^-1 dry wt are present in the liver and kidney of Indo-Pacific Humpback Dolphins from Hong Kong (Parsons 1999), which is in the middle of the range reported for several other species of cetaceans throughout the world (Table C1-6). Zinc is an essential micronutrient and Law et al (1992) suggested that common porpoises, Phocoena phocoena, regulate Zinc concentration in their liver in the range of 70 to 340 mg kg^-1 dry wt.

Table C1-6 Concentration ranges of Zinc in liver of cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 dry wt.

Species	Location	Total Zinc	Reference
Sousa chinensis	Hong Kong	24.13 - 243	Parsons, 1999
Neophocaena phocaenoides	Hong Kong	40.55 – 476	Parsons, 1999
Neophocaena phocaenoides	E. China Sea	110 – 365	Zhou et al 1994
Tursiops truncatus	Texas	80 – 748	Meador et al 1999
Tursiops truncatus	Florida	97.0 – 167	Meador et al 1999
Tursiops truncatus	S. Carolina	30.4 – 935	Beck et al 1997
Tursiops truncatus	Great Britain	2.24 – 89.7	Law et al 1992
Tursiops truncatus	Florida	79.7 – 722	Wood & van Vleet, 1996
Stenella coeruleoalba	Italy	111	Monaci et al 1998
Stenella coeruleoalba	Spain	162	Monaci et al 1998
Lagerorhynchus acutus	Cape Cod Bay	106 – 180	Mackey et al 1995
Platanista gangetica	Ganges River	64.0 – 210	Kannan et al 1993a
Phocoena phocoena	Great Britain	86.2 – 483	Law et al 1992
Phocoena phocoena	Gulf of Maine	87.3 – 132	Mackey et al 1995
Orcinus orca	Great Britain	166	Law et al 1997
Mesoplodon densirostris	Great Britain	141	Law et al 1997
Monodon monoceros	Canadian Arctic	79.4 – 442	Wagemann et al 1996
Delphinapterus leucas	W. Canadian Arctic	37.3 – 159	Wagemann et al 1996
Delphinapterus leucas	E. Canadian Arctic	31.5 – 312	Wagemann et al 1996
Globicephala melas	Massachusetts	97.6 – 176	Mackey et al 1995
Physeter macrocephalus	S. North Sea	90 – 125	Holsbeek et al 1999
Physeter macrocephalus	S. North Sea	117	Law et al 1996
Balaena mysticetus	Alaska	88.0 – 261	Krone et al 1999
Balaenoptera physalus	Spain	68.6 – 209	Sanpera et al 1996
Balaenoptera physalus	Iceland	59.1 – 198	Sanpera et al 1996
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Silver

Jefferson (1998) stated that Silver was analyzed in tissue samples of 13 stranded Indo-Pacific Humpback Dolphins, but presented no concentration data. There are few data available on concentrations of Silver in cetacean tissues. Becker et al (1995) reported Silver concentrations of 0.1 to 0.99 mg kg^-1 dry wt in the livers of eight pilot whales, Globicephala melas, stranded in Massachusetts. Livers of 15 beluga whales, Delphinapterus leucas, from Alaska contained 20.5 to 371 mg kg^-1 dry wt Silver. Six harbour porpoises, Phocoena phocoena from the US northeast coast contained an average of about 1.7 mg kg^-1 Silver in their livers. Livers of baleen whales contain much lower concentrations of Silver than livers of toothed cetaceans (Becker et al 1995). Ionic Silver is highly reactive and toxic to marine organisms. However, the high concentrations in cetacean liver appear to be complexed with selenium in an inert, non-toxic form (Becker et al 1995). However, like Mercury which is sequestered by the same mechanism in cetacean liver, it is possible that Silver may become toxic if it is accumulated to concentrations higher than the complexation capacity of the cetacean liver.

Organics

Polychlorinated biphenyls (PCBs) are industrial chlorinated organic chemicals that have become widely disseminated in the marine environment. They are highly bioaccumulative and tend to biomagnify in marine food webs. Odontocete cetaceans being the top consumers in many marine food webs, often contain high concentrations of PCBs in their soft tissues, particularly the liver and blubber (Table C1-7). Because these highly hydrophobic chemicals selectively accumulate in tissue lipids, their concentrations usually are normalized to lipid weight. Blubber of Indo-Pacific Humpback Dolphins contains 0.19 to 155 mg kg^-1 lipid wt total PCBs (Minh et al 1999; Parsons 1999). There are many reports of higher concentrations in blubber of other species, particularly from the Mediterranean Sea and St. Lawrence River estuary (Table C1-8). Highest concentrations in blubber are above 2000 mg kg^-1 dry wt.

