early trend determination of organochlorine contamination from residue ratios in the sea lamprey (...

Early Trend Determination of Organochlorine Contamination from Residue Ratios in the Sea Lamprey (Petromyzon marinus) and its

Lake Whitefish (Coregonus clupeaforrnis) Host

Er~vironmental Contaminants Division, National Water Rasearch Pnstitblte, Can~da Centre for Inland Wakrs, Burlington, Ont. L7R 4.45

KAISER, K. E. E. 1982. Early trend determination of organochlorine contamination from residue ratios in the sea lamprey (Pebromyzon imrirzacs) and its lake whitefish (Coregonus clupeqfor~nis) host. Can. J . Fish. Aquat. Sci. 39: 571 -579.

A detailed statistied evaluation of the levels of organochlorine contaminants in sea lamprey (Pefrsmyzon marinus) and simultaneously caught lake whitefish (Coregonus elupeaforzis) from the northern parts of Lakes Huron and Michigan is described. The analysis of residue ratios, both within each species and between, allows an immediate recognition of rising and falling trends of contamination with a high degree of confidence. This improvement over the conventional method of monitoring one species over several years is accomplished with comparatively little effort in sampling and chemical contaminant analysis. The described technique exploits the unique biological relationship of the lamprey and its host and is also based on the significantly shorter lifespan of the (adult) lamprey compared to that of the host. Rising trends in K B and DDE contamination and declining trends for the levels of DDT, dieldrin, endrin, chlordane, hexachlorobenzene, heptachlorepoxide, and aw-hexachlorocyclohexane were observed in 1978, the year of collection.

Key ~ ~ o r d s : organochlorine, contamination, trend, ratio, Petromyzon marinus, Csrsgoraus ckugec~ormis

KAISER, K. L. E. 1982. Early trend determination of organochlorine contamination from residue ratios in the sea lamprey (Pcfromyaon marinus) and its lake whitefish (Coregoaus clupeaformis) host. Can. J. Fish. Aquat. Sci. 39: 571-579.

On trouvera dans l'article qui suit la description d'une evaluation statistique dCtailICe des niveaux de contaminants organochlon5s chez la grande lamproie marine (Pe~rovnyzon marims) et le grand corkgone (C~regonus ckupeafoamis) captures en mCme temps dans les secteurs nord des lacs Huron et Michigan. L'analyse des rapports de rdsidus, tant au sein de chaque espkce qu'entre les espkces, permet de reconnaftre immkdiatement, avec un haut degre de confiance, les tendances, B la hausse ou h la baisse, de la contamination. Cette amelioration sur la methode conventionnelle de surveillance continue d'une espkce pen- dant plusieurs amntes est le fruit d'un Cchantillonnage et d'une andyse chirnique des contaminants ndcessitant relativement p u d'effort. La methode met B profit la relation biologique unique entre la lamprsie et son hate et se base, en outre, sur la dur6e de vie de la lamgroie (adulte), nettement plus courte que celle de l'hdte. Nous avons observe en 1978, I'annCe de collection, me tendmce h la hausse de la contamination par BPC et DBE, et it la baisse des niveaux de BBT, dieldrine, endrine, chlordane, hexachlorobenzkne, heptachlorCpoxyde et a-hexachlorocyclohexane.

Received December 10, 1980 Accepted October 28, 198 1

R e ~ u le 10 dkcembre 19848 Accept6 le 28 octobre 1981

THE presence of organochlorine contaminants (OC), such as Canada and the United States, the use of PCB and DDT has polychlorinated biphenyls (PCB) and numerous pesticides, been banned now for several years. notably p,pl-DBT (DDT) in the Great Lakes ecosystem is To determine the degree and direction of any changes in well recognized. The high levels of many of these contami- environmental contamination, extensive surveillance pro- nants in fishes and birds are of great concern and have led to grams are in place to analyze thousands of fish, sediment, international agreements for stringent water quality objectives and other samples. So far, however, the expected decline of (International Joint Commission 19781, and restrictions on the contaminant levels, based on the limitations of PCB produc- production and use of such chemicals. For example, in tion. has not been verified by the surveillarnce programs

(International Joint Commission 1979). The large standard Winted in Canada (J6317) deviations of contaminant concentrations for most groups of Imprimt au Canada (363 17) biological samples defy attempts to ascertain the degree or

