Arch. nvirn. Cntam. Txicl. 27, 82-87 (1994) ARO HIV S OF nvirnmental Cntaminatin a n d Txiclgy 1994 Springer-Verlag New Yeck Inc. Organchlrine Cntaminant Cncentratins in ggs and Their Relatinship t Bdy Size, and Clutch Characteristics f the Female Cmmn Snapping Turtle (Chelydra serpentina serpentina) in Lake Ontari, Canada C. A. Bishp, G. P. Brwn, R. J. Brks, D. R. S. Lean, J. H. Carey nvirnment Canada, Canadian Wildlife Service (Ontari), Bx 5050, Burlingtn, Ontari, L7R 4A6, Canada Received: 17 September 1993/Revised: 27 December 1993 Abstract. Statistical analyses were used t determine relatinships between bdy size, clutch size and mass, and relative clutch mass and levels f rganchlrine pesticides and seven plychlrinated biphenyl cngeners in the eggs f adult female cmmn snapping turtles (Chelydra serpentina serpentina). N significant crrelatins were fund between bdy size (bdy mass, carapace length, carapace width, plastrn length) and lipid nrmalized cncentratins f p,p'-dd, mirex, dieldrin, and plychlrinated biphenyl (PCB) cngeners (IUPAC): #52, #105, #118, #138, #153, #180, #194, and the sum cncentratin f thse cngeners. Small sample size and clumping f data arund the mde f the bdy size values prevented inferences f nnlinear relatinships. It was cncluded that bdy size and clutch characteristics are nt strng r reliable predictrs f the level f cntaminants in snapping turtle eggs and that adjustment fr thse parameters wuld nt reduce variatin in cntaminant levels amng clutches. Other variables such as individual fd preferences and/r fraging activities are mre likely t cause variatin in chemical cncentratins amng clutches f eggs within a ppulatin. In rder t reduce interclutch variatin in cntaminant levels t 38.6-55.9% in snapping turtles, sample sizes f at least 15 clutches per site are recmmended. mn snapping turtle (Chelydra serpentina serpentina), bdy mass, clutch size, and clutch mass can vary greatly amng females within ppulatins (Cngdn et al. 1987), and relatinships have been fund in this species between bdy mass and plychlrinated biphenyl (PCBs) and rganchlrine pesticide cncentratins in liver (Hebert et al. 1993) and PCBs in fat (Bishp 1990). The strength f thse relatinships increases with higher hydrphbicity f chemicals (Hebert et al. 1993). Relatinships between snapping turtle size and cncentratins f plychlrinated dibenzfurans and dixins in their fat have als been suggested (Ryan et al. 1986). Statistical cmparisns within snapping turtle ppulatins find that rganchlrine cncentratins amng clutches can be highly variable (Bishp et al. 1991; Struger et al. 1993); hwever, the effect f bdy size, age, and clutch characteristics n variatin in cntaminant levels in their eggs has nt been previusly studied. The hypthesis tested was that in a single snapping turtle ppulatin the eggs frm larger, lder female turtles with the largest clutch size and/r mass wuld cntain the highest cncentratins f plychlrinated biphenyls and rganchlrine pesticides. These results will be imprtant fr interpretatin f gegraphic and tempral trends f persistent chemicals in the eggs f this species. Cncentratins f lipphilic envirnmental cntaminants are strngly influenced by bdy size and age in mammals (Drescher et al. 1977; Gaskin et al. 1979; Dentn 1980; Hnda et al. 1983) and fish (Yungs et al. 1972; Sctt and Armstrng 1972). Such relatinships in lake trut (Salvelinus namaycush), ch salmn (Oncrhynchus kisutch), and walleye (Stizstedin vitreum) in the Great Lakes necessitate the cllectin f a single age r size class f fish fr the study f gegraphic and tempral variatin in rganchlrine cncentratins (Baumann and Whittle 1988; Brgmann and Whittle 1991). In the cm- Crrespndence t: C.A. Bishp Methds In 1990, snapping turtle eggs were cllected fr chemical analysis immediately after vipsitin frm 15 nests. Nests were lcated n the shres f Ctes Paradise, a