Table C1-7 Concentration ranges of total polychlorinated biphenyls (PCBs) in blubber of odontocete (toothed) cetaceans throughout the world compared to concentrations in blubber of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 lipid weight.

Species	Location	Total PCBs	Reference
Sousa chinensis	Hong Kong	0.19 – 125	Parsons, 1997
Sousa chinensis	Hong Kong	6.1 – 155	Minh et al 1999
Sousa chinensis	Bay of Bengal	7.7 – 9.6	Prudente et al 1997
Neophocaena phocaenoides	Hong Kong	0.47 – 17.4	Parsons, 1997
Tursiops truncatus	Maryland	195	Kuehl et al 1991
Tursiops truncatus	Texas	0.8 – 187	Kuehl & Haebler, 1995
Tursiops truncatus	Italy	230 – 2100	Corsolini et al 1995
Tursiops truncatus	California	0.28 – 30.0	Reddy et al 1998
Tursiops truncatus	Italy	0.25 – 175	Marsili et al, 1997
Stenella coeruleoalba	W. Mediterranean	210 – 2600	Kannan et al 1993b
Stenella coeruleoalba	Italy	9.3 – 996	Marsili et al, 1997
Stenella coeruleoalba	Japan	42.6 – 80.3	Prudente et al 1997
Stenella longirostris	Philippines	10.0 – 14.6	Prudente et al 1997
Stenella longirostris	Bay of Bengal	1.28 – 3.33	Prudente et al 1997
Stenella longirostris	Tropical Pacific	0.61 – 2.4	Prudente et al 1997
Lagenorhynchus acutus	Faroe Islands	25.3 – 42.68	Borrell, 1993
Grampus griseus	Italy	42 – 1000	Corsolini et al 1995
Grampus griseus	Italy	676	Marsili et al, 1997
Grampus griseus	Japan	86.4 – 148	Prudente et al 1997
Steno bredanensis	Italy	81.7	Marsili et al, 1997
Lissodelphis borealis	N. Pacific Ocean	34.1 – 53.4	Prudente et al 1997
Lagenorhynchus obliquidens	N. Pacific Ocean	21.6 – 28.4	Prudente et al 1997
Delphinus delphis	N. Pacific Ocean	25.7 – 33.8	Prudente et al 1997
Lagenodelphis hosei	Japan	46.9 – 93.8	Prudente et al 1997
Lagenodelphis hosei	Philippines	10.6	Prudente et al 1997
Phocoena phocoena	Great Britain	0.13 – 90	Kuiken et al 1993
Phocoena phocoena	Faroe Islands	8.83 – 13.39	Borrell, 1993
Phocoena phocoena	Netherlands	2.13 – 63.61	van Scheppingen et al 1996
Phocoena phocoena	Denmark	1.56 – 52.0	Granby & Kinze, 1991
Phocoenoides dalli	N. Pacific Ocean	9.6 – 33.8	Prudente et al 1997
Delphinapterus leucas	Point Lay, Alaska	0.70 – 9.42	Wade et al 1997
Delphinapterus leucas	N. Canada	0.96 – 5.58	Norstrom & Muir, 1994
Delphinapterus leucas	St. Lawrence R.	17.4 – 103	Béland et al 1993
Delphinapterus leucas	St. Lawrence R	8.33 – 412	Muir et al 1996
Delphinapterus leucas	St. Lawrence R	7.69 – 49.1	Gauthier et al 1998
Delphinapterus leucas	Chukchi Sea, Alaska	1.52 – 3.87	Schantz et al 1993
Delphinapterus leucas	Newfoundland	2.14 – 3.73	Muir et al 1996
Globicephala melas	Faroe Islands	26.27 – 48.81	Borrell, 1993
Globicephala melas	Italy	137	Marsili et al, 1997
Globicephala melas	Massachusetts	7.55	Weisbrod et al 1999
Berardius bairdii	Japan	12.5 – 18.8	Prudente et al 1997
Peponocephala electra	Japan	83.6 – 90.2	Prudente et al 1997
Physeter macrocephalus	Iceland	10.51	Borrell, 1993
Physeter macrocephalus	North Sea	0.31 – 21.2	Wells et al 1997
Note: Wet wt values were converted to lipid wt by dividing by the fraction lipid in the blubber.

