AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS, VOL. 3, 43-5 I (1993)

PCBs and organochlorine pesticide residues in otter (Lutra lutra) spraints from Welsh catchments and their significance to otter conservation strategies

C. F. MASON and S . M. MACDONALD Department of Biology, University of Essex, Wivenhoe Park, Colchester C04 3SQ, UK

ABSTRACT

1. A survey is presented of PCB and organochlorine pesticide concentrations in otter (Lutra lutra) spraints (faeces) from 18 catchments/sub-catchments in Wales and adjacent English counties.

2. There were wide differences in concentrations of lindane, dieldrin, DDE and PCBs between catchments and at sites within catchments. Only PCBs were considered likely to be of significance in influencing otter populations. Mean PCB concentrations (but not those of dieldrin and DDE) were inversely related to otter population performance (as measured by both catchment distribution and sprinting intensity) between catchments.

3. It is suggested that PCB contamination is exerting a negative impact on otter populations in four catchments, while there is concern over four others. A study of food chain contamination should be an essential compunent of otter conservation strategies at both the national and local level.

INTRODUCTION

Otter (Lutra lutra) populations began a steep decline over much of Britain in the late 1950s and by the time the first field survey of Wales was conducted in the 1970% signs of the species were found at only 20% of 1030 sites (Crawford et al., 1979). When the survey was repeated 7 years later some expansion in otter distribution was recorded (Andrews and Crawford, 1986), a finding consistent with similar range increases noted on the English/Welsh borders and in south-west England by Strachan et al. (1990). However, despite the improvement in Wales by the 1980s, some regions still lacked otters (e.g. Mid Glamorgan), while certain catchments (e.g. the Usk) showed limited evidence of otter activity despite having good habitat and fish stocks.

The gradual increase in otter range, both within Wales and in the Border Counties, has continued into the 1990s but there appear to be regional variations in the success of consolidation of expanding populations. On the River Severn, for example, the species was largely confined to the upper stretches above Welshpool in the early 1980s but there was evidence of animals downstream to Worcester by 1992 (Mason and Macdonald, in press). This extension into the English lowlands does seem, however, to be tentative in view of the potential for recruitment from the upper reaches. By contrast, recolonization of upland Welsh rivers, like the Lugg (a tributary of the Wye), has been rapid and successful (Mason and Macdonald, in press). The current pattern of otter distribution in Wales and the regional variations in expansion suggest that local contamination of the aquatic food chain may be affecting the success of population recovery.

1052-7613/93/010043-09$09.00 01993 by John Wiley & Sons, Ltd.

43

Received 14 September 1992 Accepted 10 November 1992

44 C. F. MASON AND S. M. MACDONALD

The present study investigates the possible role of organochlorine contamination in determining current otter distribution. Since relatively few tissues become available for analysis, organochlorine levels are determined in otter spraints (faeces), which can be collected both easily and over large areas. They provide a non-destructive method of monitoring OC residues in aquatic environments since burdens in otter spraints reflect levels impacting populations of this top carnivore. The aim is to identify regions or parts of catchments where organochlorines may be posing a threat to otters and where further investigations might be advisable. The present study and other publications in the series (Mason et ul., 1992; Macdonald and Mason, in press; Mason and Macdonald, in press) attempt to define environmental quality objectives for protecting otter populations from the effects of organochlorine contaminants. We believe this to be a necessary way forward to conserve those species which have proved highly vulnerable to the activities of man.