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direction of any changes in many problem areas (International Joint Commission 1979, 1977a). Moreover, changes in fish populations and in the sampling and analytical techniques. result in further reduction of statistical confidence in residue data from different years. Although recent studies on the correlations of certain OC levels with the size and age of fish have improved our understanding QNiimi 198 1, 19791, the application of these to the interpretation of Bakewide trends in OC levels is still limited. Even in groups of narrowly defined specimens the relative standard deviation of a contaminant is frequently found to be in the order of 50% (Niimi 1949). The combination of such variations with the considerable length of time required by species of high trophic level to equilibrate with a change in the rate of contaminant input (Cairns and Parfitt 1980) will continue to hamper the intespretatican of many surveillance program data.

In general, the OC concentrations in open lake waters arc in the low part per trillion (ng/L) range. Such concentrations are difficult to sample and analyze, amd the data accuracy and precision are correspondingly low. Biomagnification and bisconcentration processes (for a discussion of their relative importance see, for example, Veith et al. 6 1979)) lead to OC concentrations in fish in the part per million (pglg) range which can be analyzed more accurately. Furthermore, the d a t i v e ease sf sampling and the importance of fish as a food source makes them practical indicators of OC contamination (Norstrom et al. 1978). In addition, many contaminants are very resistant to metabolism and elimination; therefore, both the totals body burdens and the concentrations of PCB and other compounds increase with weight and age of carnivores such as lake trout (Salvelinus nanlaycushj (Niinai 198 I ) . The same fact, however, makes it difficult to determine a change in the rate of contaminant input to a lake, as this change must be observed as a deviation from the expected concentration in the fish species. Attempts to bypass this problem of "background" contamination, for example, by the comparison of sequential years' fish of the same age or weight group have had limited success.

To overconae the noted difficulties in finding trends of contaminant concentrations in the ecosystem, I explored the possibility of using contaminant ratios and quotientsq' both within one species and between two food chain related species. Contaminant ratios had previously been used to describe either spatial or temporal trends. For example, Olsson et al. (1975) used DDElZDDT, DDDICDDT, and DDTIZDDT ratios to determine contamination gradients in northern pike (E.~ox lercius) from different parts of the Stockholm Archipelago. More frequently, contaminant ratios were based to determine changes over time (Neidermyer and Hickey 1976; Fleet and Plapp 1978) within one species. Ht seems logical then to compare such contaminant ratios of different species from the same location and time. The corn- parison of such intraspecies ratios by way of interspecies

"Fhe term '2ntraspecies ratio" (W) is used k r e for the mean of such ratios ( R - C,IC2) of two contaminant concentrations 4CI ,C2) of all specimens of the same species; i.e. sea lamprey (RL) or its lake whitefish host (RH). "Interspecies quotients" are obtained by division of the means d either contaminant concentrations 4Qc = CH/CLj or contaminant ratios (OR = WY/RL.) of the host species (CH,RH) by that of the parasitic lamprey (CI..RL).

quotients between a long-lived and a short-lived species of similar trophic level should provide information as to the trends in accumulation rates of different contaminants. Two species which appear most suited for such an investigation are the sea lamprey (Pe~ronpzon marinus) and its host, the lake whitefish (Corego~a~ss c*lupeaforrnbs). This pager describes the results on samples from Lake Huron.

Materials and Methods

Lake whitefish were caught with nets at depths between 10 and 30 rn in the northern parts of Lakes Huron and Michigan in the fall of 1978. The fish that had sea lamprey attached were selected, and both the whitefish and lamprey were frozen and shipped to this Institute. Upon thawing, the weight, length, sex, and visual appearance of each specimen were recorded (Table 1 ) . Each whitefish and each lamprey was then homogenized separately by repeated passage through a Hobart commercial meat grinder. Except for the eggs and sperm sf s o w of the whitefish, which were sepa- rated and homogenized with a Polytron blender, each specimen was ground without removal of any other part such as head or skin. Aliyuots of -50 g of each sample were frozen until the QC analysis by established methods (Chau and Sampson 1975).

