Persistent organochlorine residues in small cetaceans from the east and west coasts of southern Africa

the Science of the Total Environment Sa latmue~ J*~-=~ ~ Setuemc i I , . t . B ~ Into the I~,l,Nmmmt ~ Im I 1 ~ wlllD~ l m

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The Science of the Total Environment 154 (1994) 153-162

Persistent organochlorine residues in small cetaceans from the east and west coasts of southern Africa A . C . d e K o c k *a, P . B . B e s t h, V . C o c k c r o f t c, C . B o s m a d aCatakysis Research Unit, Faculty of Applied Science, dDepartment of Mathematical Sciences, Port Elizabeth Technikon, Private Bag X6011, Port Elizabeth, 6000 South Africa bMammal Research Institute, University of Pretoria, Pretoria, South Africa Cport Elizabeth Museum, Port Elizabeth, South Africa

Abstract Organochlorine pollutant levels in the blubber of small cetaceans and ratios between concentrations of compounds, such as DDE/tDDT and tDDT/PCB, were used to identity the chronology of input of DDT and PCB into the coastal waters along the west and east coasts of southern Africa. Although regression analyses, with time as the only independent variable, do not show a statistically significant decline in tDDT from 1980 to 1987 in the common dolphin from the east coast of South Africa, there is a fairly strong indication that tDDT concentrations did not increase or even stay constant with time. tDDT concentrations in the bottlenose dolphin declined significantly from 1980 to 1987 (P < 0.05). The regression analyses for PCB in the bottlenose dolphin from the east coast show no decline (P > 0.05). The data from this study illustrate that it would take a long time in the coastal waters and open ocean before the restriction and prohibition on the production and use of organochlorines will take effect. Keywords: Marine mammals; Organochlorines; DDT; PCBs; Cetaceans

1. Introduction T h e sea is the ultimate repository of terrestrial matter, including the vast array of m a n - m a d e chemicals introduced annually. Some of these synthetic chemicals, such as the insecticide D D T , were used because of their chemical stability, persistence and toxic properties. Others, like the polychlorinated biphenyls (PCBs), have f o u n d widespread industrial applications because of their chemical inertness. T h e lipophilic organochlorine c o m p o u n d s , such as PCBs and D D T , are known

* Corresponding author.

tO accumulate in the blubber of marine m a m m a l s ( O ' S h e a et al., 1980; Gaskin, 1982; T a n a b e et al., 1983; W a g e m a n n and Muir, 1984; A b e r n o u et al., 1986; Morris et al., 1989). T h e females can also transfer the organochlorines f r o m one generation to the next t h r o u g h lactation (Tanabe et al., 1981; A d d i s o n and Brodie, 1987; Aguilar and Borrell, 1988; S u b r a m a n i a n et al., 1988; Cockcroft et al., 1989, 1990). A l t h o u g h reports suggest that some organochlorine residues are declining in some marine m a m m a l populations (Addison et al., 1984, 1986; L o g a n a t h a n et al., 1990), there is little information available on the t e m p o r a l variation of these chemicals in the coastal marine ecosystems and marine m a m m a l populations along the

0048-9697/94/$07.00 © 1994 Elsevier Science BV. All rights reserved. SSD1 0048-9697(94)4226-D

154

A.C. de Kock et aL / Sci. Total Environ. 154 (1994) 153-162

South African coast. This study is an attempt to assess the status of organochlorine concentrations in cetaceans from the east coast (Indian Ocean) and west coast (Atlantic Ocean) of southern Africa.

and the silt brought by the rivers into the sea can affect the water many kilometres offshore. 2.2. West coast specimens The blubber of beach-stranded and free-ranging individuals taken under scientific permit or incidentally captured by fishermen along the west and southwestern coast of South Africa during the period 1977-87 were used in the analysis for organochlorines. Blubber were removed from each animal from the dorsal blubber immediately anterior to the dorsal fin. Following collection, the samples were immediately wrapped in aluminium foil and stored at -20°C prior to analysis. Details of the marine mammals sampled are given in Table 1.