MATERIALS AND METHODS

Eighteen catchments, or sub-catchments, of rivers which rise in Wales were surveyed in the present study (Figure 1). The main rivers of the Teme (including the Clun), the Severn and the Lugg (including the Arrow) were surveyed every two months between June 1989 and March 1992 and formed part of a detailed study (Mason and Macdonald, in press). Tributaries of these rivers and all other catchments were surveyed once only within the same period. Sampling stations were visited throughout each catchment and at each station, starting at a bridge, a maximum of 600m of river bank was searched for otter spraints. The method followed the standard British survey method (Macdonald, 1983) but the survey was continued after first finding positive evidence of otters until a sample sufficient for analysis had been collected. The reliability of the method for detecting otters is discussed by Mason and Macdonald (1987, 1991). Note was made of whether the station proved positive for otters and the number of spraints per sprainting site (a place where spraints are deposited, at least 1 m from other spraints) was recorded. Spraint samples (all spraints from a station combined) were wrapped in aluminium foil, placed in labelled polythene bags and deep frozen prior to analysis.

In October 1990 small samples of fish were obtained by electrofishing from five stations on the River Lugg which had been surveyed regularly for otter spraints. Fish were deep frozen and individual fish were minced prior to analysis.

In the laboratory samples were weighed and homogenized in 10 mL acetone : hexane (35 : lo), the filtrate being collected into a separatory funnel containing 25 mL phosphoric acid/NaCl solution (11.7 g NaCl in 11 0.1 M orthophosphoric acid). The sediment was resuspended in two further 10mL aliquots of hexane: diethyl ether (9: 1) and decanted after 5 min. The separatory funnel was shaken and the aqueous phase was decanted and re-extracted in hexane. The solvent phase extracts were evaporated to dryness at 50°C in the air-flow of a fume cupboard and the weight determined. The extract was re-dissolved in hexane and cleaned in a column of sodium sulphate and alumina. Organochlorine concentrations were determined with a Varian 3300 gas chromatograph, with a tritium electron capture detector and using a 25m capillary column. The column temperature was 280"C, the injector 300°C and the detector 310°C. PCB concentrations were determined against an Aroclor 1260 standard. Blanks were run every 20 samples and standards, with or without added lard, every 4 to 9 samples. Recovery rates were always greater than 80% and the detection level was 0.01 mg kg-1.

RESULTS

The distribution of sampling stations is shown in Figure 1. For each catchment or sub-catchment, the percentage of stations found positive for otters and the mean number of spraints per sprainting

PCBs AND ORGANOCHLORINE RESIDUES IN OTTER SPRAINTS 45

0 1 0 2 0 3 0 4 . 50 KIII

U

Figure 1. The study area in Wales showing the 18 catchments and organochlorine contaminants at four levels of concern: Level 1, concentrations in spraints>16mg kg-' of PCB and dieldrin, singly or combined, or concentrations in spraints of total OCs>U) mg kg-'; Level 2, concentrations in spraints>9-16 mg kg-' of PCB and dieldrin, singly or combined, or concentrations in spraints of total OCs> 16-20 mg kg-'; Level 3, concentrations less than 9 mg kg-', but greater than 4 mg kg-'; Level 4, less than 4mg kg-' for all individual contaminants (see text for details). Catchments of the Severn, Teme and Lugg were broken into upper and lower sections at the dotted lines. Catchments are: 1, Clwyd; 2, Dee; 3, Vyrnwy; 4, Severn, upper; 5 , Severn, lower; 6, Tern; 7, Teme, upper; 8, Teme, lower; 9, Lugg, upper; 10, Lugg, lower; 11, Wye; 12, Usk; 13, Tawe; 14, Tywi; 15, Cleddau;

16, Teifi; 17, Ystwyth; 18, Dyfi.

46 C. F. MASON AND S. M. MACDONALD

Table t. The percentage of stations found positive for otters in each catchment (or sub-catchment) and the mean number of spraints per sprainting site.