Each lamprey and whitefish aliquot was analyzed for common arganochloriaae residues including PCB, DDT-type compounds, chlordane and dieldrin, and related OC pesticides. Arithmetic residue means and standard deviations of the means for each species and contaminant or contaminant group were calculated by common procedures (Davies and Goldsmith 1976). Likewise, the intraspecies residue ratios ( R ) are the means and standard deviations of the jintraspecimen residue concentrations each for the whitefish and lamprey groups. One-way analysis of variance tests for the statistical significance of differences of the residue concentrations (C) and the residue ratios ( R ) between the lamprey and whitefish groups were made. This analysis of variance procedure is well known to be robust for non-nomal data (Plackett 196$) and hence the interpretations are valid for a wide class of para- metric distribartioa~s.

Results and Discussion

Each of the whitefish and lamprey specimens investigated had residues of the common organochlorine contaminants, such as PCB, p.pl-DDE QDDE), p,pf-DDT (DDT), a-chlordane (@HA), y-chlordane (CHC), and dieldrin (HE0 j. Hn addition, o p '-DDT (DDO) , hexachlorobenaene (HCB), a-hexachlorocyclohexipppe (BHC), heptachlorepoxide (HEX), endrin ((END), amd p,pP-TDE were found in many of the samples, whereas Iindane and rnirex were absent. Table 2 gives the residue concentrations of the major contaminants for each specimen. Hn all cases, the concentpations of PCB were higher than those of any of the other contaminants determined. This is consistent with many other reports on OC residues in Great Lakes fish, including sea lamprey from Lake Ontario (Kaiser and Valdmanis 1978) and Lake Superior (unpublished data).

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KAISER: CONTAMINATION TRENDS FROM RESIDUE RATIOS

TABLE I . Sources and descriptions of the investigated Bake whitefish (Coregonus clupeaformis) and sea lamprey (Petromjzon murinus] specimens.

Date Weight, Length, No." ~oeat iora~ 1978 e cm Sex Remarks

South Baymouth

6.

Murphy's Harbour Murphy's Harbour Burnt Island Burnt Island Blind River Blind River Bailey's Harbour Bailey's Harbour

Sept. 25 Sept. 25 Sept. 22 Sept. 22 Segt. 30 Sept. 30 Sept. 26 Sepe. 26 Sept. P Sept. 8 Sept. 1 3 Sept. 13 Sept. 5 Sept. 5 Nov. 11 Nov. 1 1 Oct. 4 a t . 4 Sept. 6 Sept. 6 Oct. Oct.

50 hq One open scar 42 M 53 M One scar 49 )

5 0 F 46 M

7 M Owe scar 36 7

'? F Deep open scar 44 '?

7 M No scar 27 ? 64 F One scar 37 ? 57 F 46 ? 54 F 34 *? 55 F 47 F 53 F 42 M

"KI, whitefish; k, lamprey. bBailey's Harbour locaked in northern Lake Michigan; all others in northern Lake Huron.

TABK: 2. Qberved organochlorine contaminant concentrations of specimens listed in Table 1. All data in ~ g l k g , whale fish basis.

-

No. HCB" BHC HEX CHC CHA H E 0 END DBE DDO BDT PCB

"For codes, see text. 'Samples also contain trace amounts of TBE.

As seen from the data in Table 2 the contaminant concen- 180% (Table 3). In part, this results from the very high PCB trations vary considerably among the specimens of both the and XDDT concentrations in the lamprey specimen 46-L, the whitefish and lamprey groups. In particular, the relative stan- levels of which are nearly two orders s f magnitude above dnrd deviations for the means of the PCB. DDO, DBE, and those of the specimen 43-L (Table 2). As the concentrations 2DDT concentrations in the sea lamprey are in the order of in 46-E were reconfirmed by a duplicate analysis, there is no

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CAW. J . FISH. AQUAT. SCB., VOL. 39, 1982

TABLE 3. Contaminant concentration means and standard deviations of the Hake whitefish (C,) and sea lamprey 4CL) groups, probabilities that those means tare different at the level of significance (B) and the interspecies quotients (Qc) of the concentration means; means and standard deviations in g~g/kg.

Mean -t- standard deviation

Whitefish Lmprey Significance Quotient Contaminant 438 c, P Qc = CH!CL

PCB CDDT XCHLB DDT HCB BHC DDE XHEND DDO HEX

'nns = Not significant ( P > 0.05).

justification in rejecting that sample from the data set. Statis- tically, however, the levels of PCB and CDDT in the specimen are outliers (Gmbbs test. P < 0.02) with respect to the means of the PCB and ZDDT concentratisaas in this group of lamprey (Davies and Goldsmith B 976).