Concentrations of total DDT (the pesticide DDT and its primary degradation products, including DDE) also are high in blubber of cetaceans from many parts of the world, including Indo-Pacific Humpback Dolphins from Hong Kong (Table C1-8). Indo-Pacific Humpback Dolphin blubber contains 1 to 380 mg kg^-1 dry wt total DDT (Minh et al 1999; Parsons 1999). Highest concentrations of total DDT in other species are above 1000 mg kg^-1 dry wt. Blubber of Indo-Pacific Humpback Dolphins also contains several orther chlorinated pesticides, including hexachlorocyclohexanes (0.009 to 6.9 mg kg^-1 lipid), chlorobenzenes (0.04 to 1.8 mg kg^-1 lipid) , chlordanes (0.01 to 24.9 mg kg^-1 lipid), lindane (0.04 to 5.8 mg kg^-1 lipid), dieldrin (0.07 to 2.3 mg kg^-1 lipid), and mirex (0.01 to 2.0 mg kg^-1 lipid) (Parsons, 1997; Minh et al 1999). Concentrations of these pesticides, although lower than those of total DDTs in dolphin blubber, are high enough to possibly contribute to systemic toxic effects of total organochlorines in the dolphin tissues.

Table C1-8 Concentration ranges of total DDT in blubber of odontocete (toothed) cetaceans throughout the world compared to concentrations in livers of Indo-Pacific Humpback Dolphins (Sousa chinensis). Concentrations are mg kg^-1 lipid weight.

Species	Location	Total DDT	Reference
Sousa chinensis	Hong Kong	1.0 – 381	Parsons, 1997
Sousa chinensis	Hong Kong	9.4 – 203	Minh et al 1999
Sousa chinensis	Bay of Bengal	78.8 – 121	Prudente et al 1997
Neophocaena phocaenoides	Hong Kong	22.57 – 309.4	Parsons, 1997
Tursiops truncatus	Italy	48 – 1100	Corsolini et al 1995
Tursiops truncatus	Italy	0.64 – 57.6	Marsili et al, 1997
Tursiops truncatus	Texas	0.37 – 80	Kuehl & Haebler, 1995
Tursiops truncatus	California	0.75 – 245	Reddy et al 1998
Stenella coeruleoalba	W. Mediterranean	62 – 1200	Kannan et al 1993b
Stenella coeruleoalba	Italy	6.0 – 858	Marsili et al, 1997
Stenella coeruleoalba	Japan	49.2 – 78.7	Prudente et al 1997
Stenella longirostris	Philippines	48.4 – 88.7	Prudente et al 1997
Stenella longirostris	Bay of Bengal	26.7 – 55.0	Prudente et al 1997
Stenella longirostris	Tropical Pacific	1.9 – 4.8	Prudente et al 1997
Lagenorhynchus acutus	Faroe Islands	15.0 – 22.5	Borrell, 1993
Grampus griseus	Italy	11 – 670	Corsolini et al 1995
Grampus griseus	Italy	428	Marsili et al, 1997
Grampus griseus	Japan	10.2 – 59.1	Prudente et al 1997
Steno bredanensis	Italy	24.4	Marsili et al, 1997
Lissodelphis borealis	N. Pacific Ocean	90.9 – 109	Prudente et al 1997
Lagenorhynchus obliquidens	N. Pacific Ocean	19.3 – 29.5	Prudente et al 1997
Delphinus delphis	N. Pacific Ocean	21.6 – 48.6	Prudente et al 1997
Lagenodelphis hosei	Japan	46.9 – 77.8	Prudente et al 1997
Lagenodelphis hosei	Philippines	50.7	Prudente et al 1997
Phocoena phocoena	North Sea	10.22	Beck et al 1990
Phocoena phocoena	Faroe Islands	3.78 – 5.57	Borrell, 1993
Phocoena phocoena	Denmark	0.73 – 52.6	Granby & Kinze, 1991
Phocoenoides dalli	N. Pacific Ocean	8.4 – 73.3	Prudente et al 1997
Delphinapterus leucas	Point Lay, AK	0.32 – 6.83	Wade et al 1997
Delphinapterus leucas	N. Canada	0.67 – 6.83	Norstrom & Muir, 1994
Delphinapterus leucas	St. Lawrence R.	4.75 – 142	Béland et al 1993
Delphinapterus leucas	St. Lawrence R.	3.36 – 389	Muir et al 1996
Delphinapterus leucas	St. Lawrence R.	2.23 – 67.4	Gauthier et al 1998
Delphinapterus leucas	Chukchi Sea, AK	1.68 – 4.65	Schantz et al 1993
Delphinapterus leucas	Newfoundland	1.46 – 2.80	Muir et al 1996
Globicephala melas	Massachusetts	18.34	Weisbrod et al 1999
Globicephala melas	Italy	63.9	Marsili et al, 1997
Globicephala melas	Faroe Islands	6.4 – 33.6	Borrell et al 1995
Berardius bairdii	Japan	10.6 – 21.9	Prudente et al 1997
Peponocephala electra	Japan	82.0 – 107	Prudente et al 1997
Physeter macrocephalus	Iceland	7.8	Borrell, 1993
Physeter macrocephalus	North Sea	1.18 – 15.5	Wells et al 1997
Note: Wet wt values were converted to lipid wt by dividing by the fraction lipid in the blubber.