2. Materials and methods 2.1. Study area

South Africa is bounded by two major oceanographic systems, the intermittent and cold Benguela System situated on the west coast, and a strong southerly flowing warm Agulhas Current on the south and east coasts (Fig. 1). The western half of the African subcontinent is arid. Along the Namibian coast, dry river valleys occur with episodic flooding on time scales of several decades. The east coast of South Africa borders onto the waters of the south-west Indian Ocean. River outflow along this coast can be substantial at times. This is particularly the case in summer,

Dolphins in the coastal waters off the east coast are subjected to accidental capture in antishark nets set off bathing beaches. Blubber from

z oE

ANSOLA CURRENT (seasonaL)

-20"S

2. 3. East coast specimens

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AFRICA

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Fig. 1. Features of the large scaleocean environmentaroundsouthernAfrica.

50 °

A.C de Kock et al. / ScL Total Ent~ron. 154 (1994) 153-162

155

Table 1 Organochlorine residue levels (/zg g-1 wet mass) in the blubber of cetaceans from the west coast of South Africa (1977-1987) Species

Sample size

Year

Sex

Length (m)

tDDT

PCB

HCB

Southern right whale

2

1984

M

9.25

0.01

0.01

0.02

1

1986 1987

M F

4.85 6.5

0.01 0.05

0.01 0.12

0.01 0.01

1

1984

F

3.3

0.08

0.01

0.1

1

1986

F

16

0.39

0.13

0.01

5

1978

F

2.93

0.51

0.26

0.06

4

1984 1986 1986 1987 1976

F F M M M

3.01 3.21 2.18 2.33 1.67

0.3 1.02 1.11 0.3 1.43

0.12 1.1 0.29 0.26 0.18

0.05 0.06 0.08 0.03 0.04

6

1984 1984 1984 1984

M M M F

2.11 2.3 1.78 3.46

0.37 0.54 0.65 1.47

0.15 0.29 0.38 0.88

0.03 0.03 0.03 0.15

2

1984 1984 1984 1984 1986 1986

F M F F M F

4.54 2.25 4.54 4.25 3.76 3.19

0.29 1.86 0.38 0.36 0.39 0.91

0.3 0.29 0.51 0.27 0.26 1.22

0.02 0.16 0.03 0.03 0.02 0.09

2

1986 1978 1985

F M M

4.17 2.9 5.2

1.37 0.54 1.22

0.75 0.15 1.93

0.11 0.13 0.27

2

1984

M

3.14

7.51

2.72

0.02

2

1986 1984 1986

F F M

1.29 2.3 2.01

1.29 1.02 0.74

0.39 1.28 1.11

0.03 0.02 0.03

6

1976

M

2.69

4.14

0.34

0.03

17

1980 1984 1985 1985 1987 1984

M M M M F M

2.86 1.35 1.72 2.61 2.88 2.08

0.17 2.52 3.6 12.29 1.75 9.63

0.16 1.93 2.33 8.29 1.62 6.94

0.01 0.01 0.03 0.03 0.01 0.4

1984 1984 1984 1984 1984 1984

M M M M M F

2.22 2.3 1.97 1.49 1.55 2.15

0.48 5.73 0.07 13.69 25.25 3.02

0.43 3.39 0.07 12.27 15.51 2.61

0.02 0.02 0.02 0.16 0.18 0.04

( Eubalaena australis) Pygmy right whale

( Caperea marginata ) Minke whale

( Balaenoptera acutorostrata) Sperm whale

( Physeter macrocephalus) Pygmy sperm whale

( Kogia bret~ceps)

Dwarf sperm whale

( Kogia simus )

Blainville's beaked whale

( Mesoplodon densirostris)

True's beaked whale

( Mesoplodon mirus) Layard's beaked whale

(Mesoplodon layardi) Risso's dolphin

(Grampus grissus) Striped dolphin

(Stenella coeruleoalba) Bottlenose dolphin

( Tursiops truncatus )

Common dolphin

( Delphinus delphis )

A.C. de Kock et al. /Sci. Total Environ. 154 (1994) 153-162

156 Table 1 (Continued) Species

Heaviside's dolphin ( Cephalorhynchus hea visidii)

Median (Mean) Dusky dolphin ( Lagenorhynchus obscurus)

Sample size

Year

Sex

Length (m)