Table 3 shows the residue concentration means, standard deviations, and the levels of significance of the difference of the means between the two species, determined by one-way analysis of variance as described above. For convenience, certain contaaninants were grouped together, such as a- and y-chlordane to give CCHLD, dieldrin and endrin to give ZHEND, and DDE, DDO. and DBT to give ZDDT. Only the concentrations of HCB, BHC, DDT, DDO. CHEND, and HEX were found to be different between the two species at the 95% confidence level. No statistically significant differences exist between the residue means of the major contaminants, 2CHLD, CDDT, and PCB of the two species.

Also given in Table 3 are the interspecies quotients of the contaminant concentration means between the whitefish and lamprey groups (Qc = CHICL). The values of the quotients range from QpCB = 0.22 to -- 8.7 1, indicating substan- tial differences in contaminant accumulations between the two species. As noted before, those quotient values are tc~ be considered approximations only, as the means from which they are derived are quite uncertain as a result of the large standard deviations. For example, the means of the PCB concentrations of 504 and 2243 ~ g l k g in the whitefish and lamprey groups, respectively, show no statistically significant difference (ANOVA test, P > 0.85) even though the quotient of the means (Table 3) is considerably smaller than one. Therefore, no valid csnclusions as to the difference of contaminant accumulations can be drawn directly f r ~ m such concentrations. However, the quotients introduce the possibility that the sea lamprey could serve as an indicator species for contaminants in the Great Lakes region and possibly beyond.

The potential use sf sea lamprey as indicator species for OC contamination in the Great Lakes offers several advantages over other species. First, it is available from each of the Great

Lakes as well as from most areas of the eastern coast of North America, including the St. Lawrence River and important inland lakes such as the Finger Lakes (Scott and Crossman 1973). Also, lampreys we regularly caught as part of the ongoing Sea Lamprey Control Program under the auspices of the Great Lakes Fishery Commission. Lamprey are also an occasional by-product of the commercial fishing industry of little market value. Perhaps the most important advantage of using sea lamprey as indicator species is its fast growth and particularly its shofl adult life span compared to other fish of similar trophic level. Furthermore, because of its unique feeding habit, it appears possible to determine contaminant trends by con~paring residue levels in the lamprey and its long-lived host species.

In the Great Lakes, the sea lamprey is an external parasite of large fishes, particularly the salmonid and coregonid species (Famer and Beamish 1973; Lett and Beamish 1945). Laboratory studies on the adult lamprey showed its gross food conversion efficiency to average -40-50% (Farmer et al. 8975). It was also demonstrated that the lamprey lives almost entirely on the blood of the host fishes, with the intake of muscle tissue being less than 2% of the blood consumed (Farmer et al. 1975). Assuming an average weight of 250 g for the adult Banlprey and given a blood content of 3.13% of the host fish (Conte et al. 19631, the total weight of fish destroyed by one lamprey could be 20 kg. This is likely a conservative estimate as it assumes the ingestion of all the hosts' blood by the lamprey. Given an average weight of the teleost as -2 kg (Table I), it is apparent that a lamprey will feed on a minimum of 18 host fish before it reaches maturity.

The sea lamprey matures from the young adult stage, weighing only a few grams, to a spawning adult of -200- 400 g, and then to subsequent death, generally within 12 -28 mo (Crowe 1975). En contrast. the life span of the lake whitefish, lake trout, and other coInmon sea lamprey host species is in the order of 10- 15 yr (Scott and Crossman 1943).

During the annual period of growth, from spring to fall, the OC body burdens of fish are accumulated primarily from their diet. This has been shown for DDT and lake trout (Reinert et al. 1974), and is supported by field observations on the

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KAISER: CONTAMINATION TRENDS FROM RESIDUE RATIOS 5-75

correlation sf contaminant and fat levels in other species (Kelso and Frank 1974). From feeding experiments on channel catfish (Icbalunas puprcrarus), it is also known that the concentrations of PCB isomers in fish blood are about 10% of those in the total body (Wansen et 31. 1976). Therefore, in the growth period, the lamprey accumuHate contaminants from the hosts' blood which reflects the recent dietary exposure of the host specimens rather than the hosts' total body burdens. as might be the case in periods of lipid mobilization. Zoo- plankton, a major food item for lake whitefish (Scott and Crossman 19731, equilibrates very rapidly with contaminants in the water column (J . H. Carey, National Water Research Institute, Canada Centre for Inland Waters, Burlington, Ont. E7W 4A6, personal communication). Therefore, lamprey caught near the end of the annual growth cycle will have accumulated those contaminants that were present in the water body in the preceding spring and summer. Because of the small weight of the preparasitic or ammocoete phase of the lamprey, any contaminants accumulated during that phase contributc negligibly to that of the hIBy grown individual.

