Marine Environmental Research, Vol. 44, NO. 1, pp. 9%113, 1997 0 1997 ElsevierScienceLtd All rights reserved. Printedin Great Britain
PII:
SOl41-1136(96)00105-5
0141-1136/97 %17.00+0.00
Organochlorine Contaminants in the Northern Shrimp, Pandahs borealis, Collected from the Northwest Atlantic J. Hellou,* D. Parsons & G. Mercer Science Branch, Department of Fisheries and Oceans, P.O. Box 5667, St John’s, Newfoundland AlC 5X 1, Canada (Received 11 April 1996; revised version received 3 October 1996; accepted 21 October 1996) ABSTRACT Northern shrimp, Pandalus borealis, were sampled at two commercially important locations in the Northwest Atlantic andsoft tissues analysedfor a variety of organochlorine pollutants. Sampling facilitated examination of the environmental and experimental variability to determine if and how location, season, sex or size aflects results. Organochlorine compounds including polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins and dibenbenzofurans were non-detectable in muscle tissue (DLs=O.O14.5 rig/g and 0.14.5 pgjg, for the two groups, wet weight). Concentrations were highest in hepatopancreas, the tissue with a higher lipid content (mean = 28% vs 0.27% in muscle. The larger variation in the tissue distribution of contaminants was observed in April versus Novemberfemales. Higher concentrations were observed in November eggs and in hepatopancreas of females sampled in April. The present study indicates the presence of a larger number of PCB and PCDF congeners in the hepatopancreas of shrimp, a lower link in the Northwest Atlantic food chain, as compared to livers of previously studied fin&h species. 0 1997 Elsevier Science Ltd. All rights reserved
INTRODUCTION The Toxic Chemicals Program, a five year initiative of the Canadian Federal government, began in 1992 and aims to assess the state of the environment. One study is related to determining the level of priority pollutants in commercially valuable fisheries resources of the Northwest Atlantic (Hellou et al., 1993a,b, 1994a,b, 1995). In 1994, northern shrimp were sampled to determine the level of contaminants present in soft tissues of a benthic species representing an integral part of the food chain. The northern shrimp, Pandalus borealis, also called pink shrimp, can be found in the Northwest Atlantic from as far north as Davis Strait to the Gulf of Maine (Butler, 1971). *To whom correspondence
should be addressed. 99
deviation.
April April April July August November April July July July August November
F F F F F F M M M M M M
25 25 25 25 OA OA 25 2J 25 25 OA OA
*SD. standard
Month
Sex
NAFO
Length (mm) of Sampled
24.6 24.35 23.59 24.18 26.08 26.23 18.17 16.95 17.29 17.30 18.32 19.50
Mean 1.22 1.13 1.02 1.67 1.07 1.04 1.68 1.38 1.28 1.28 0.96 13.8
22.28-26.74 22.28-27.06 21.99-25.77 20.74-27.29 24.04-28.37 24.4G28.74 14.89-21.71 13.18-20.83 13.41-20.77 14.35-20.44 15.99-20.76 16.01-21.88
Range 167(72) 153(70) 138(69) 143(87) 160(84) 152(65) 173(91) 139(86) 1.9(85) 146(86) 161(85) 189(88)
Muscle 78gO.26 77-o. 19 784.20 774.08 77-0.16 774.38 774.14 77-O. 11 78&0.12 78&O.13 78-0.57 784.49
W-L
TABLE 1 (g) of Organs Followed by (%) of Soft Tissue Weight (W) and Lipid (L) Content (%)
SD*
Shrimp and Weight
20(9) 20(9) 18(9) 22(13) 30(16) 27(11) 18(9) 23(14) 24(15) 23(14) 28( 15) 25(12)
Hepatop.
Disregarding
61-22 61-22 59-24 58-27 58-27 65-29 6619 53-33 5628 52234 53-38 62-28
W-L
the Weight
79-2.4 79-2.2 79-2.7
62-8 56(24)
W-L 43(19) 46(21) 43(22)
Eggs
of the Head, Water
3 $ L g 9 0 r
Organochlorinecontaminantsin the northern shrimp, Pandalus borealis
101
The commercial fishery in the Canadian northwest began in the mid 1970s. Catches in the 1990s reached 25,000 to 30,000 tons annually with the 1995 catch the highest recorded. This crustacean migrates both vertically through the water column, as part of its feeding behaviour, and horizontally, showing seasonal changes in the distribution of the various sex and age classes (Shumway et al., 1985). The northern shrimp is a protandric hermaphrodite. Eggs, carried by the female for up to eight months in some divisions, hatch in spring and pelagic larval stages last for several months (Parsons, 1982). Juveniles settle in relatively shallow waters and gradually move to deeper water with age. They mature first as males and function as such from two to several years. Then, through a series of moults, they pass through a transitional stage when sex change occurs and spend the rest of their lives (two years or more) as mature females (Parsons ef al., 1986). Life span varies by area, lasting for eight years or more in some northerly populations. In the Northwest Atlantic, larvae feed on plankton in the near-surface waters, generally within the first 50 m. Juveniles and adults are found near or on the ocean floor during the daytime where they feed on a variety of items including polychaete worms, diatoms, foraminifera, crustaceans, phytobenthos and detritus. Shrimp also migrate vertically in the water column during the night where they prey primarily upon pelagic crustaceans (e.g. mysids, euphasiids, copepods). Predators of the northern shrimp are numerous and include Greenland halibut (and other flatfishes), cod, hake, eelpouts, skates and sometimes harp seals. The protandry of Pandalus borealis allows the combination of two variables, size and sex, during sampling. Many endogenous (organism-related) and exogenous (environmentrelated) variables can affect the bioaccumulation of contaminants and their delineation allows a better interpretation of fates and effects (McElroy et al., 1989). Knowledge regarding the distribution of contaminants in tissues of organisms, along with the physical-chemical properties of the studied compounds, help in modelling, assessing and ultimately predicting toxicity (e.g. McCarthy & Mackay, 1993).