There has been considerable concern and speculation about whether high concentrations of organochlorines in cetacean blubber are harming the cetaceans. These and related organochlorine compounds may decrease immunity, affect hormone levels, interfere with reproduction and development, and contribute to a wide variety of pathological conditions in cetaceans (Addison 1989; Kannan et al 1989; Reijners 1994). Beluga whales, Delphinapterus leucas, from the St. Lawrence River estuary suffer from a wide variety of pathological conditions including viral and bacterial infections and cancers. These diseases have been attributed to immunosuppression caused by accumulated organochlorines, particularly PCBs and DDT (Béland et al 1993; Martineau et al 1994; De Guise et al 1995). Accumulated organochlorines were correlated with alterations in lipid metabolism in striped dolphins, Stenella coeruleoalba (Kawai et al 1988). There was an inverse correlation between concentrations of DDE in blubber in Dall’s porpoises, Phocoenoides dalli, from the North Pacific Ocean and concentrations of the male sex hormone, testosterone, in the blood (Subramanian et al 1987). Concentrations of DDE in blubber of about 50 mg kg^-1 dry wt seemed to be associated with hormonal suppression. Hormonal suppression may be associated with induction of liver mixed function oxygenase enzymes by the accumulated organochlorines (Tanabe et al 1994), and may contribute to reproductive impairment (Reijnders 1980, 1986).

Organotins

Organotins, particularly tributyltin (TBT) have been used widely in antifouling coatings on submerged marine structures, including boats. Butyltin concentrations often are high in sediments from coastal and estuarine waters supporting boating and shipping activities. In a study conducted in 1994, sediments from the vicinity of eight shipyards and six marinas in Hong Kong contained a mean of about 0.5 mg kg^-1 dry wt total organotins, with a maximum concentration of 53 mg kg^-1 (Ko et al 1995). Because butyltins are extremely toxic to marine organisms, many of their uses have been banned in most parts of the world (Cardwell et al 1999). Tributyltin degrades in the environment to dibutyltin and finally monobutyltin, both of which are less toxic than tributyltin. These butyltins are highly bioaccumulative in tissues of marine animals, particularly the liver (Kannan et al 1995). Butyltin concentrations have been measured in the livers of several species of odontocete cetaceans, mostly from the northwestern North Pacific (Table C1-9). No data are available on butyltin concentrations in the liver of Indo-Pacific Humpback Dolphins from Hong Kong. However, Sousa chinensis from the Bay of Bengal, India, contained 0.23 to 0.69 mg kg^-1 dry wt total butyltins in their livers (Tanabe et al 1998). Liver of Indo-Pacific Humpback Dolphins from Hong Kong did contain total tin (Sn) at concentrations ranging from below the method detection limit to 8.9 mg kg^-1 dry wt (Porter et al 1997). Dolphin kidney contained a similar concentration, but the tin concentration in blubber was lower. Finless porpoises, Neophocaena phocaenoides, from Japan and coastal China (near Hong Kong) contain 1.2 to 34 mg kg^-1 dry wt butyltins (Tanabe et al 1998). Livers of rough-toothed dolphins, Steno bredanensis, from ocean waters east of Japan contained 0.06 to 0.13 mg kg^-1 dry wt total butyltins (Tanabe et al 1998). It is not known what concentrations of butyltins in cetacean liver and kidney are associated with systemic toxicity.