wetland at the extreme western end f Hamiltn Harbur in Ontari, Canada [43 45'N, 78 7'W; see als Struger et al. (1993) and Bishp et al. (I991) fr map and descriptin f Ctes Paradise]. Bdy mass, clutch size and mass, carapace length and width, and plastrn length were measured in the 15 female turtles. Due t the lack f significant variatin in cntaminant levels amng eggs in snapping turtle clutches (Bishp 1990), eggs fr chemical analysis were cllected frm each clutch using the fllwing prtcl: A five-egg sample was taken that included ne f the first five eggs and ne f the last five eggs vipsited and
Organchlrine Cntaminants in Turtle ggs 83 Table 1. Spearman rank crrelatin cefficients between bdy-clutch size measurements and PCB and rganchlrine cncentratins in eggs frm 15 cmmn snapping turtles a % Lipid 0.08 DD -0.29 Mirex 0.007 Dieldrin -0.14 PCB #52-0.19 PCB #105-0.25 PCB #118-0.15 PCB #138-0.13 PCB #153-0.19 PCB #180-0.17 PCB #194-0.28 Ttal PCB -0.19 Bdy mass 1.0 Carapace length 0.91 Carapace width 0.88 Plastrn length 0.91 Clutch size 0.77 Clutch mass 0.77 ap < 0.05 Relative Bdy Carapace Carapace Plastrn Clutch Clutch clutch mass length width length size mass mass 0.10 0.25 0.11 0.003 --0.158 --0.29 --0.23 --0.22 --0.008 --0.26 --0.03 0.004 0.10 0.36 0.12 --0.14 --0.22 --0.21 --0.11 --0.38 --0.33 --0.26 --0.32 --0.54 --0.29 --0.17 --0.05 --0.03 0.15 --0.12 --0.14 --0.03 --0.03 0.08 --0.03 --0.16 --0.04 --0.08 0.06 --0.13 --0.16 --0.09 --0.06 0.16 --0.05 --0.18 --0.13 --0.17 0.04 --0.1 --0.14 --0.13 --0.13 0.12 0.0 --0.15 --0.06 --0.08 0.12 --0.09 1.0 0.88 1.0 0.85 0.93 1.0 0.72 0.79 0.79 1.0 0.81 0.78 0.78 0.93 1.0 --0.54 --0.15 --0.12 --0.52 --0.41 --0.25 --0.36 --0.25 --0.18 --0.09 0.06 --0.24 three ther eggs arbitrarily selected frm the clutch that were nt any f the first r last five eggs laid. All eggs were cllected by hand. The cntents f the eggs were pled by clutch and stred at -20 C within 12 h f field cllectin. Dental casts f carapacial scutes f all females were made, and, where pssible, the age f each female was determined (Galbraith et al. 1986). Relative clutch mass (RCM) was calculated fr 12 females as the prprtin f clutch mass t bdy mass. Relative clutch mass is an indicatin f the relative amunt f energy female turtles allcate t prduce a clutch f eggs (Iversn and Smith 1993). Using the methd f Nrstrm and Wn (1985), lipid cncentratin and the fllwing rganchlrine cmpunds were measured in eggs: p,p'-dd, mirex, dieldrin, and PCB cngeners (IUPAC Nmenclature): #52, #105, #118, #138, #153, # 180, # 194 (Ballschmiter and Zell 1980). Sum cncentratin f thse PCB cngeners is referred t as Ttal PCB in the fllwing text. Thse cngeners are representative f an increasing range f lg ctanl:water partitin cefficients (Kw) frm 5.84 (PCB #52) t 7.80 (PCB #194) (Hawker and Cnnell 1988). Briefly, analytical methdlgy invlved dehydratin f egg hmgenates by grinding with a 6:1 excess f anhydrus sdium sulfate and extracted with hexane in a clumn. The extract was cleaned up and separated int three fractins by Flrisil chrmatgraphy. The fractins were analyzed by gas chrmatgraphy-electrn capture detectr, using a 60-m DB-5 capillary clumn (Supelc Inc.). Fractin 1 cntained PCBs, p,p'-dd, hexachlrbenzene (HCB), pentachlrbenzene (QCB), 1234-tetrachlrbenzene (1234- TeCB), 1235/1245-tetrachlrbenzene (1235/1245-TeCB), and mirex. Fractin 2 cntained cis-chlrdane, xychlrdane, trans-nnachlr, and beta-hexachlrcyclhexane (b-hch). Fractin 3 cntained dieldrin. Recveries f thse cmpunds in this methd range frm 82% t 94% (Nrstrm and Wn 1985). Detectin limits were 0.005 mg/kg fr rganchlrine pesticides and 0.0025 mg/kg fr PCBs. Bdy and clutch measurements and lipid weight cncentratins (mg/kg wet weight/% lipid) f each chemical were tested fr nrmality, and all were fund t be nrmally distributed except PCB #52. Simple linear and Spearman rank