MATERIALS
AND METHODS
Northern shrimp, Pandulus borealis, were collected with the help of the Observers Program of the Department of Fisheries and Oceans from two Northwest Atlantic Fisheries Organisation (NAFO) divisions. Sampling was performed in early April and at the end of July, in division 25 (depth: 38&399 m); at the end of August .and in early November, in division OA (depth: 29@460 m; Fig. 1). Prior to analysis, shrimp were separated into abdominal shell, muscle, hepatopancreas and eggs, when appropriate. Only soft tissues were used for analyses of organic contaminants, while the cephalothorax was discarded. To obtain enough material to perform several analyses on one sample, pools of 43 females or 115 males were needed in April and this number was maintained during the later sampling. Shrimp were selected somewhat randomly from a large number of organisms obtained from three boxes (several kg/each) collected from one or three contiguous tows. Sex was determined using external characteristics of the endopod of the first pleopod and oblique carapace length (mm) measured with calipers from the posterior margin of the eye socket to the posterior mid-dorsal margin of the carapace.
J. Hellou et al.
102
66
GREENLAND
64
62
\
\
\
\
Si
5(
41
4t
41
c
48
?6O
74’
72’
10’
68.
6P
64.
62.
60.
UT
56’
Fig. 1. Map of the Northwest Atlantic Fisheries Organisation
54.
5T
Divisions. Cross indicating the location of sampling in OA and 25.
Organochlorine contaminants in the northern shrimp, Pandalus borealis
103
Analyses of various organic contaminants, dry weight and lipid content were performed by sub-sampling homogenised tissue pools. The analytical approach was identical to that outlined in detail in Hellou et al. (1993a). Briefly, PCDDs and PCDFs are extracted by mixing tissue and anhydrous sodium sulphate with dichloromethane:hexane (1: I), purification takes place by column chromatography while quantification is performed by HRGC-MS (MIM). Other OC pesticides are purified on a Florisil column, OCs eluted with hexane are analysed by GC-MS and a fraction eluted with dichloromethane:hexane (1: 1) is analysed by GC-ECD. The QA/QC protocol includes the processing of a blank, a duplicate and a standard reference material or spiked matrix with every batch of samples (3-8). Females caught in April and males caught in July were sampled in triplicate to determine the environmental variability. Tissues from one pool of these latter females and males were analysed in duplicate to determine the experimental variability (five samples). Each analysed sample also contained labelled surrogate standards that allowed the determination of recoveries and adjustment of the concentrations. The following series of 23 OCs were analysed: ~1,B and y-HCH; HCB; oxychlordane; trans- and cis-nonachlor- and chlordane; heptachlor; heptachlor epoxide; methoxychlor; o,p’- and p,p’-DDE, DDT and DDD; mirex; dieldrin; endrin; aldrin and polychlorinatedbiphenyls (PCBs) measured as Aroclor standards (1242, 1254 and 1260, where the highest values using 1254 are reported). A series of 17 polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) substituted at C-2, 3, 7, 8 and total tetra-, penta-, hexa-, hepta- and octa-chlorinated were also analysed. Also, PCBs were quantified as congeners, with some unresolved (/): 5/8, 15, 16/32, 17, 18, 19, 21/28,22,24/27,25, 26, 33, 40, 41164171, 45, 46, 47148, 49, 52, 56160, 66, 70176, 74, 83, 84189, 85, 87, 90/101, 91, 95, 97, 99, 105, 107, 110, 114, 118, 128, 129, 130, 131, 134, 136, 135/144, 137, 138/163/164, 141, 146, 149, 151, 153, 156, 157, 158, 170/190, 171, 172, 174, 175, 176, 177, 178, 180, 182/ 187, 183, 185, 189, 191, 194, 195, 196/203, 197, 198, 199,201,205,206,207,208 and 209. All concentrations are expressed in terms of wet weight and can be converted to dry weight using mean moisture values of 60, 71 and 78% for hepatopancreas, eggs and muscle, respectively. Lipid content was determined gravimetrically by evaporating a subsample of dichloromethane:hexane (1: 1) tissue extract. Recoveries of standard reference materials for OCs and PCB congeners (cod liver oil CRM235) ranged between 66 and 120%. Recoveries of 13C labelled dioxins and furans standards ranged between 58 and 96%. Recoveries of internal standards for OCs, dioxins and furans, displayed means between 85 and 108% (for 9 labelled OCs) and 57 to 84% (for 9 labelled PCDDs or PCDFs). Detection limits varied with each injection, DL = O.Ol0.5 rig/g,, with an increasing DL going from PCB congeners to OCs, while for dioxins and furans, DL = 0.14.5 pg/g.