The unique lamprey-host relationship in terms of 8C contaminants is illustrated in an idealized model spanning 9 yr as shown in Fig. 1. As only the relative contaminant levels in the various compartments are of interest, only qualitative concentration values are given in the ordinate. The model shows a contaminant's concentration in lake water and the corresponding levels in the blood and tissues of a host and in the tissues of lampreys feeding on this host species. For the purpose of illustration, the life span of each lamprey generation is assumed to be exactly I yr and that of the host -9 yr. In this example, there is a medium contaminant concentration in the lake water at the beginning of year 1 and it remains so over a period of 3 years. Consequently, the host fish is exposed to a constant contaminant level in its food (not shown) which leads through the bioconcentration and biomagnification mechanisms to a constant concentration in its blood. The level in the blood determines the rate at which the host tissues accumulate the contaminant; for ease of illustration, an exactly linear function of exposure and time is assumed. In year 4, the contaminant concentration in the water is assumed to be -twice, and in the years 6, 8, and following, only one-half of that in the years 1-3. The changes in the contaminant concentrations in the water result in concurrent concentration changes of equal magnitude in the host blood, as shown. However, the contaminant concentration in the host tissues continues to rise above the level at the end of year 3 at rates of accumulation twice (year 4) or one-half (years 6, 8 - 10) of that of year 3. Therefore, the actual contaminant concentrations in the host tissues at the end of year 4 or year 8 is not much different from those expected if there had been no change of the contaminant concentration in the water, as shown by the broken lime in Fig. 1. This is a consequence of the "buffering" effect of the total body burden which the host has accumulated in the years prior to that of any change.

The contaminant concentrations in the tissues of the successive generations of sea lamprey are much more clearly related to those in the host blood and, of course, to those in the lake water. In Fig. 1, this is apparent from the levels in lamprey tissues of y e a 4, compared to that of year 8. As a new generation of sea lamprey appears each yeah, it suggests the

FIG. t . An illustrative model of contarninant concentrations in lake water, host blood, host tissue, and lamprey tissue vs. tinme.

sea lamprey to be a better indicator species than the comparatively Bong-lived coregonid and salmonid host species. However, differences in contaminant burdens between individual lamprey specimens are of a similar magnitude as those found in other groups of fish samples, and therefore attempts to determine trends in contamination from contaminant concentrations in lamprey co%Iections of successive years arere subject to the same problems as described earlier for other sumeillmce progams.

Further investigation of the model shown in Fig. I reveals that the interspecies quotients of the contaminant concentrations in the lamprey and host tissues are even more sensi- tive to changes in the lake water than the actual concentrations in lamprey tissues. This can be demonstrated in more detail by determining intraspecies contaminant ratios and their interspecies quotients.

For each of the whitefish and lamprey specimens, the ratios of the concentrations of each of the contaminant groups with each of ZDDT and PCB as denominators were calculated. The ratios were then grouped by species and the means and standard deviations of such intraspecies ratios are given in Table 4. The individual specimen ratios were further analyzed by one-way analysis of variance and the levels of significance of the differences between the lamprey and whitefish ratio means determined (also given in Table 4). With the exception of the DDEIPCB ratios, the means of the intraspecies contaminant ratios are different between the whitefish and lamprey groups at a level of significance of 99.9% or higher.

In analogy to the caIculations of interspecies quotients of the means of the contaminant concentrations ((Ic = CHICL), shown in Table 3, interspecies quotients (QR = RHIRL) were also calculated from the means of the intraspcies ratios BDEJZDDT, PCBJXDBT, etc., to yield the values given in Table 4. The values of these quotients of ratios with XDDT as denominator range from 0.48 to 5.7, and sf those with PCB

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CAN. B. RSH. AQUAT. SCI., VOL. 39, I982

TABLE 4. Means and standard deviations sf intraspecies contaminant ratios of the lake whitefish (RH) and sea lamprey ( R L ) groups, probabilities that t h e means are different at the Level sf significance ( P ) , and the interspecies quotients (ex) of the ratio means.