Table C1-9 Concentration ranges of total butyltins in liver of odontocete (toothed cetaceans throughout the world. Concentrations are mg kg^-1 dry wt.

Species	Location	Total Butyltins	Reference
Tursiops truncatus	Italy	4.14 – 7.59	Kannan et al 1996
Phocaenoides dalli	NW Pacific	0.14 – 0.62	Tanabe et al 1998
Phocaenoides dalli	Japan	1.07 – 3.45	Tanabe et al 1998
Mesoplodon stejnegeri	Japan	1.38	Tanabe et al 1998
Mesoplodon ginkgodens	Japan	1.14	Tanabe et al 1998
Berardius bairdii	Japan	0.38 – 1.07	Tanabe et al 1998
Globicephala macrorhynchus	Japan	5.18 – 8.97	Tanabe et al 1998
Tursiops truncatus	Japan	8.97 – 10.35	Tanabe et al 1998
Steno bredanensis	Japan	11.38	Tanabe et al 1998
Orcinus orca	Japan	7.59 – 9.32	Tanabe et al 1998
Kogia simus	Japan	2.52	Tanabe et al 1998
Kogia breviceps	Japan	0.79	Tanabe et al 1998
Neophocaena phocaenoides	Japan	3.80 – 34.5	Tanabe et al 1998
Neophocaena phocaenoides	China	1.21 – 4.14	Tanabe et al 1998
Stenella longirostris	Philippines	0.14 – 0.23	Tanabe et al 1998
Lagenodelphis hosei	Philippines	0.31 – 0.34	Tanabe et al 1998
Steno bredanensis	W Pacific	006 – 0.13	Tanabe et al 1998
Sousa chinensis	Bay of Bengal	0.23 – 0.69	Tanabe et al 1998
Stenella longirostris	Bay of Bengal	0.23 – 0.45	Tanabe et al 1998
Tursiops truncatus	Bay of Bengal	0.18 – 0.54	Tanabe et al 1998
Grampus griseus	Japan	1.90 – 20.70	Kim et al 1996
Note: Wet wt values were converted to dry wt by multiplying by 3.45 (Siebert et al 1999).

Literature Summary of Indo-Pacific Humpback Dolphins in Hong Kong

Heavy metals have been analyzed for Indo-Pacific Humpback Dolphins only from Hong Kong (Parsons 1999; Jefferson 2000) and Xiamen (Huang et al. 1999). In both study areas, dolphin tissues contained higher levels of mercury than did their prey species (Huang et al. 1999; Parsons 1999), which indicates that biomagnification is occurring. This finding is not surprising as mercury is known to biomagnify in species high up the food chain. Although arsenic levels have not been identified from studies in Hong Kong as one of the metals of highest concern (see Parsons 1999; Jefferson 2000).

Significantly more work has been done on organochlorines and their effects on cetaceans. Organic chemicals (including PCBs, hydrocarbons, and pesticides such as DDT) are known to be a potential threat to cetaceans, because they bioaccumulate in top predators, and are passed from generation to generation. Also, due to the absence or reduction of certain enzymes, cetaceans have a low capacity to metabolize (and thus detoxify) these compounds (Tanabe et al., 1994).