RESULTS Environmental and experimental variability
A large number of shrimp were pooled in order to obtain enough material for several analyses and to reduce the environmental variability known to accompany field studies of contaminant concentrations. Sampling took place in two separate divisions, and at two times of year in each division, to determine the possible influence of these variables. The
104
J. Hellou et al.
April and July sampling was performed at one site, near Newfoundland and Labrador, while the August and November sampling was at a more northern location in the Davis Strait (Fig. 1). The July and August sampling allowed comparison between locations at approximately the same time of year and helped to determine the extent of the comparison between April and November. The environmental variability was assessed by comparing results of analyses performed on triplicate pools obtained from one division for various tissues of each sex. Variability was independent of sample size, i.e. pools of 43 or 115 shrimps. Detectable concentrations in hepatopancreas displayed a coefficient of variation ([standard deviation/mean] x 100) between 0 and 63%, with a mean of 8 and 30%, for the series of pesticides and group of dioxins and furans, respectively. The experimental variability was estimated from the analysis of five pools in duplicate and showed a O-80% variation in concentrations, with a mean of 20% (comparing higher to lower values). In some cases, over a 100% variation was observed when comparing fractions of a nanogram or picogram. Size-sex distribution Depending on location and water temperature in a particular environment, growth rate, which is also related to diet, may vary (Parsons et al., 1989). Therefore, care was taken in identifying sexes, by examining the external structure of the first two pleopods, along with measuring length (Berreur-Bonnenfant & Charniaux-Cotton, 1965). In the present sampling, males measured between 13 and 22 mm, while females were between 21 and 29 mm (Table 1). Shrimp undergoing a sex change were not used. According to the literature, males are expected to be up to six years old, while larger females are between six and 8 + years of age. No smaller shrimp were sampled, since the commercial fishery targets the larger sizes through selective mesh size in the trawls and by fishing on grounds where, primarily, larger animals are found. As outlined in Table 1, sampling in Division OA tended to cover shrimp of a slightly larger size range than in the southern division, 25. This difference is observed between divisions, irrespective of month, and is more pronounced in females than in males. The weight of the various organs is reported in terms of the total removed soft tissue per pool (minus cephalothorax), and percent contribution of an organ to the total soft weight. In males, muscle represented 85 to 91% of the soft tissue weight while in ovigerous females muscle represented 65 to 72% of the weight. In April and November, eggs represented 21 and 24% of the weight. Hepatopancreas represented between 9 and 16% of the soft tissue weight. Water and lipid content The water content of muscle tissue did not vary with sex or time of year and was higher than in hepatopancreas (Table 1). The water content of April eggs was higher than in November. The lipid content of tissues showed a trend opposite to that of moisture, with muscle tissue containing the least lipid. The larger difference between sexes was observed in July and August, for muscle and hepatopancreas, where males had a higher lipid content than females (Table 1). The lipid content of eggs was higher in November than April, with values between those observed in muscle and hepatopancreas.
Organochlorine contaminants in the northern shrimp, Pandalus borealis
Females
105
Males
Fig. 2. Concentration
(pg/g, wet) of polychlorinated dibenzo-p-dioxins and dibenzofurans (TCDF: tetrachloro- and pentachloro-dibenzofuran, TCDD: tetrachlorodioxin) in hepatopancreas presented by sex (M and F) and sampling month, IV: April, VII: July, VIII: August and XI: November. 2,3,7,8-TCDF represented 15% of total TCDF.