9

1986 1986 1986 1986 1986 1986 1986 1987 1987 1987 1977

M M M M F F F F F F F

1982 1984 1984 1984 1985 1985 1985 1987 12

tDDT

PCB

HCB

2.07 1.97 2.07 2.43 2.11 1.95 2.2 2.17 1.62 2.29 1.68

9.83 9.58 5.49 7.73 2.96 0.96 2.68 0.57 2.88 0.71 1.17

2.88 5.75 5.41 4.18 2.96 1.12 5.07 0.59 5.03 2.41 0.11

0.02 0.05 0.01 0.01 0.01 0.05 0.05 0.02 0.08 0.05 0.04

F M M M NA F M M

1.58 1.47 1.56 1.56 NA 1.18 1.51 1.53

1977

F

0.85

4.21 4.77 2.71 1.96 0.26 0.25 3.61 0.78 1.97 (2.17) 2.74

0.65 1.76 0.75 0.65 1.09 0.07 1.13 0.27 0.65 (0.72) 0.64

0.06 0.06 0.01 0.08 0.02 0.01 0.04 0.03 0.04 (0.04) 0.01

1977 1984 1984 1986 1986 1986 1986 1986 1987 1987 1987

M M F F F F M M F M M

1.69 1.66 1.69 1.61 1.71 1.87 1.84 0.89 1.78 1.76 0.92

16.15 13.74 1.49 1.69 1.31 1.04 8.17 0.49 5.82 2.21 1.21 2.20 (4.67)

2.29 5.59 2.37 1.17 0.56 0.76 4.24 0.38 1.71 1.58 1.89 1.71 (1.88)

0.02 0.14 0.06 0.01 0.03 0.02 0.06 0.02 0.04 0.05 0.07 0.04 (0.04)

Median (Mean) NA, not available.

a n i m a l s caught in the a n t i - s h a r k nets were analyzed for o r g a n o c h l o r i n e residues. D o l p h i n s caught in shark nets were frozen as soon as possible after c a p t u r e to await g e n e r a l dissection. B l u b b e r samples (30 g) were r e m o v e d from each animal, from the flank in the neck region a n t e dorsal-dorsal to the flipper i n s e r t i o n w h e r e the greatest b l u b b e r thickness was consistently found. T h e samples were w r a p p e d in a l u m i n i u m foil a n d i m m e d i a t e l y frozen to await analysis.

2.4. E x p e r i m e n t a l T h e p r e p a r a t i o n a n d extraction p r o c e d u r e s were as described in de Kock (1990). O n l y a b r i e f description is given here. A b o u t 5 g of b l u b b e r was g r o u n d with a n h y d r o u s s o d i u m sulphate to the consistency of a free-flowing powder. T h e mixture was extracted for 4 h in a soxhlet a p p a r a tus, with hexane as the solvent. A s u b - s a m p l e of the fat extracted was c l e a n e d up, using a l u m i n a a n d silica gel as adsorbents. A n aliquot of the

A.C. de Kock et al. / Sci. Total Entiron. 154 (1994) 153-162

cleaned up extract was injected into a Carlo Erba gas chromatograph, equipped with a cold on-column injector with secondary cooling, and a 63Ni electron capture detector (ECD). A 30-m fused silica capillary column (0.32 mm i.d.), coated with SPB5 as the liquid phase (0.22 mm), was used to separate the residue peaks. An effort was made, within reason, to ensure that peak height response of the compounds under investigation should match the peak heights from the working standards. Individual PCB congeners were not available for the analysis of the samples from the east coast. PCBs were identified by their peak characteristics and retention times in relation to a standard mixture of Aroclors 1254 and 1260 (1:1). Individual PCB congeners in cetaceans from the west coast were identified and quantified using the standard congener mixtures as supplied by the National Research Council Canada, Marine Analytical Chemistry Standards Program. Identification of the PCB congeners was according to the numbering system of Ballschmiter and Zell (1980) and Ballschmiter et al., (1987). Critical pairs eluting as single peaks under the gas chromatographic conditions used in the study were: 105 and 153, 118 and 149, 128 and 183. A linear regression model, with time as the only independent variable, was used to establish whether the concentrations of tDDT and PCB declined over time (1980-1987) in the common and bottlenose dolphins from the east coast. The available data do not pass the test for normality and prediction values could not be calculated. To avoid the fluctuations in the concentrations of organochlorines caused by parturition and lactation, only mature males and juveniles were used in this analysis. All concentrations of organochlorines are expressed as /zg g-1 wet mass. 3. Results 3.1. West coast