- - -

Mean + standard deviation

Contaminant Whitefish Lamprey Significance Quotient ratio RH WI- P QR = RHIRL

'ns = Not significant ( P > 0.1).

as denominator from 1.17 to 20.8. Accordingly, they have similar range factors (maximum divided by minimum value) of 84.3 and 17.8, respectively. In comparison, the values of the interspecies quotients of the contaminant concentrations (Table 3) range from 0.22 to 8,71 wlth the large range factor of 39.6. More impo~Tant, the quotients of the means of ratios (Table 4) are considerably more accurate than those of the means of concentrations (Table 3) as is evident from the considerably lower relative standard deviations of the former. This is even more clearly evident from the highly significant differences of the ratio means for all but the BDEIPCB ratios (Table 4) when compared to the means of concentrations (Table 3). In fact, all but the DDE/PCB ratios are different between the lamprey and whitefish groups at a confidence level of P = 0.001 or better.

Having so gained a much improved level of confidence from the wide range of contaminant concentrations, inclaading the highly contaminated lamprey specimen 46-L (Table 2), it is worthwhile to consider how such ratios can be used to determine contamination trends.

In order to visualize the dependence of interspecies quotients between host and lamprey on the intraspcies ratios of the contaminant concentrations, Fig. 2 illustrates the concentrations and ratios of two independent contaminants over time. Contaminant A is assumed to be at a constant concentration in the lake water over the entire period. As a result, the host fish accumulate this compound sat a constamt rate and all lamprey generations feeding on such telehssts accumulate A to equal tissue concentrations. Another contaminant. B, the solid line in Fig. 2, is assumed to have a fluctuating rate of input to the lake, exactly as shown for the contaminant in Fig. 1, with high levels in year 4 and low levels in the years 6, 8, and following. As shown before, the background concentrations of B in the host species result in only minor devi-

ations of its concentrations in the tissues of the host. There- fore, the intraspecies ratio of A/B in the host remains nearly constant at R - 1.0. In contrast, the same ratio of A/B for the lamprey changes strongly to become Re C 1.0 in year 4, and RL > 1.0 in year 6 or 8. If we now calculate the interspecies quotients of such ratios Q R = RNIRL. we find Q R ) 1.0 for year 4 and QR < 1.0 for year 6 or 8. This change in the value of Q is directly proportional to the change of the rate of input of contaminant B to the lake.

R,. .= 1.0 for ease of illustration (Fig. 2); for most actual cases the value of R will be different from 1. In contrast, the value of the interspecies quotient of the contaminant ratios (Q> will only be different from Q = B .O, if the values of RH and RL are different from each other. The calculation of the ratios We and RH can therefore be regarded as a normalization procedure, analogous to the use of an internal standard, a common technique in trace analysis. The validity of this concept is most strikingly demonstrated by the lamprey specimens 43-k and 46-L whose DDE and PCB concentrations differ by nearly two orders of magnitude while their residue ratios RL = DDEIPCB are almost identical wlth 0.22 and 0.33, respectively. Therefore, the contaminant concentrations of the specimen 46-L, otherwise to be disregarded as outlier, are also of value to the determination of contaminant ratio means and the interspecies quotients.

As the mean of the contaminant ratios of all specimens is of much higher precision than the mean sf the concentrations, the interspecies quotients of the r-atios (Table 4) are more precise than those derived from the concentrations, For example, for the lafanprey group for PCB/ZDDT, the value RL = 1.90 * 0.65 was found (Table 4). Calculated frona the means of concentrations, the value would be RL = 22431 1069 = 2.10 with an uncertain standard deviation. Consequei.mtly, also the interspecies quotient Q R = is of higher precision than Q? = CHIC&. This can further be demonstrated by correlating the values of the quotients of BBE, XCHLD, etc. with ZDBT as denominator with those for the

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KAISER: CONTAMINATION TRENDS FROM RESIDUE RATIOS 577

f lNTEHSPEClES QUOTIENT

, I

oLi-T-Tt I t 4-:rT- t 1, 7-L-v- T I M (yr)

FIG. 2. An illustrative model of intraspecies contaminant ratios in the host (RH) and lamprey (18,) of two contaminants (A, B) and the resulting interspecies contaminant quotients (OR = RHIRL.) VS. time.

same contaminants with PCB as denominator. For the six pairs of quo~ents given in Table 4, and a linear correlation, a correlation coefficient of R* = 0.97 is obtained.