Polychlorinated dibenzo-pdioxins and dibenzofurans The concentration of OCs, including the group of dioxins and furans, followed the general pattern observed with lipid content. OCs were nearly undetectable in muscle while the highest levels were observed in hepatopancreas. Tetrachloro-dibenzofurans (TCDFs) were 4 to 6 times higher than pentachlorofurans (PCDFs), while total tetrachlorodioxins were below 3 pg/g (wet weight; Fig. 2). When detected 2,3,7,8-TCDF and 1,2,3,7,8-PCDF represented about 15 and 17% of total TCDFs and PCDFs, respectively, while 2,3,7,8TCDD, the most toxic congener of the series represented 25% of total TCDDs. Concentrations of TCDFs in hepatopancreas varied by less than 50% among males or females, or with sampling time. However, in the hepatopancreas of both sexes PCDFs increased from July to August to November (almost double), with the highest levels observed in hepatopancreas of April females. In April and November, TCDFs and PCDFs were present in eggs with November concentrations double those observed in April (Table 2). Concentrations of TCDFs in females were in a 7:l and 2.5:1 ratio in hepatopancreas:eggs, in April and November, respectively. During the same months, lipids in these same tissues were present in a 9.5:1 and 3.5:1 ratio. Other organochlorine
compounds
Of the analysed organochlorine compounds, PCBs measured as Aroclor 1254 predominated over other pesticides (Fig. 3). Very few organochlorines were detected in muscle, and then only at 0.1 rig/g (HCB, trans-nonachlor, heptachlor epoxide and dieldrin). Concentrations in eggs from April were nearly half those observed in November and about 10 and 4 times lower than in hepatopancreas (Table 2). In hepatopancreas of females, PCB concentrations were similar for July and August, in the different divisions,
106
Concentration
J. Hellou et al.
of Furans,
TABLE 2 Pesticides and PCB Congeners Except for *)
Contaminant
April
Total TCDF* 3,4,7,8-TCDF* Total PCDF* PCBs t-Nonachlor Dieldrin a-HCH HCB Oxychlordane cis-Nonachlor p,p’-DDE Heptachlor epoxide Endrin
6.5 1.1 1.1 4.3 1.7 1.6 0.8 1.6 < 1.0 0.5 0.5 0.3 0.3
November
12 2.0 2.9 10 5 2.2 3.1 3.4 1.8 1.6 1 0.5 0.3
Detected in Eggs (ng/g, Wet Weight,
Congener
April
153 138/163/164 9OjlOl 118 99 180 74 70176 149 31 66 105
1.1 0.6 0.5 0.6 0.3 0.2 0.3 0.3 0.2 0.2 0.2 0.2
November
2.8 1.4 1.1 1.5 1 0.5 0.7 0.5 0.4 0.3 0.4 0.4
*Concentrations in pg/g, wet weight. IUPAC congeners and contaminants present at or above 0.2 n/g (wet weight), where April values represent means.
Concentration of organochlorines~--/ in hepatopantmas
;Itahs
jFrmaks1 I
PCB + t-non * die1 iv HCH HCB + c-non ~~ DDE x hep -+ endtin -0xy
+
Fig. 3. Concentration
of organochlorine compounds above 1 rig/g (wet) in hepatopancreas presented by sex (M and F) and sampling month, IV: April, VII: July, VIII: August and XI: November, t-non: trans-nonachlor, diel:dieldrin, HCH:u-hexachlorocyclohexane, HCB:hexachlorobenzene, oxy: oxychlordane, c-non: cis-nanochlor, hep: heptachlor epoxide.
and showed a 50 and 100% increase in November and April, respectively. In hepatopancreas of males from division 25, the July concentration was half that observed in
April, August or November. The same general trend was observed for several OCs including truns-nonachlor, HCH and HCB which give strong correlations with total PCBs (Table 3). Correlations between TCDFs and many OCs tended to be the weakest.
0.0001 0.0007 0.0044 0.0047 0.0067 0.0207 0.0562 0.0000 0.0002
0.0006 0.0003 0.0000
0.0000
HCB
of Pearson
0.0000 0.0001
a-HCH
Correlations
0.0023 0.0014 0.0002 0.0004
t-non
dieI 0.0243 0.0138 0.0083 0.0010 0.0088
oxy 0.0571 0.0385 0.0180 0.0019 0.0273 0.0001
c-non
oxy: oxychlordane,
0.0965 0.0643 0.0442 0.0504 0.0826 0.0037 0.0010 0.0011 0.0026
DDE
Concentrations
0.0874 0.0422 0.0304 0.0102 0.0478 0.0007 0.0004 0.0000
hept
diel: dieldrin,
0.0687 0.0333 0.0226 0.0031 0.0383 0.0004 0.0002
end
TABLE 3 between Lipid Content and Organochlorine Observed in Hepatopancreas (n = 8)
0.0000 0.000 1 0.0000 0.0002
Performed
*The following abbreviations are used in the Table. Lip: lipid, t-non: tram-nonachlor, endrin, hept: heptachlor epoxide.