Number of Mean spraints Catchment stations Qo positive per site

1. Clwyd 11 55 1.5 2. Dee 30 67 1.9 3. Vyrnwy 22 91 4.0 4. Severn, upper 21 94 3 -4 5. Severn, lower 26 42 2.0 6. Tern 18 67 3.3 7. Teme, upper 31 86 4.0 8. Teme, lower 24 59 2.1 9. Lugg, upper 21 94 7.4

10. Lugg, lower 11 92 3.6 11. Wye 42 73 3.4 12. Usk 18 89 1.9 14. Tywi 14 93 4.8 15. Cleddau 27 85 3.2 16. Teifi 34 85 2.1 17. Ystwyth 27 70 2.1 18. Dyfi 14 71 2.4

site are given in Table 1. The Tawe catchment is omitted from Table 1 because the spraints were collected by a third party who walked the entire catchment. There is a positive relationship between the number of spraints deposited per sprainting site and the percentage of positive stations within the catchment (rs=0.74, P<O.Ol). The greater the proportion of a catchment occupied by otters, the greater the intensity of marking at individual sprainting sites.

A total of 816 samples were analysed for organochlorine residues. Lindane concentrations were below the level of detection in samples from the Tawe catchment, but occurred at detectable levels in 25-100% of samples from other catchments. Lindane was present in the majority of samples collected in summer but in few samples collected in winter. Concentrations were generally low, arithmetic means (in samples above the limit of detection) for catchments ranging from 0.08-0.83 mg kg-’ lipid, apart from the Usk (samples collected in July) with a mean of 1.81 mg kg-I lipid. Lindane is not discussed further. Small quantities of o,p-DDD and o,p-DDT were also found.

The percentage of samples containing measurable dieldrin ranged from 94- 100% and containing p,p-DDE 98-100Vo between catchments. All samples had measurable quantities of PCBs. The means and ranges of these contaminants in spraints from catchments are given in Table 2. The means of dieldrin, DDE and PCBs were significantly different between catchments (Anovars on log-transformed data, F= 14.06, 12.53, 26.23 respectively, P < 0.001).

Mason and Macdonald (in press) argued that concentrations of individual contaminants in spraints less than 4mgkg-1 were equivalent to ‘no effects’ levels of contaminants in tissues. Few individual samples, and no catchment mean, exceeded this concentration for dieldrin. Mean concentration of DDE exceeded 4mg kg-1 on the Usk and Clwyd. Mean concentrations of PCBs exceeded 4mgkg-l in samples (in decreasing order of mean concentration) from the Usk, Tawe, Severn (lower), Lugg (lower), Clwyd, Dee, Wye, Teme (lower) and, marginally, the Cleddau, i.e. half the catchments under consideration. Apart from the Cleddau for PCBs, those catchments rising and flowing in west Wales (Dyfi, Ystwyth, Teifi, Tywi) had generally low concentrations of all contaminants.

PCBs AND ORGANOCHLORINE RESIDUES IN OTTER SPRAINTS 47

Table 2. Arithmetic means and ranges (mg kg-I) of dieldrin, DDE and total PCBs in otter spraints from catchments in Wales and adjacent English counties.

Catchment Dieldrin DDE PCBs

n mean range mean range mean range

1. Clwyd 2. Dee 3. Vyrnwy 4. Severn, upper 5. Severn, lower 6. Tern 7. Teme, upper 8. Teme, lower 9. Lugg, upper

10. Lugg, lower 11. Wye 12. Usk 13. Tawe 14. Tywi 15. Cleddau 16. Teifi 17. Ystwyth 18. Dyfi

4 2.64 19 0.75 15 0.87

102 1.08 62 2.03 14 2.26

149 1.16 62 1.26

176 1.58 70 3.41 26 0.85 11 1.59 11 1.24 11 0.36 34 0.25 23 0.49 17 0.74 10 0.36

1.19- 3.68 0.14- 1.69 0.10- 2.92

nd-1 1.05 nd- 19.79

nd- 7.95 nd- 7.00

0.26- 5.39

0.02- 8.90 6.04-23.91 0.15- 3.07 0.49- 3.13 0.03- 5.16 0.09- 1.21 0.03- 1.17 0.06- 2.49

nd- 2.95 nd- 2.08

4.22 1.91 2.25 1.67 3.46 2.91 1.89 2.87 1.61 3.75 1.70 4.67 1.72 0.79 0.71 1.01 1.19 0.51