Residues of DDE, PCBs and hexachlorobenzene (HCB) were found to be the most prevalent in the blubber of the specimens analyzed. DDT

157

was detected less frequently and dieldrin residues were only present in a small percentage of the samples. The variation in concentration levels between individuals was great and no clear trend could be established. The residue levels of tDDT and PCBs in the species analysed were substantially lower than values reported for the northern hemisphere (Table 2). PCB congeners, eluting as single peaks, detected most frequently were; 105, 114, 118, 128, 138, 151, 153, 180, 189, 194 and 200. The toxic non-ortho coplanar PCBs 77, 126, and 169 and the mono-ortho coplanar 156 could not be isolated from other PCB congeners present in the sampies. Contributions to the results from invisible co-eluting congeners cannot therefore be excluded. The concentration of the di-ortho-congeners was higher than the mono-ortho congeners. The frequency of detection of 151, having a group of adjacent unsubstituted non-chlorinated meta and para carbon atoms in the biphenyl ring lends support to the observation that small cetaceans do not have the capacity to metabolise these PCBs (Tanabe et al., 1988; Tanabe and Tatsukawa, 1991). Lower chlorinated biphenyls were found to contribute only a small fraction to the total composition of PCBs in these animals. Tanabe et al., (1988) reported that the proportion of lower chlorinated biphenyls is less in warm water than in cold water with a similar pattern in prey species of small cetaceans. 3.2. East coast

When allowing for the variation with age, sex and condition, mature bottlenose dolphins were found to have higher overall burdens than common dolphins between 1980 and 1987 (Fig. 2). tDDT and PCB concentrations were significantly higher in mature male dolphins than in mature females in both the common dolphin and bottlenose dolphin (P < 0.05). Regression analysis of the residue levels with sex, age and length show that the relationships, in both males and females, were non-linear. The results of the linear regression model with time as the only variable are summarised in Table 3. There is a fairly strong indication that DDT and PCBs in the

A.C de Kock et al. /Sci. Total Environ. 154 (1994) 153-162

158

Table 2 Organochlorine residues detected in blubber of cetaceans from various areas in the world. Residue concentrations expressed as /zg g-1 wet mass Species

Locality

Year

Sex

Minke whales

Indian Ocean Indian Ocean Antarctic Antarctic South Atlantic California

1974 1974 1986 1986 1986 1968

Caribbean

1971-1975

Indian Ocean

1974

Mediterranean South Atlantic

1980 1986

M F M F F M F F M F M M and F M

0.19 0.21 0.07 0.04 0.07 5.6 5.9 15 1.1 0.23 0.22 4.2 0.39

South Carolina

1971-1975

Mediterranean South Atlantic

1982 1984 1986

M M F F M

38 65 11 0.62 0.39

14 29 4.8 0.47 0.26

Aguilar et al., 1982 This study This study

South Atlantic South Atlantic

1971 1984 1986

NA M F

0.26 7.5 1.3

ND 2.7 0.39

Aucamp et al., 1971 This study This study

Eastern Pacific

1980 1983 1984 1986 1978-1979

32 53 29 1.01 0.74 38

7.3 5.1 21 1.28 1.11 29

O'Shea et al., 1980

Japan South Atlantic

F M M F M M

Tanabe et al., 1983 This study This study Loganathan et al., 1990

1986

M

37

28

Loganathan et a1.,1990

Bay of Bengal

1976 1980 1984 1987 1990

Indian Ocean

1980-1987

M F M F M F M

4.1 1796 12 17 4.5 9.9 28

California

1980

Japan

1980

South Atlantic

1984-1986

F M F M M F

822 966 36 84 8.4 1.9

South Pacific South Atlantic

1983 1986-1987

M M

9.6 3

Sperm whales

DDT

PCB

Reference

ND ND 0.01 0.01 0.01 ND

Henry and Best, 1983 Henry and Best, 1983 Tanabe et al., 1985 Tanahe et al., 1985 This study Wolman and Wilson, 1970

4.0 0.72 ND

Taruski et al., 1975

8.3 0.13

Henry and Best, 1983 Aguilar, 1983 This study

Blainville's beaked whale Taruski et al., 1975

Risso's dolphin

Striped dolphin

Western Pacific Bottlenose dolphin South Atlantic California South Atlantic

0.34 420 1.6 1.6 0.52 0.51 16

This study O'Shea et al., 1980 This study This study Tanabe et al., 1993 Tanabe et al., 1993 This study

80 123 50 64 5.5 1.8

O'Shea et al., 1980

Common dolphin

O'Shea et al., 1980 This study

Dusky dolphin

ND, not detected; NA, not available.