Lip HCB HCH t-non die1 oxy c-non end hept DDE TCDF PCDF TCDD
PCBs
Level of Significance
0.0010 0.0006 0.0001 0.0007 0.0001 0.0003 0.0033 0.0055 0.0076 0.0217 0.0678
PCDF
end:
0.0005 0.0028 0.0151 0.0170 0.0176 0.0711 0.0573 0.0001
0.0026 0.0007 0.0011
TCDD
Organochlorine
c-non: cis-nonachlor,
0.1153 0.0756 0.0691 0.0000 0.0626 0.1200 0.1404 0.0773 0.0675 0.3178
TCDF
and between
108
J. Hellou et al.
lFemdes j
-1 *153+138+90 +149+31 t-88
+-118+99 a 105-52
~180474 -70 *170+183--187
Fig. 4. Concentration (ng/g, wet) of PCB congeners (IIIPAC number) in hepatopancreas presented by sex and sampling month, IV: April, VII: July, VIII: August and XI: November. Correlation coefficients between lipid content and OC concentrations were generally significant (Table 3). PCBs were also analysed in terms of specific congeners and none was detected in muscle (DL = 0.01 and 0.22 rig/g,, wet weight). However, more congeners were detected in hepatopancreas and at a higher concentration (0.1-I 1 rig/g)) than in eggs (0.04 2.8 rig/g,, Fig. 4 and Table 2).
DISCUSSlON Organic contaminants Organochlorine compounds are a group of chemicals that were synthesized to respond to specific needs for pesticides, insecticides, fungicides and industrial additives (Kalmaz & Kalmaz, 1979). Some OCs also derive from combustion processes and have been identified in pulp mill effluents using chlorine bleach (Rappe et af., 1987; Barrie et al., 1992; Fangmark et al., 1993). Although the production or use of many OCs has been restricted or banned since the 70s their chemical stability has lead to their persistence in the environment. Due to their associated toxicity, many OCs have been recognized as priority pollutants by the US, Canada and the European Community. It is important to investigate the level of OCs in biota to assess the risk faced by various species through potential biomagnification in the food chain, to monitor changes with time, as well as to assess toxic effects that could occur within a species (McCarthy & Mackay, 1993). It is now well established that organic contaminants with a high Henry’s law constant (ratio of solute partial pressure in air to equilibrium concentration in water) tend to volatilise from warmer locations, undergo atmospheric transport and condense into colder waters (Iwata et al., 1993). This phenomena explains why contaminants can be detected in more remote locations such as the Arctic (Mackay & Wania, 1995; Lockhart, 1995).
Organochlorinecontaminantsin the northern shrimp, Pandalus borealis
109
Variability and observations Feral and experimental exposures carry a degree of variability in the response of individuals. Laboratory exposures standardise many variables to allow a better interpretation of the results. In field studies, it is important to determine the influence of environmentrelated or organism-related variables on fate to provide a better assessment of results. Two major aspects of variability need consideration: environmental and experimental. Environmental variability will depend on the geographical area covered, the number of organisms pooled (or not), the migration, movement and/or preferred habitat of the species and the specificity of the sampling (e.g. restricted size or age, sex, season). The experimental variability, addressed by good laboratory practices (QA/QC) shows larger variability at lower concentrations. Previous sampling indicated a mean environmental variation of 13% when pooling tissues from seven fish (Hellou et al., 1995). Kelly and Campbell (1994) reported a field variance of 150% for individual fish and of 30% for pools of 25 fish. In the present study, a relatively equal environmental and experimental variation (between 0 and 30%) was observed, in three types of analyses when using 43 or 115 shrimp. These observations demonstrate the importance of delineating the sampling variables and of reporting them in any study (Uthe el al., 1996). An accurate knowledge of, at least, sex, size and season will allow a better interpretation of results. To draw a cautious conclusion when comparing the present results, a greater than fifty percent increase in contaminant concentration would be needed (DLs also need consideration). Therefore, the present study would indicate higher levels of PCBs and TCDFs in hepatopancreas of April females versus other samples. The more obvious change is a two-fold increase in the concentration of OCs observed in November versus April eggs, correlating with a four times higher lipid content. These changes are associated with the reproductive cycle of females, where higher levels in eggs correspond to lower levels in hepatopancreas (November). A similar ratio of PCDF:TCDF (4:l) is observed in both tissues in November, while higher levels of TCDF in April eggs versus hepatopancreas (6: 1 vs 4: 1) would tend to indicate a less efficient transport of PCDF from mother to eggs. The recommended log K,, for 2,3,7&TCDF and 2,3,4,7,8-PCDF is of 6.1 and 6.5, respectively, indicating a lower solubility of the more chlorinated congener (Mackay et al., 1991). Differences have also been observed in the ratio of organochlorines analysed in tissues of marine mammals and finfish (e.g. Jenssen et al., 1996; Hellou et al., 1995). Another trend is represented by higher levels of PCDFs in hepatopancreas of both sexes, from July through to November. This higher log K,, of PCDF would also indicate a longer time to reach equilibrium within tissues, possibly explaining why the trend is observed with the less soluble furan (Mackay, 1991). This increase could possibly be due to a higher atmospheric input in the winter versus summer (Brun et al., 1991). Within the 2,3,7,8-chlorodioxins, TCDD has a recommended log K,, of 6.80, while the more chlorinated congeners display values of 7.4, 7.8, 8.0 and 8.2 (Mackay et al., 1991). It has been proposed that under ideal conditions, the bioaccumulation of contaminants can be explained for compounds with a log K,, below 4 by uptake through the water (McKim, 1994). More hydrophobic compounds with a log K,, above 6-7 are taken up more efficiently through the diet, while those with an intermediate K,, value are available through both water and diet. The present results point to very low concentrations of organochlorines with a log K,, value above 7 in the diet of the shrimp.