In the Great Lakes, sea lamprey arc known to feed on several host species, most commonly on lake whitefish, lake trout, and coho salmon (Onc~srhynchus kisutch) (Farmer and Beamish 1973). Most of the lake whitefish specimens collected for this study had lamprey scars, some quite fresh and deep (Table I). It is likely, therefore, that at least some of the lamprey have actually fed on these whitefish. There is no guarantee, however, that lake whitefish were the only or the predominant teleosts of this group of lamprey prior to the catch. This raises the question as to the species dependence of contaminant uptake rates and possible contaminant interactions, all of which could affect the intraspecies contaminant ratios.

Three lake trout specimens, caught together with the whitefish and larnprey for this study. were also analyzed for their QC contaminants. Although their contaminant levels were higher than those of the whitefish, the intraspecies contaminant ratios were very similar for both species. The following values for the lake trout data were observed, with the corresponding values for the whitefish (from Table 4) in parentheses: PCB/xBDT: 0.83 (8.76); DDE/;'CDDT, 0.49 (8.41); BDT;'CDDT, 0.30 60.31). A similar comparison of PCB/ZDDT data for a total of 84 each of lake trout and lake

whitefish from nine locations in Lake Superior (International Joint Commission B977k) results in an interspcies quotient mean and standard deviation of 1 .OB iz 0.50, indicating identical ratios of the PCB and XDDT accumulation rates for both species. As a result, for the purpose of comparing the lamprey with its host, it does not matter on which of the two species the lamprey has fed on predominantly.

The interpretation of interspecies contaminant quotients also requires the understanding of species-dependent uptake rates and interactions of contaminants. The assumption made here is that the host species and the lamprey have constant but not necessarily equal ratios of uptake efficiencies for any pair of contaminants. It is known that concurrent exposure to dietary dieldrin and DDT increases the tissue storage of DBT in rainbow trout, compared to DDT by itself (Mayer et al. 1970). No such data are available for the sea lamprey, but it appears likely that both the directions and magnitudes of such contaminant interactions are the same for lamprey and host as similar effects have also been noted for rats exposed to dieldrin and DDT (Street and Blau 1966). As shown above for whitefish and lake trout, rates of contaminant uptake are generally higher in the latter, but the ratio of the two contaminants PCB and XDDT is the same, resulting in an interspecies quotient of I . Further support for the constancy of relative accumulation rates can be found in the linearity of the uptake rates of DDT and dieldrin by rainbow trout (Saho gairdjzeri) at various dietary exposures over long periods (Macek et a%. 1970). Therefore, the variation in uptake efficiency with the contaminant, the general trend being PCB > DDT > dieldrin > lindane (Addison 1976) is tin- likely to affect the intraspecies ratios of contaminants. Further evidence for this is available from a number of laboratory and field investigations. For example, the ratios of TDE to BDMU when determined 19 years after exposure to TDE were essentially the same for all fish species (Cairns and Parfitt l980), and constant dieldriniDDT elimination ratios were observed for bluegill (Lepomis macrochirus) and gold- fish (Carassius aurotus) exposed in flow-through aquaria (Gakstatter and Weiss 1967).

With the knowledge of constant interspecies quotients under equal exposure conditions, it is of interest to interpret the range of values actually observed (Table 4) for the sea lamprey and lake whitefish specimens.

As seen from the data in Table 4, the values of the interspecies quotients Q vary considerably with the contaminants in the numerators. Hn principle, it would be of interest to calculate the ratios and interspecies quotients with each of the observed contaminants as numerator and denominator. Wow- ever, this would be impractical and unnecessary. In most situations it will suffice to compute the quotients of the ratios with the two most abundant contaminants or groups as denominators only, BDT and PCB in this case. As seen from Table 4, the interspcies quotients Q vary by a factor of - 10 for each of the two denominators. It is also seen that the sequence of increasing quotient values is the same for each denominator. This constancy of the sequence indicates that within each species, whitefish and lamprey, the abundance of each contaminant relative to XDDT and PCB is constant. In