Organochlorines have been reported to interfere with reproductive capacity, cause immunosuppression (lowered resistance to disease), and have carcinogenic (cancer-causing) and teratogenic (development) effects (Tanabe & Tatsukawa, 1991; Busbee et al., 1999). Exposure during early development can affect the endocrine, reproductive, immune, and nervous systems, sometimes not expressing its effects until adulthood. For instance, it has been found that high concentrations of PCBs and DDE were correlated with lowered testosterone levels in the blood of Dall's porpoises (Phocoenoides dalli) in the North Pacific (Subramanian et al., 1987). In another study, Martineau et al. (1988) found that industrial contaminants were associated with lesions and cancer-like tumours in beluga whales (Delphinapterus leucas) in the St. Lawrence Estuary. Many of these were implicated in the animals' death. Clear evidence showed that high levels of organochlorines suppressed the immune response of bottlenose dolphins in the southeastern USA (Lahvis et al., 1995). Cockcroft (1989) suggested that OC concentrations in South Africa may be high enough to impair reproductive function of male humpback dolphins, and to prove fatal to neonates of primiparous females. Finally, high concentrations of OCs are suspected to have been a causal factor in the die-offs of dolphins in the Mediterranean Sea and northeastern USA in recent years (Kannan et al., 1993b; Aguilar, 2000).

Levels of OCs have been analyzed in humpback dolphin tissues from only a few areas: South Africa (Cockcroft 1989), India (Tanabe et al. 1993, 1996; Prudente et al. 1997), and Hong Kong (Parsons and Chan 1998; Minh et al. 1999). Although sample sizes have generally been very low, concentrations of at least certain OCs appear to be a concern everywhere that they have been examined in humpback dolphin tissues.

Within Hong Kong waters, two groups of OC compounds have been identified as potentially quite high and of possible health concern: DDTs (Parsons and Chan 1998; Mihn et al. 1999) and PCBs (Minh et al. 1999). In particular, DDTs have been identified as the most serious concern, due to the very high levels in some specimens. Using a toxic equivalent approach (TEQ), Minh et al. (2000a) determined that PCBs (and their congeners) exceeded levels that have been associated with immunosuppression in harbor seals (Phoca vitulina). In fact, the TEQs for Hong Kong Indo-Pacific Humpback Dolphins were comparatively higher when compared with 14 areas/species (Minh et al. 2000c).

Another class of compounds that has caused concern in recent years is the butyltins (BTs or organotins). Butyltins have not been recognized as serious threats to marine mammals until recently. These compounds, most commonly used in anti-fouling paints applied to ship hulls in dry docks, are among the most toxic substances known to occur in the oceans. Although their serious effects on lower animals have been well documented, it is only in the last few years that researchers have even begun searching for them in cetaceans (see Tanabe et al., 1998; Tanabe, 1999). Finless porpoises in Japan were reported to have high levels of these compounds, likely representing a serious health risk (Iwata et al., 1995, 1997).

Levels of butyltins have been analyzed for humpback dolphins only from India (Tanabe et al. 1998) and Hong Kong (Takahashi et al. 2000), so there is little possibility for interspecies comparison. However, Hong Kong Indo-Pacific Humpback Dolphins contained relatively higher levels among 14 areas and marine mammal species compared by Takahashi et al. (2000).

Based on the above review, a few compounds were identified from several classes to be of particular concern when dealing with Indo-Pacific Humpback Dolphins in Hong Kong. These include DDTs and PCBs among the organochlorines; arsenic and mercury among the metals; and butyltins.

Recent Analysis of Contaminant Levels in Dolphin Tissues

The analysis below examines all available data on COCs in specimens of Indo-Pacific Humpback Dolphins from Hong Kong, thereby providing the most up-to-date information currently available for assessment of ecotoxicology of these animals.

Materials and Methods

Sample and Data Collection

Stranded humpback dolphin carcasses have been examined in Hong Kong since 1993 (see Parsons & Jefferson, 2001). Necropsies were performed either in the laboratory (for fresh specimens) or in the field (for those that were badly decomposed or in relatively inaccessible locations). Basic biological data and samples were collected (see Parsons & Jefferson 2001 for a detailed discussion of the stranding program and sampling procedures). Specimens were classified as to their level of decomposition, using the codes outlined in Geraci & Lounsbury (1993).

A total of 46 specimens were sampled for environmental contaminants from 1993 to 2001. Blubber samples, for organic contaminant analyses, were collected from the dorsal thoracic region, and were wrapped in aluminum foil and frozen. Samples of liver and kidney were taken for heavy metal and trace element analyses; samples were placed in plastic ziplock bags and stored in a freezer. Teeth from the middle of the lower left jaw of most specimens were also collected for age determination.