crrelatin cefficients, and regressins were determined fr each cmbinatin f variables. Residuals and scatter plts f values and Spearman ranks were visually examined fr indicatins f nnlinear relatinships. Multiple regressin analyses were then carried ut with each chemical as the dependent variable and bdy r clutch size measurements as the independent variable. Maximum r 2 values were determined fr each variable mdel. All statistical analysis was perfrmed using CMS/SAS and statistical tests were determined as described in Skal and Rlhf (1981). Results Bdy mass ranged frm 2.6 t 8.1 kg, clutch size ranged frm 28 t 57 eggs with clutch masses between 285 t 745 g (Appendix 1). Age ranged frm 7 t 50 years amng the eight females fr which age culd be determined. There was a significant and psitive crrelatin amng bdy and clutch measurements (Table 1). Crrelatin cefficients fr fur variables (carapace length and width, plastrn length and bdy mass) in linear regressin mdels varied frm 0.06 t 0.24. The cefficient f variatin in rganchlrine cncentratins amng clutches ranged frm 38.6% t 55.9% (Appendix 1). Lipid nrmalized chemical cncentratins were als significantly psitively crrelated with ne anther with the fllwing exceptins: PCB #52 was nt significantly crrelated with any ther cmpund and p,p'-dd was nt crrelated with dieldfin. Bdy and clutch size measurements were nt significantly crrelated with any chemical levels in eggs (Table 1; Figure 1)
84 C.A. Bishp et al. "i am k g t~ g lo,= -~ p,p'-dd Mirex m. ~ 2~ 10,, " p,p'-dd Mirex Dieldrin Dieldrin ~ 0.1 0.1 0 0.01 I I [ I I I I L I I I 2.5 3 3.5 4 4.5 5 5.5 6 6.5 77.58 Bdy Mass (kg) (A) O.Ol I I I I I I I I I J 22 23 24 25 26 27 28 29 30 31 32 33 Carpace Length (cm) (B) '5.._. g lo e- ~ t I m ~bk p,p'-dd Mirex Dieldrin.g c lo 1 ~ p,p'-dd Mirex ~< Dieldrin 0 0 ~K > 0.t I I [ I I I I I I 270 320 370 420 470 520 570 620 670 720 Clutch Mass (g) (c).1 I [ I I I I I I I I I 6.9 7.4 7.9 8,4 8.9 9,4 9.9 10,410,911.411.912.412,9 Relative Clutch Mass (% f bdy mass) (D) Fig. 1. Bdy mass (A), carapace length (B), clutch mass (C), and relative clutch mass (D) f 15 female snapping turtles and rganchlrine cncentratins in their eggs but crrelatin cefficients generally indicated weakly negative relatinships between bdy size and chemical (Table 1; Figure 1). Carapace lengths ranged frm 22.2 t 32.7 cm, but 80% f the sample lie between 25 and 30 cm. The slightly negative crrelatins amng many bdy and clutch parameters and cntaminant cncentratins (Table 1) result frm relatively high cntaminant levels in eggs f a single, small female (bdy mass = 2.6 kg). The distributin f residuals, data, and ranks did nt suggest an bvius nnlinear relatinship. Multiple regressin analysis did nt reveal significant relatinships between any chemical cncentratins in eggs and bdy and clutch size measures, and maximum r 2 values were cnsistently lw and nn-significant (Table 2). The independent variables in the multiple regressin analyses were highly crrelated with ne anther, and thus additin f several different measures f bdy size t the mdel did little t imprve the fit. Age estimates were pssible fr nly eight females, and, due t the large expected errr in estimates, thse data were nt included in the analysis. Hwever, fr this sample f females, Table 2. r 2 and p values fr multiple regressin mdels f bdy size and clutch size n cntaminant levels in cmmn snapping turtle eggs r 2 p r 2 p (mass, CL,CW,PL)" (clutch size, RCM) b DD 0.238 0.56 0.001 0.99 Mirex 0.106 0.87 0.234 0.35 Dieldrin 0.065 0.95 0.258 0.93 PCB #52 c PCB #105 0.075 0.93 0.091 0.68 PCB #118 0.069 0.94 0.062 0.77 PCB #138 0.114 0.86 0.017 0.93 PCB #153 0.01 0.89 0.009 0.96 PCB #180 0.115 0.86 0.002 0.99 PCB #194 0.104 0.88 0.005 0.98 Ttal PCB 0.098 0.89 0.015 0.94 amass = bdy mass; CL = carapace length; CW = carapace width; PL = plastrn length brcm = relative clutch mass cpcb #52 is nt nrmally distributed