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578 CAN. J . FISH. AQUAT. SCI., VOL. 39, 1982

contrast, the relative abundance of a contaminant between the two species varies with the value of its quotient. This becomes mare evident after a transformation of such quotients (Q) . For example, the quotient Q of contaminant A with CBDT as denominator can be expressed by the general formula:

where the value of the constant (c) depends on the ratio 2BDTH/XDDTL. It follows that for a series of contaminants (A, , AZ,. . . .AD), low (high) values of Q, are the results of high (low) concentrations of A in the lamprey relative to those in the host fish. With the previous example, A, = DDE and Q, = 0.51, and with A2 = 2HEND and Qz = 4.46 (Table 4), it is evident that the concentration of DBE is much higher and that of ZMEND much lower in the lamprey compared to the respective DDE and CHEND concentrations in the whitefish. Analogous conclusions can be drawn for each of the other contaminmts listed in Table 4. The combination of these comparisons results in a sequence of decreasing contaminant concentrations in lamprey relative to whitefish. This sequence is PCB > DBE >> DDT > ZCHLD > ZHEND > HEX > BDO. As the quotients for both PCB and DDE are less than unity and all other quotients greater, it can also be concluded that there are higher concentrations of PCB and DDE in the lamprey than in the whitefish and lower concentrations of the other contaminants.

Now, to determine which of the contaminants is increasing or decreasing in the lake, it is necessary to know the exact value of the above-used constant c = C D D T ~ I ~ D D T , ~ which is the interspecies quotient of the mean CDDT concentrations of the two species. The value of this quotient, 0.64, in Table 3 is derived from the set of lamprey data including the statistically outlying concentrations of the specimen 46-L. For present purposes, this specimen is to be excluded from the data resulting in a new mean ZDDT concentration of 600 2 320 yglkg for the lamprey. This value is close to that of the whitefish and therefore the value for the constant is,close to 2 . Hence it is concluded that of the above- noted sequence of contaminants, both PCB and DDE show increasing trends, all others decreasing trends. Such results for Lake Huron (in 1978) are both expected and unexpected. The decreasing trend of DDT, for example, appears reason- able in view of the ban on this insecticide and is also indicated from other data. Hn contrast, the stepwise reduction of the use of PCB has yet to lead to a reduction of its abundance in the aquatic ecosystem. In fact, an increased loading, possibly through atmospheric input, is indicated.

At present, trends of contaminant levels in the Great Lakes are determined from the change of residue concentrations in fish over several years. Because of the large variations of concentrations among the samples, great efforts in sample collection and analysis must be expended to obtain accurate means with low standard deviations. Even then, small changes in cogltaminatisn levels are difficult to recognize. and the degree of confidence remains low. The cause of this

problem lies in the large "background" levels of contaminants in the larger and older fish. Any change of the rate of accumulation is difficult to ascertain against this background.

This study demonstrates a significant gain in the accuracy of the determination of contaminant abundance by the calcu- Bations of intraspecies contaminant ratios for each specimen. Such ratios are analogous to the use of internal standards, a common procedure in the field of quantitative trace analysis. This increase in acctaracy strongly reduces the number of samples required.

This study also shows the usefuIwess of the inherspecies contaminant quotients between sea lamprey anki host species for an immediate recognition of recent trends in contaminant levels. The basis for this is the unique lamprey-host relationship and also the comparatively short life spans of the adult lamprey. The combination of this principle of interspecies quotients of contaminamts in host and lamprey, together with the principle of intraspecies ratios could significantly reduce the need for, and cost of, present surveillance programs for persistent organochlorine contaminants in the Great Lakes.

Acknowledgments

I am thankful to Mr John Novak, Dr J. J . Tibbles, Dr J . Kitchill, and Dr A. Niimi for their efforts to provide fish and lamprey samples; to Mr John Coburn for the organochlorine residue analyses; to Drs A. Niimi, A. El-Shaarawi, and W. M. J . Strachan for helpful discussions and advice on the interpretation of the results. I also thank the refer- ees, particularly Dr It. F. Addison. who, without agreeing in all aspats with my interpretation of the data, supported the pubiication of this article by very detailed, constmctive criticisms of its earlier versions.

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early trend determination of organochlorine contamination from residue ratios in the sea lamprey (...

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