2.12- 6.03 0.28- 4.18 0.20- 4.97 0.03- 8.18 0.17-34.29 0.04- 9.28 0.08-12.41 0.30- 14.76

nd- 8.52 nd-23.06

0.31- 4.60 2.54- 9.98 0.24- 4.22 0.30- 2.08 0.05- 2.17 0.04- 6.75 0.03- 4.96 0.05- 2.36

6.34 6.15 3.72 2.16 8.08 3.27 2.32 5.48 1.85 7.60 5.92

14.3 1 8.42 3.33 4.18 3.05 2.29 3.09

4.96- 7.99 0.82-32.04 0.12-16.72 0.03-62.68 0.33-44.68 0.41- 6.90 0.04-11.94 0.06-40.8 1 0.02- 7.47 0.20-67.23 1.05-17.64 2.97-34.19 1.73-20.75 0.34- 8.49 0.49-33.58 0.15- 9.03 0.15- 6.45 0.08- 15.05

~

To assess the significance of contaminant levels in spraints, a hierarchy of concentrations is used:

1.

2.

3.

4.

Critical levels. Concentrations in spraints> 16 mg kg-I of PCB and dieldrin, singly or combined; or concentrations in spraints of total OCs > 20 mg kg- I .

Levels of concern. Concentrations in spraints> 9-16 mg kg- of PCB and dieldrin singly or combined; or concentrations in spraints of total OC > 16-20 mg kg- l .

Maximum allowable concentration. Concentrations less than the level of concern but greater than the no effects level. No effects level. Less than 4 mg kg- for all individual contaminants, as described above.

This approach is based on a single compartment model relating PCB concentrations in spraints to tissue concentrations (Mason et al., 1992, Mason and Macdonald, in press). Because of concern of the possible role of dieldrin in the decline of the otter (Chanin and Jefferies, 1978), we have used identical target values for both PCBs and dieldrin. The values for total OCs are entirely arbitrary, but in fact only one sample was placed in categories 1 and 2 because of the total OC concentration, the majority being placed there because of their PCB concentration alone, dieldrin being of much less significance. The approach is fully described and justified by Mason and Macdonald (in press). We are in effect taking a precautionary approach to conserving otter populations. We adopt a ‘compliance’ level of 90% of samples within a catchment falling below levels 1 and 2, in a manner analogous to that of regulatory authorities protecting water resources from polluting discharges. The results are shown in Table 3. Catchments with greater than 10% of samples in levels 1 and 2 (‘70 in brackets) were Usk (63), Clwyd (50), Lugg, lower (48), Tawe (43, Severn, lower (41), Teme, lower (27), Wye (23) and Tern (14). However the Clwyd (only 4 samples) and Tern had no samples in level 1.

The relationship between mean contaminant levels in catchments and both the mean number of spraints per site (marking intensity) and the percentage of stations positive for otters was examined. There was a significant negative relationship (both variables log-transformed) between mean number of spraints per site and mean PCB concentration ( r= -0.54, p<0.02), but not with mean DDE ( r = -0.31, NS)

48 C. F. MASON AND S. M. MACDONALD

Table 3 . Percentage of samples in four contaminant concentrations: 1, critical; 2, concern; 3, maximum allowable concentration; 4, background. See text for definitions of levels.

Level Catchment n 1 2 3 4

1 . Clwyd 4 0 50 50 0 2. Dee 19 10 0 32 58 3 . Yyrnwy 15 0 7 13 80 4. Severn, upper 102 3 7 6 84 5. Severn, lower 62 18 23 24 35 6. Tern 14 0 14 36 50 7. Teme, upper 149 1 8 7 84 8. Teme, lower 62 8 19 16 57 9. Lugg, upper 176 0 3 10 87