Organchlrine Cntaminants in Turtle ggs 85 estimated age appears t generally cincide with the trends in bdy size and suggests that a significant crrelatin between age and rganchlrine levels wuld nt be expected. Discussin The hypthesis that larger, lder turtles r thse with highest clutch size, mass, r relative clutch mass wuld prduce eggs that are mst cntaminated with rganchlrine cntaminants is nt supprted. Alternately, eclgical r physilgical parameters such as individual variatin in feeding lcatins, and/r fd preferences and metablism may be pssible determinants f variability in cntaminant levels amng clutches. In an mnivrus species such as the snapping turtle, feeding lcatin and preferences may mre greatly influence cntaminent accumulatin, and, in the case f Ctes Paradise, fd preference wuld be a mre likely factr. Ctes Paradise has relatively lw sediment cntaminatin (Sernkin and McLarty 1976) whereas certain areas f Hamiltn Harbur, t which Ctes Paradise is directly cnnected, cntain sediments and bita highly cntaminated with trace metals, PCBs, and plyarmatic hydrcarbns (Harlw and Hdsn 1988). xpsure t cntaminants might be highly variable amng female turtles if differences in fraging lcatins ccurred. Fr example, amng clnial-nesting great blue herns (Ardea herdia), differences in fraging lcatins fr individual females, rather than fd preferences r wintering areas, are thught t determine variatin in rganchlrine cntaminant levels fund amng clutches frm the same clny (llitt et al. 1992; Harfenist et al. 1993). Hwever, fr snapping turtles in Ctes Paradise during 1990-1992, raditelemetry studies f the 15 female snapping turtles examined in this study fund that the maximum distance travelled by any female frm the nesting site was 2,020 m and hme ranges were 0.1-28.4 ha in size. Nne f the female turtles left Ctes Paradise n any ccasin during the 2-year study (Bishp, unpublished data). Therefre, all female turtles in the study were expsed t similarly lw levels f sediment cntaminatin within their fraging area. If distance mved represents greater fraging and prey capture rates, certain females may cnsume mre fd and thus accumulate higher cntaminant levels in their tissues; hwever, we cannt cnfirm that increased mvement necessarily crrelates with higher fd cnsumptin. Snapping turtles are mnivrus, but studies f different ppulatins shw that their diet is apprximately ne-third fish, ne-third plant material, and ne-third miscellaneus items including amphibians, crnstacea, mllusca, birds, bird eggs, sediment, and refuse (Alexander 1943; Culter 1957). Many f thse fd items are knwn t biaccumulate rganchlrine chemicals (Greichus et al. 1973; MacDnald and Metcalfe 1989; Metcalfe and Charltn 1990). If distinct differences in fd preferences amng individual snapping turtles ccurs within a ppulatin, thse snapping turtles that fed mre heavily upn fish in Ctes Paradise culd be expsed t higher persistent cntaminant levels in their fd than female turtles that, fr example, chse plants and invertebrates, which wuld generally cntain relatively lwer rganchlrine cncentratins relative t fish. At present, there are n diet studies f this nature t cnfirm r refute this pssibility. Significant relatinships ccur between bdy size and cncentratins f lipphilic cmpunds in fat r liver in adult snapping turtles; the lack f such relatinships fr eggs suggests that levels f chlrinated hydrcarbns in the bdy tissues are accumulated prgressively with size and age, whereas cntaminant levels in eggs are nt. Thse differences cincide with patterns f accumulatin and relatinships between bdy mass and cntaminant levels in tissues and eggs in birds and fish. In female herring gulls, endgenus fat reserves are nt an imprtant surce f energy fr egg prductin; rather, diet just prir t egg-laying is the main surce (Rudybush et