1.4 2.02

Tanabe et al., 1983 This study

A.C. de Kock et al. / Sci. Total Environ. 154 (1994) 153-162

159

Bottlenose Dolphin

Common Dolphin 40

10 8

3,~ o~0

T

~z5 I.,-20

r

1

"'2

0 MM

MF

JM

FJ

MM

MF

Common Dolphin

JM

FJ

Bottlenose Dolphin

12 9

- ' 0

T

1 MM

~

MF

JM

FJ

2O

T

t0

1 MM

MF

JM

FJ

Fig. 2. Average D D T and PCB residue concentrations in the blubber of common and bottlenose dolphins from the east coast of South Africa. MM, mature males; MF, mature females; JM, juvenile males; FJ, juvenile females.

common dolphin did not increase over time. DDT in the bottlenose dolphin showed a significant decline (P < 0.05). The PCBs in the bottlenose dolphin show no significant decrease with time (P > 0.05; Fig. 3). 4. D i s c u s s i o n

It is difficult to compare concentrations of DDT and PCBs in cetaceans from various geographical areas. Frequently, the sample sizes are small and not always well characterised (e.g. sex, age and collection methods) with incomplete information on the life history of the sampled animal. HeaviTable 3 Regression analysis of DDT and PCBs in the blubber dolphins from the east coast of South Africa Variable

Gradient

P-value

Bottlenose dolphin PCB Bottlenose dolphin DDT Common dolphin PCB Common dolphin DDT

0.21 -2.4 -0.38 -0.37

0.75 0.02 0.35 0.19

Note: Mature females were excluded from the data set.

side's dolphin (Cephalorhynchus heavisidii) is endemic to the west coast with a coastal distribution from Cape Point in the south to the southern Angolan border. The dusky dolphin (Lagenorhychus obscurus) occurs in inshore waters off the west coast to about 12°S in Angola, and ranges over to the continental slope. Consequently, the organochlorine concentrations in these species should give an indication of the contamination of the marine ecosystem in which they live. The tDDT and PCB median levels for the two species are similar (Table 1). The average HCB concentration in these two species is 0.04/zg g-I on a wet mass basis or 0.08 /xg g-1 on an extractable lipid basis. In their survey on Commerson's dolphins, Abernou et al., (1986) found, on average, HCB concentrations of 0.5 /zg g-1 (extracted lipid). The high t D D T / P C B ratios for 1977 and 1982 were not observed again in the samples after 1982. Martineau et al., (1987) regarded a t D D T / P C B ratio of < 1 as an indication of the lack of DDT input to an ecosystem. The mean D D E / t D D T ratio for the Beluga whales in the same study was 0.52. In our study, the

A.C. de Kock et al. /Sci. Total Ent~ron. 154 (1994) 153-162

160

I

15

I

!

;

t i

I00

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i

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i ....... t

80

L

~ 9

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f

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o

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1980

1,,,

1981

,I . . . . . . . .

198Z

1983

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o

1984

19e5

igeo

1982

COMMON DOLPHIN

g.1 w e t I

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I

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198e

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40

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mass

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i

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l

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~ ............... ~ .............. ;.............. ~ -

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30

m

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BOTTLENOSE DOLPHIN

T D D T C o n c e n t r a t i o n e x p r e s s e d as/~g

! |

1904

I

i

~----=---~

•

r

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zo, . "--~..~.... _. .'r.....~,m_, .roB" .]-',--! ;;; .....

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1980 1981 198Z 1983 19B4 1985

IgeO 198Z 1984 1988 1988

COMMON DOLPHIN

BOTTLENOSE DOLPHIN

P C B C o n c e n t r a t i o n e x p r e s s e d as/~g g.1 w e t m a s s Fig. 3. Graphs of the regression analysis (with time as the only independent variable) for DDT and PCBs in common and bottlenose dolphins. Mature females were not included in the data set.