110
J.
Hellou et al.
Size range, water and lipid content The age and growth of Pandalus borealis inhabiting the Northwest Atlantic has been studied by Savard et al. (1994) and by Parsons et al. (1989) where slower growth and increased longevity were observed in northern areas where temperatures tend to be lower. Although the size distributions of the shrimp analyzed here differ between areas, they are representative of the sizes and ages observed in samples from both the commercial fisheries and research surveys conducted in each. Our results on the lipid content of individual organs can be compared to that previously reported for whole shrimp (Hopkins et al., 1993). A total lipid content of 2.6, 3.6,4.4 and 5.4% (wet weight, without hard tissue) can be deduced for females collected in April, July, August and November, respectively (Table 1). For males, a total of 2.1, 4.5, 5.2, and 3.8% lipid was observed during the same months. This trend can be expressed in terms of dry weight, 7.9, 8.6, 10.8 and 19.2% for females and 6.5, 10.1, 14.2 and 10.7% for males. Therefore, for both sexes, lipid content was lower in winter (April) and has been previously associated with a lower abundance of food (Hopkins et al., 1993; up to 40%:April-Sept., 8%:winter). Comparison of organochlorine results There are very few reports on the level of organic contaminants in shrimp, and none for Pandalus borealis. Levels of OCs have been reported for Parapenaeus longirostris inhabiting the Saronikos Gulf, Greece, where PCB concentrations were 3.7-32; DDTs, 1.5-4.1; HCHs, 0.14.5 rig/g;; while lipids ranged from 0.24 to 0.91% and moisture from 73 to 78% (wet weight; Satsmadjis & Gabrielides, 1983). Although complete analytical information was not provided by Satsmadjis and Gabrielides, according to de Boer (1986) a soxhlet extraction using hexane would tend to underestimate the level of OCs. Nevertheless, expressing our results in terms of whole body burden would give PCBs, 2.84.6; DDTs, 0.2-0.7; HCH, 0.8-1.3 rig/g;; lipids, 2.65.4%; moisture, 73-77% (wet weight). As discussed by several authors, results should be compared on a lipid weight basis and would suggest lower concentrations in shrimp from the Northwest Atlantic (e.g. Muir et al., 1988). A previous comparison of OC concentrations observed in livers of cod to fish from various locations has generally indicated low levels in biota of the Northwest Atlantic (Hellou et al., 1993a). Since various species of finfish from the Northwest Atlantic were previously analysed, an analogy is warranted. Of the series of seventeen specific dioxins and furans analysed in tissues of shrimp and finfish, TCDFs predominated in all cases; however 2,3,7,8-TCDF represented 67-100% of total TCDFs in finfish and 13-17% in shrimp eggs and hepatopancreas. The difference would represent the fraction of furans metabolised by fish MFO enzymes or possibly by other fish-ingested prey (Brown, 1992). The fingerprint for other pesticides detected in hepatopancreas was only slightly different from that in finfish livers. Comparison is done between these two organs since they would reflect bioconcentration in the more lipid rich tissue where more OCs are detected and possibly where equilibrium would be reached more readily. For example, the mean ratio of a-HCH: y-HCH is 6: 1 and 7: 1, in finfish and shrimp; DDE:DDT is 4: 1 for both; PCBs:chlordanes are generally in a 1:1 ratio; while PCBs:DDTs differ, giving a ratio of 7: 1 in hepatopancreas and 1:1 in liver. This latter difference could be partly due to the low concentrations and non-detectable levels of DDD and possibly to the different lipid composition of the tissues and therefore their affinity for DDTs.
Organochlorine contaminants in the northern shrimp, Pandalus borealis
111
The fingerprint of the PCB congeners can also be compared between what was previously reported for flatfish and the present shrimp (Hellou et al., 1995). In both groups, IUPAC congener 153 predominated, followed by 138 (unresolved from 163 and 164), and then by 118 and 180. These congeners are recognized as some of the most bioaccumulative PCBs, while congeners 138 and 118 are members of the 10 most toxic PCBs (McFarland & Clarke, 1989; Falandysz et al., 1994). A noticeable difference between liver and hepatopancreas is due to the presence of four isomers with 3, 4, 4 and 6 chlorine atoms (UIPAC congeners 31, 70 + 76 are unresolved, 74 and 149) in a higher relative proportion in shrimp. Depletion of some congeners in finflsh would be assigned to metabolism in liver and/or possibly in the fish’s prey (Brown, 1992). Concentrations expressed on a lipid weight basis tended to be slightly lower in the hepatopancreas of shrimp than in the liver of finfish.