al. 1979; Nrstrm et al. 1986a). There is n evidence that any winter fat is still stred when breeding begins, and fat accumulatin prir t ylk frmatin is prbably nt necessary since egg weight relative t bdy weight is nly 25%; thus energy requirement fr egg prductin is a mdest demand in the annual energy budget fr herring gulls (Nrstrm et al. 1986a). ggs accunt fr nly 12% f the annual excretin f p,p'-dd in herring gulls (Nrstrm et al. 1986b). In Adelie penguin (Pygscelis adeliae), the transfer rate f female ttal bdy burden t clutch is nly 4% fr bth PCBs and p,p'-dd (Tanabe et al. 1986). In rainbw trut (Salm gairdneri), where clutch mass relative t bdy mass is 13.6% (Nimi 1983), mass f visceral and perirbital fat des nt decline during egg prductin when abundant fd is available and nly 10-15% f the ttal bdy burden f 2,2', 5,5'-tetrachlrbiphenyl (PCB # 52) is excreted via eggs (Guiney et al. 1979). As much as 40% f PCB #52 remains in rainbw trut after spawning (Guiney et al. 1979). In snapping turtles frm Ctes Paradise, clutch mass accunted fr nly 6.95-13.0% f bdy mass f females. The energy required fr egg prductin in snapping turtles is diluted because varian fllicle enlargement ccurs ver a 5-mnth perid, and prductin f shelled eggs requires anther several weeks (White and Murphy 1973). With such a small percentage f turtle bdy mass and energy required t prduce eggs, and the annual energy requirements f ecttherms being generally much lwer than fr birds (Spellerberg 1982), it is prbable that lipids fr snapping turtle eggs, and cnsequently lipphilic cntaminants in eggs, are derived frm daily dietary intake just prir t egg prductin as in sme birds and fish, rather than utilizatin f stred fats. Thus, it is nt surprising that cncentratins f rganchlrines in snapping turtle eggs are nt strngly crrelated with size and clutch characteristics f the female snapping turtle, while cncentratins in bdy tissues increase as the turtle ages. The results f this study shw that adjustments fr bdyclutch characteristics f female snapping turtles during egg cllectin r statistical analysis f the cntaminant data will nt reduce variability in rganchlrine levels in eggs. Cefficients f variatin f chlrinated hydrcarbn cncentratins in snapping turtle eggs have been reprted as high as 137% when sample sizes ranged frm five t ten clutches (Struger et al. 1993). Amng 15 clutches in the present study, we fund cefficients f variatin ranging frm 38.6% t 55.9%. That level f variatin is cnsistent with thse fund fr ther species used as chemical bimnitrs in the Great Lakes such as herring gull eggs [calculated frm Weselh et al. (1979); N = 10-13/sample site], Atlantic puffin (Fratercula arctica), Leach's Petrel (Oceandrma leucrha) [Gilbertsn et al. (1987); N = 5/sample site fr each species], and spttail shiners (Ntrpis hudsnius) [calculated frm Suns et al. (1991); N = 6-10/sample site]. In cntrast, cefficients f variatin f less than 15% are reprted fr fish used fr bimnitring such as lake trut and rainbw smelt (Osmerus mrdax) (N = 12-
86 C.A. Bishp et al. Appendix 1, Summary statistics f bdy mass (kg) and size (cm), clutch size and mass (g), relative clutch mass and rganchlrine cncentratins (mg/kg lipid weight) in eggs a Standard Cefficient f Minimum Maximum Mean deviatin variatin Bdy mass 2.6 8.1 5.3 1.5 27.7 Carapace length 22.2 32.7 28.1 2.6 9.4 Carapace width 20.3 27.2 24.2 1.8 7.5 Plastrn length 18.4 25.2 21.7 1.9 8.7 Clutch size 28.0 57.0 43.1 8.0 18.6 Clutch mass 275.0 745.0 477.0 146.6 30.7 Relative clutch mass 6.95 13.0 9.6 1.7 17.7 % Lipid 4.2 9.4 6.0 1.3 21.4 DD 1.0 14.9 5.9 3.3 55.9 Mirex 1.4 2.7 1.4 0.71 50.7 Dieldrin 0.09 0.8 0.49 0.2 40.8 PCB #52 0.01 0.04 0.02 0.01 50.0 PCB #105 0.47 2.9 1.7 0.7 41.1 PCB #118 2.1 11.7 7.3 2.8 38.6 PCB #138 2.0 16.2 9.3 3.7 39.7 PCB #153 2.5 16.2 9.3 3.7 39.7 PCB #180 1.3 1.3 6.4 3.0 46.8 PCB # 194 