10. Lugg, lower 70 21 27 15 37 1 1 . Wye 26 4 19 38 39 12. Usk 1 1 45 18 27 27 13. Tawe 1 1 18 21 27 27 14. Tywi 1 1 0 9 36 55 15. Cleddau 34 3 6 26 65 16. Teifi 23 0 4 22 74 17. Ystwyth 17 0 0 29 71 18. Dyfi 10 10 0 20 70

or dieldrin (r = - 0.05, NS) concentrations. There was also a significant relationship between the percentage of stations positive in a catchment and mean PCB concentrations (rs= -0.41, p<0.05), but not with mean DDE (rs = - 0.29, NS) and dieldrin (rs = - 0.15, NS) concentrations. There was also a significant relationship between the mean number of spraints per site within catchments and the percentage of samples in contaminant levels 1 and 2 (rs = - 0.46, p < 0.05). Thus overall, the performance of an otter population, as measured by catchment distribution and marking intensity, is inversely related to the concentration of PCBs in spraints.

Small numbers of fish (5-12 per station) were collected from five stations on the River Lugg. The majority consisted of eels (Anguilla anguilla) and trout (Salmo fruffa), and only these are considered here. Station 1 (upstream) had only trout. Both trout and eels were collected from station 3 and had similar mean PCB concentrations in whole body mince (0.04 and 0.03 mg kg- fresh weight respectively). Eels were also present at stations 2, 4 and 5. In Figure 2 mean body concentration of PCB in fish is plotted against station numbers and it can be seen that concentration increases downstream. Also plotted are the mean concentrations of PCBs in spraints from the same stations. Mean concentrations of PCBs in fish and spraints are highly correlated (r, = 1, p <0.001). There is also a general trend of increase in the concentrations of dieldrin and DDE in fish at downstream stations.

DISCUSSION

The results of an otter survey of Wales in 1984-85 indicated that there had been a small increase in otter populations compared with the previous survey of 1977-78 (Andrews and Crawford, 1986). Increases had been greatest on the rivers of West Wales, significantly those with the lowest amounts of organochlorine contaminants in otter spraints in the current study. Concern was expressed over the population on the Usk and this river had the highest amount of organochlorines in otter spraints. Similarly much of the Clwyd catchment had no evidence of otters in the 1984-85 survey and a high proportion of spraint samples were above the level of concern for contaminants, though sample size was small. The Tawe has been colonized by otters since 1984-85 but our results suggest that animals are occupying a contaminated habitat.

PCBs AND ORGANOCHLORINE RESIDUES IN OTTER SPRAINTS 49

1 1 S 4 s Sltn

Figure 2. Mean concentration of PCBs in whole body mince of fish and in otter spraints at five stations on the River Lugg.

The Welsh otter survey did not consider the lower, English reaches of the Severn, Teme and Lugg but Mason and Macdonald (in press) detail the hesitant nature of the expansion of these rivers, which they relate to contamination, particularly with PCBs. Similarly, expansion into the English Wye is slow, although under ideal conditions population expansion can be rapid (Mason and Macdonald, in press).

The present study has shown a negative correlation between the mean PCB concentration in spraints and the average marking intensity (mean number of spraints per sprainting site) and percentage of sites positive (distribution) within catchments. The relationships were statistically significant despite other strong influences on marking intensity in the region, e.g. habitat quality (Macdonald and Mason, 1983) and seasonality (Macdonald and Mason, 1987). There were no such significant correlations with dieldrin or DDE. Thus the evidence suggests that PCBs may be currently exerting an adverse impact on otter populations in some rivers in the region. PCBs are known to affect the reproduction, endocrine and immune systems of mammals and mink (Mustela vison), a close relative of the otter, has been shown experimentally to be susceptible to low doses of PCBs (see review in Mason, 1989).

The organochlorine residues measured in otter spraints are very largely derived from the unabsorbed residue of the last meal (Mason et al., 1992; Mason and Macdonald, in press). From the one river (the Lugg) from where we have data on PCBs in both fish and otter spraints at various sites, there is a direct relationship in PCB concentrations (Figure 2). Average concentrations in fish at the lowermost two sites may be too high to support otter populations, using the standard (<0.05 mg kg-I fresh weight PCB) suggested by Macdonald and Mason (in press).