Analyses

Six groups of contaminants were examined in two types of tissue. These were total DDT pesticide residues (∑DDTs = DDE + DDT), total polychlorinated biphenyls (∑PCBs = monochlorobiphenyl + dichlorobiphenyl + trichlorobiphenyl + tetra-chlorobiphenyl + pentachlorobiphenyl + hexachlorobiphenyl + hepta-chlorobiphenyl + octachlorobiphenyl + nonachlorobiphenyl + decachlorobiphenyl), total hexa-chlorocyclohexanes (∑HCHs = alpha-HCH + beta-HCH + gamma-HCH), and total butyltins (∑BTs) in the blubber; and concentrations of the heavy metals mercury (Hg) and Selenium (Se) in the liver. This selection was based on indications from earlier studies that these contaminants were the most critical, due to high levels and in some cases high known toxicity (Parsons & Chan, 1998; Parsons, 1999; Minh et al., 1999; Tanabe, 1999). Contaminants in kidney tissue were not analyzed for this study, but the samples were archived for future analysis.

Some laboratory analyses were performed by Prof. S. Tanabe and his colleagues at Ehime University in Japan (see Minh et al. 1999, 2000a, b, c). For other specimens, frozen tissue samples were sent to a commercial ecotoxicology laboratory in Hong Kong (ALS Technichem [HK] Pty, Ltd.) for chemical analyses. For the determination of mercury levels, samples were dissected with titanium tools. The samples were then digested by a close vessel microwave digestion unit by nitric acid and hydrogen peroxide mixture prior to Inductively-Coupled Plasma Mass Spectroscopy (ICPMS) and Flow Injection Mercury Analyzer (FIMS) testing. For trace organic analysis, samples were extracted with a dichloromethane/acetone mixture and pre-cleaned by passing through a GPC column prior to analysis by GC systems.

Routine quality-control (QC) checks were run with each batch of 20 samples processed. For a QC check to have been judged acceptable, 80% of target analytes must have passed all three of the following criteria: (1) average recovery of Single Control Sample (SCS) and Duplicate Control Sample (DCS) must have fallen within the recovery control limits, (2) Relative Percent Difference for the SCS and DCS must have been < 20%, and (3) blank concentrations must have been less than the limit of reporting.

Age was estimated by decalcifying and sectioning 1-2 teeth from each specimen on a sledge-type microtome, followed by staining, and counting of growth layer groups (GLGs) in the postnatal dentine and cementum. One GLG was assumed to represent 1 year. Age data were not available for a few specimens; for these an estimate of age was made from the total length using the growth curves presented in Jefferson (2002). For more details on aging techniques, see Jefferson (2000).

Results

Organochlorine concentrations ranged from near zero to 80,000 µg/kg wet wt. (DDTs) and 50,000 µg/kg wet wt. (PCBs). The highest concentrations for both types of contaminants were in specimens less than 1 year of age (Figure C1_a). The patterns with respect to age and sex were very similar for both contaminants. In males, there was a slight increasing trend with age, while in females there was an increase until about 6-8 years of age, and then a decrease after that, followed by another increase after about 24-26 years of age (Figure C1_a). This pattern in females can be attributed to offloading of organochlorines through gestation and lactation at around sexual maturity. The increase late in life may be associated with reduced lactation as females near the end of the their reproductive lifetime.

Figure C1_a. Relationship of organochlorine concentrations with age and sex in Hong Kong humpback dolphins.

Mercury concentrations ranged from zero to about 900 mg/kg dry wt. (Figure C1_b). The age and sex-related pattern was very different than that for organochlorines. Mercury levels remained near zero until after 10 years of age, when they began to increase exponentially in both sexes (Figure C1_b).

Figure C1_b. Relationship of mercury concentrations with age and sex in Hong Kong humpback dolphins.

Temporal trends for both DDTs and PCBs showed evidence of a decrease from 1995 through 2000 (Figure C1_c). This result needs to be treated with caution, however, as different laboratories conducted the analyses at different times of the study. Therefore this result may be at least partially attributable to inter-laboratory biases.

Figure C1_c. Trend in organochlorine concentrations in dolphin tissues, 1995 through 2000.

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