0.17 1.2 0.61 0.29 47.5 Ttal PCB 13.3 96.4 54.3 22.3 41.1 an = 15 in all samples except relative clutch mass utput fr which N = 12 98/sample site) (calculated frm Whittle and Fitzsimns 1983), in which adjustment fr size and age is made. Therefre, it appears that by cllecting samples frm 15 clutches f turtle eggs per site, we can expect that cmmn snapping turtle eggs can be used as integratrs f cntaminatin n an annual basis in wetland ecsystems with variability cmparable t that ccuring in clnial waterbird eggs and yung-f-the-year minnws but higher than that in smelt and trut frm the Great Lakes. Acknwledgments. We thank the Ryal Btanical Gardens and Mr. Len Simser fr their cperatin, and Barbara Trumper fr field assistance. We als appreciate the careful review and cmments f D. V. Weselh and Jhn llitt n an earlier versin f the manuscript. References Alexander MM (1943) Fd habits f the snapping turtle in Cnnecticut. J Wildl Mgmt 7:278-282 Baumann PC, Whittle DM (1988) The status f selected rganics in the Laurentian Great Lakes: An verview f DDT, PCBs, dixins, furans, and armatic hydrcarbns. Aquat Txicl 11:241-257 Ballschmiter K, Zell M (1980) Analysis f plychlrinated biphenyls (PCBs) by glass capillary chrmatagraphy. Fresenius Z Anal Chem 302:20-31 Bishp CA, Brks RJ, Carey JH, Ng P, Nrstrm RJ and Lean DRS (1991) The case fr a cause-effect linkage between envirnmental cntaminatin and develpment in eggs f the cmmn snapping turtle (Chelydra serpentina) frm Ontari, Canada. J Txicl nvirn Hlth 33:521-547 Bishp CA (1990) The snapping turtle (Chelydra s. serpentina) as an indicatr f rganchlrine cntaminatin in wetlands. MSc thesis, Yrk University, Nrth Yrk, Ontari, Canada Brgmann U, Whittle DM (1991 ) Cntaminant cncentratin trends in Lake Ontari Lake Trut (Salvelinus namaycush): 1977 t 1988. J Great Lakes Res 17:368-381 Cngdn JD, Brettenbach G1, Van Lben Sels RC, Tinkle DW (1987) Reprductin and nesting eclgy f snapping turtles (Chelydra serpentina) in sutheastern Michigan. Herpetlgica 43:39-54 Culter M (1957) Predatin by snapping turtles upn aquatic birds in Maine marshes. J Wild Man 20:17-21 Dentn GRW, Marsh G, Heinshn G, Burdn-Jnew C (1980) The unusual metal status f the Dugng (Dugng dugn). Mar Bil 57:201-219 Drescher H, Harms U, Huschenbeth (1977) Organchlrines and heavy metals in the harbur seal (Phca vitulina) frm the German Nrth Sea Cast. Mar Bi141:99-106 llitt J, Whitehead P, Nrstrm RJ, Sandersn JT, Hart L, Cheng K, Bellward GD (1992) Mnitring bilgical effects f dixin expsure in Great Blue Hern embrys. Annual meeting f Sciety f nvirnmental Txiclgy and Chemistry, Abstract 581, p 133 Galbraith DA (1986) Age estimates, survival, grwth and maturity f female Cheyldra serpentina Linnaeus in Algnquin Prvincial Park, Ontari. MSc. thesis, University f Guelph, Ontari, Canada Gaskin D, Stnefietd KI, Suda P, Frank R (1979) Changes in mercury levels in Harbr prpises frm the Bay f Fundy, Canada and adjacent waters during 1960-1977. Arch nvirn Cntam Txicl 8:733-762 Gilbertsn M, llitt J, Peakall DB (1987) Seabirds as indicatrs f marine pllutin. In: Diamnd AW and Filin FL (eds) The value f birds. Technical Publicatin N. 6. ICBP, pp 231-248 Greichus YA, Greichus A, merick RJ (1973) Insecticides, plychlrinated biphenyls and mercury in wild crmrants, pelicans, their eggs, fd and envirnment. Bull nvirn Cntam Txicl 9:321-328 Guiney PD, Petersn R, Melancn MJ, Lech JJ (1979) ffects f egg and sperm maturatin and spawning n the distributin and eliminatin f a plychlrinated biphenyl in rainbw trut (Salm gairdneri). Txicl Appl Pharm 47:261-272 Harfenist A, Whitehead P, Cretney WJ, llitt J (1993) Fd chain surces f plychlrinated dixins and furans t Great Blue Herns (Ardea herdia) fraging in the Fraser River stuary, British Clumbia. Technical Reprt Series N. 169. Cfinadian Wildlife Service
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