50 C. F. MASON AND S. M. MACDONALD

Ormerod and Tyler (1990; in press) provide the only other broad study of organochlorines in the biota of Welsh rivers, for the eggs of dippers (Cinclus c inch) , a passerine bird feeding on aquatic invertebrates and small fish. For the nine catchments for which there were data on both dipper eggs and otter spraints, there was a significant positive correlation (rs = 0.73, p < 0.05) in mean PCB concentrations, suggesting a general contamination of the aquatic ecosystem of some catchments.

The sources of PCBs entering Welsh rivers may be various. Concentrations tend to be highest close to the industrial south (Usk, Tawe) and also to the north and west of this region, suggesting dispersal of contaminants on the prevailing winds. The distribution is not uniform, however (see Figure 1); for example concentrations of organochlorines are very low in the upper Teme, upper Lugg (including Arrow) and Ithon (a Wye tributary), all rising in the same upland area, compared with neighbouring rivers. Agricultural slurry may also provide a source of PCBs (Jones, 1989) and its use is likely to be greater in the east of the region where there is a much larger proportion of arable farmland. There are also likely to be local sources from small industries and sewage works. The monitoring of surface waters for organochlorines in the region is extremely restricted (National Rivers Authority, 1991), with a total of only 38 sampling sites monitored monthly on main rivers. Few samples contain concentrations above the limit of detection. Data from both dipper eggs (Ormerod and Tyler, 1990; in press) and otter spraints suggest that current statutory monitoring is inadequate to detect the extent and significance of organochlorine contaminants in the rivers of the region. Both techniques provide a method of monitoring organochlorine residues in aquatic environments without the need for destructive sampling.

The current study indicates that contamination with PCBs may be exerting a negative impact on otter populations, especially in the rivers Usk, lower Lugg, Tawe and lower Severn. There is concern also over the lower Teme and Wye and maybe the Clwyd and Tern, though these latter two rivers had no samples in the highest category of concern. It is clear that these rivers of concern require more detailed investigations of PCB contamination in the food chain leading to otters to determine the extent of the problem and to identify possible sources. If individual sources can be pinpointed and controlled, the overall level of contamination may decline to below that likely to have a negative impact on otter populations, allowing expansion to occur. Mason and Macdonald (in press) observed that the level of contamination in otter spraints on the lower Lugg (but in no other river in that study) declined over several years to fall below the level of concern in 1991; they predicted an ensuing consolidation in the otter population and this appears to be happening (personal observations). Organochlorine concentrations in the eggs of dippers also appear to be declining (Ormerod and Tyler, in press).

If conditions in the lower reaches of those rivers rising in upland Wales improve, then we are likely to witness further attempts at otter range expansion eastwards across lowland England. However, we predict that a more general level of contamination of aquatic ecosystems may be more problematic for expansion into central England.

Finally, there are a number of current conservation initiatives for otters, both national and local, in Britain. Although there is little doubt that contamination of aquatic food chains was the main cause of the drastic decline in numbers and range of otters in Britain (Mason, 1989), few, if any, of these initiatives give more than cursory consideration to current levels of contamination, or attempt to add to our scanty knowledge of contaminants in British rivers. Without such information, these initiatives may do little to benefit the otter. There is little point, for example, in enhancing habitat for otters or for reintroducing the species to parts of its former range if levels of contamination are still too high to allow populations to expand.

ACKNOWLEDGEMENTS

We are grateful for the financial support of the National Westminster Bank, through sponsorship with the World Wide Fund for Nature, U. K. Mr Paul Hilder, of the National Rivers Authority (Welsh Region), collected fish samples from the River Lugg, while Kathy Pyke and Liz Flood of the Otter Project Wales collected spraint samples from the Teifi and Tawe. Helen Bland and John Ratford provided technical support.

PCBs AND ORGANOCHLORINE RESIDUES IN OTTER SPXAINTS 51

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