CONCLUSION Northern shrimp collected at two locations where commercial fishing takes place in the Northwest Atlantic were analysed for a series of priority organic pollutants. Levels of OCs were highest in hepatopancreas, lowest in muscle and correlated with lipid content of tissues. Generally, negligible variations were observed with sex and location except for higher concentrations of OCs in hepatopancreas of April ovigerous females and in November eggs. The present study demonstrated the larger number of PCB, TCDF and PCDF congeners in an organism representing a lower link in the food chain as compared to various finfish species.
ACKNOWLEDGEMENTS The authors would like to thank Mr Joe Firth from the Department of Fisheries and Oceans for his advice regarding the collection of the shrimp and his help through the Observers Program. This study could not have been accomplished without the help of many inspectors and commercial fishers. We would also like to acknowledge funding from the Canadian Toxic Chemicals Program.
REFERENCES Barrie, L. A., Gregor, D., Hargrave, B., Lake, R., Muir, D., Shearer, R., Tracey, B. & Bidleman, T. (1992). Arctic contaminants: sources, occurrence and pathways. Sci. Tot. Environ., 122, l-74. Berreur-Bonnenfant, J. & Charniaux-Cotton, H. (1965). Hermaphrodisme proterandrique et fonctionnement de la zone germinative chez la crevette Pandalus borealis Kroyer. Bull Sot. Zool. Fr., 90, 243-259.
Brown, J. F. (1992). Metabolic alteration of PCB residues in aquatic fauna: distribution of cytochrome P-4501A and P-4502B-like activities. Mar. Environ. Res., 34, 261-266. Brun, G. L., Howell, D. G. & G’Neill, H. J. (1991). Spatial and temporal patterns of organic contaminants in wet precipitation in Atlantic Canada. Environ. Sci. Technol., 25, 1249-1261. Butler, T. H. (1971). A review of the biology of the pink shrimp Pam&As borealis Kroyer 1838. Can. Fish Report, 17, 17-24.
J. Hellou et al.
112
de Boer, J. (1986). Chlorobiphenyls in bound and non-bound lipids of fishes: comparison of different extraction methods. Chemosphere, 17, 1803-l 8 10. Falandysz, J., Tanabe, S. & Tatsukawa, R. (1994). Most toxic and highly bioaccumulative PCB congeners in cod-liver oil of Baltic origin processed in Poland during 1970s and 1980s their TEQ-values and possible intake. Sci. Tot. Environ., 145, 207-212. Fangmark, J. B., van Bave, S., Marklund, B., Berge, N. & Rappe, C. (1993). Influence of combustion parameters on the formation of polychlorinated dibenzo-p-dioxins, dibenzofurans, benzenes, and biphenyls and polyaromatic hydrocarbons in a pilot incinerator. Environ. Sci. Technol., 27, 1602-1610.
Hellou, J., Warren, W. G. & Mercer, G. (1993). Organochlorine contaminants in pleuronectides: comparison between three tissues of three species inhabiting the Northwest Atlantic. Arch. Environ. Contam. Toxicol., 29, 302-308.
Hellou, J., Upshall, C., Taylor, D., O’Keefe, P., O’Malley, V. & Abrajano, A. T. (1994). Unsaturated hydrocarbons in muscle and hemolymph of two crab species, Chionoecetes opilio and Hyas coarctatus. Mar. Poll. Bull., 28, 482488.
Hellou, J., Payne, J. F. & Hamilton, C. (1994). Polycyclic aromatic hydrocarbons in Northwest Atlantic cod (Gadus morhua). Environ. Poll., 84, 197-202. Hellou, J., Warren, W. G. & Payne, J. F. (1993). Organochlorines including polychlorinated biphenyls in muscle, liver and ovaries of cod, Gadus morhua. Arch. Environ. Contam. Toxicol., 25, 497-505.
Hellou, J., Upshall, C., Payne, J. F., Naidu, S. & Paranjape, M. A. (1993). Total unsaturated compounds and polycyclic aromatic hydrocarbons in molluscs collected from waters around Newfoundland. Arch. Environ. Contam. Toxicol., 24, 249-257. Hopkins, C. C. E., Sargent, J. R. & Nilssen, E. M. (1993). Total lipid content, and lipid and fatty acid composition of the deep-water prawn Pandalus borealis from Balsford, northern Norway: growth and feeding relationship. Mar. Ecol. Progress Series, 96, 217-228. Iwata, H., Tanabe, S., Sakas, N. & Tatsukawa, R. (1993). Distribution of persistent organochlorines in the oceanic air and surface seawater and and the role of the oceans on their global transport and fate. Environ. Sci. Technol., 27, 1080-1098. Jenssen, B. M., Skaare, J. U., Ekker, M., Vongraven, D. & Lorentsen, S. H. (1996). Organochlorine compounds in blubber, liver and brain in neonatal grey seal pups. Chemosphere, 32, 21152125.