A.C de Kock et al. / Sci. Total Environ. 154 (1994) 153-162

D D E / t D D T ratio increased, from 1982 onwards, concurrently with the decrease in the tDDT/PCB ratio. After Aguilar (1984), the mean D D E / t D D T ratios of 0.76 and 0.71 for the dusky and Heaviside dolphins, respectively would seem to suggest that no significant input of DDT has occurred in the coastal waters off the west coast of South Africa. There is no clear indication of a decrease or increase of tDDT and PCB concentrations in the dolphin samples of the two species from 1977 to 1987 (Table 1). Unfortunately, the sample sizes are too small to draw any firm conclusions and one can only make a rough assessment of the chronology of input of contaminants into the marine ecosystem in which these species live. The scarcity of arable land together with a low annual rainfall along the west coast of southern Africa, makes it unlikely that high DDT or PCB levels will be found in cetaceans inhabiting the waters along this coast. DDT residues were not detected in soils, water, and biota in northern Namibia where DDT is used against malaria vectors (de Kock, 1990). The DDT was found to disperse rapidly under the prevailing hot arid conditions. Atmospheric transport of DDT to the ocean cannot be ruled out as a possible source of DDT. In southern African waters the common dolphin (Delphinus delphis) occurs along the coast between Port Elizabeth and Cape Town (Fig. 1). They are found over the continental shelf, but not as close to the coast as bottlenose dolphins. The bottlenose dolphin (Tursiops truncatus) is frequently encountered along the east coast of southern Africa, where they occur in shallow coastal waters, generally inshore of the 30-m isobath (Ross, 1984). The higher levels of organochlorines in the bottlenose dolphin as compared to the common dolphin reflects this inshore distribution of the bottlenose dolphins (Cockcroft et al., 1990). The increase of DDTs and PCBs with age in male common and bottlenose dolphins is in parallel with observations on striped dolphins (Stenella coeruleoalba) from Japan (Fukushima and Kawai, 1981), beluga whales (Delphinapterus leucas) from eastern Canadian waters (Martineau et al., 1987), and minke whales (Balaenoptera acutorostrata) from the Antarctic (Tanabe et al., 1985). Our results

161

show that PCB contamination in the marine waters along the east coast has not yet shown any significant temporal decline between 1980 and 1987. This is similar to results of a survey carried out on striped dolphins from the western north Pacific (Loganathan et al., 1990). The results of this study clearly demonstrate the slow temporal changes in the concentration of PCBs in the marine environment along the South African coast and that the present PCB contamination in cetacean species inhabiting these waters will continue. It can be concluded that cetaceans which have a long life-span and a low capacity to metabolise the organochlorines are subjected to long-term accumulation and consequently probable chronic toxic effects from the persistent organochlorines.

Acknowledgements The study was financed by SANCOR (FRD). Their support is gratefully acknowledged. Thanks are also due to the Director and staff of the Natal Sharks Board who made the collection of samples from the east coast possible. We are grateful to Mrs C. Saunders for her technical assistance.

References Abernou, A., D. Robineau and P. Michel, 1986. Organochlorine contamination of Commerson's dolphin from the Kerguelen Islands. Oceanol. Acta, 9: 19-29. Addison, R.F. and P.F. Brodie, 1987. Transfer of organochlorine residues from blubber through the circulatory system to milk in the lactating grey seal Halichoerus grypus. Can. J. Fish. Aquat. Sci., 44: 782-786. Addison, R.F., P.F. Brodie, M.E. Zinck and D.E. Sergeant, 1984. DDT has declined more than PCBs in eastern Canadian seals during the 1970s. Environ. Sci. Technol., 18: 935-937. Addison, R F., M.E. Zinck and T.G. Smith, 1986. PCBs have declined more than DDT-group residues in Arctic ringed seals (Phoca hispida) between 1972 and 1981. Environ. Sci. Technol., 20: 253-255. Aguilar, A., 1983. Organochlorine pollution in sperm whales, Physeter macrocephalus, from the temperate waters of the eastern North Atlantic. Mar. Pollut. Bull., 14: 349-352. Aguilar, A., 1984. Relationship of D D E / E D D T in marine mammals to the chronology of DDT input into the ecosystem. Can. J. Fish. Aquat. Sci., 41: 840-844. Aguilar, A. and A. Borrell, 1988. Age- and sex-related changes

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