Kalmaz, E. V. & Kalmaz, G. D. (1979). Transport, distribution and toxic effects of polychlorinated biphenyls in ecosystems: review. Ecol. Mod., 6, 223-251. Kelly, A. G. & Campbell, L. A. (1994). Organochlorine contaminants in liver of cod (Gadus morhua) and muscle of herring (Clupea harengus) from Scottish waters. Mar. Poll. Bull., 28, 103-108. Lockhart, W. L. (1995). Implications of chemical contaminants for aquatic animals in the Canadian Arctic: some review comments. Sci. Tot. Environ. 160-161: 631-641. Mckay, D., Shiu, W. Y. & Ma, K. C. (1991). Illustrated Handbook of physicalchemical properties and environmental fate for organic chemicals. Vol II. Mackay, D. (1991). Multimedia environmental models: the fugacity approach. Lewis Publishers, Chelsea, Michigan. Mackay, D. & Wania, F. (1995). Transport of contaminants to the Arctic: partitioning, processes and models. Sci. Tot. Environ. 160-161: 25-38. McCarthy, L. S. & Mackay, D. (1993). Enhancing ecotoxicological modeling and assessment. Environ. Sci. Technol., 27, 17191728.
McElroy, A. E., Farrington, J. W. & Teal, J. (1989). Bioavailability of polyaromatic hydrocarbons in the aquatic environment. In Metabolism of Polycyclic Aromatic Hydrocarbons in the Aquatic Environment. U. Varanasi, ed. Boca Raton, FL. McFarland, V. A. & Clarke, J. U. (1989). Environmental occurrence, abundance and potential toxicity of polychlorinated biphenyl congeners: considerations for a congener-specific analysis. Environ. Health Persp., 81, 225-239.
McKim, J. M. (1994). Physiological and biochemical mechanisms that regulate the accumulation and toxicity of environmental chemicals in fish. In Bioavailability: Physical, Chemical and Biological Interactions, ed, J. L. Hamelink, P. F. Landrum, H. L. Bergman, W. H. Benson, Lewis Publishers, Boca Raton, FL, pp. 179202.
Organochlorine contaminants in the northern shrimp, Pandalus borealis
113
Muir, D. C. G., Norstrom, R. J. & Simon, M. (1988). Organochlorine contaminants in Arctic marine food chains: Accumulation of specific polychlorinated biphenyls and chlordane related compounds. Environ. Sci. Technol., 22, 1071-1079. Parsons, D. G. (1982). Biological characteristics of northern shrimp (Pandalus borealis) in areas off Labrador. MSc. Thesis, Memorial Univ, St John’s, Newfoundland, Canada. Parsons, D. G., Lilly, G. R. & Chaput, G. J. (1986). Age and growth of northern shrimp Pandalus borealis off northeastern Newfoundland and Southern Labrador. Trans. Amer. Fish Sot., 115, 872-881. Parsons, D. G., Mercer, V. L. & Veitch, P. J. (1989). Comparison of the growth of northern shrimp (Pandalus borealis) from four regions of the Northwest Atlantic. J. Northw. Atl. Fish Sci., 9, 123-131. Rappe, C., Anderson, R., Berqvist, P. A., Brohede, C., Hanson, M., Kjeller, L. O., Linstrom, G., Marklund, S., Nygren, M., Swanson, S. E., Tyskling, M. & Wiberg, K. (1987). Overview on fate of environmental fate of chlorinated dioxins and dibenzofurans. Sources, levels and isomerit patterns in various matrices. Chemosphere, 16, 160316 18. Savard, L., Parsons, D. G. & Carlsson, D. M. (1994). Estimation of age and growth of northern shrimp Pandalus borealis in Davis Strait (NAFO subareas 0 + 1) using cluster and modal analyses. J. Northw. Atl. Fish Sci., 16, 63-74. Satsmadjis, J. & Gabrielides, G. (1983). Organochlorines in mussel and shrimp from the Saranikos Gulf (Greece). Mar. Poll. Bull., 14, 356-358. Shumway, S. E., Perkins, H. C., Schick, D. F. & Stickney, A. P. (1985). Synopsis of biological data on pink shrimp Panaidus borealis Kroyer, 1838. NOAA Tech Report NMFS 30. Uthe, J. F., Misra, R. K. & King, T. L. (1996). Estimating analytical variances in measurement of PAH and application to monitoring contaminants in American Lobster (Homarus americanus). JAOAC Int., 79, 797-802.