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Abundance, diet and Salmonella contamination of gulls feeding at sewage outfalls
PII: S0043-1354(99)00427-3
Wat. Res. Vol. 34, No. 10, pp. 2653±2660, 2000 7 2000 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0043-1354/00/$ - see front matter
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ABUNDANCE, DIET AND SALMONELLA CONTAMINATION OF GULLS FEEDING AT SEWAGE OUTFALLS PETER N. FERNS1* and GREGORY P. MUDGE2 1
School of Biosciences, Cardi University, PO Box 915, Cardi CF1 3TL, UK and 2Scottish Natural Heritage, The Governor's House, The Parade, Fort William, Inverness-shire, PH33 6BA, UK (First received 1 July 1999; accepted in revised form 1 December 1999)
AbstractÐThe abundance and activity of gulls at sewage outfalls in South Wales and southern England was studied between 1972 and 1999. In winter, the black-headed gull was the most abundant species, followed by herring, common and lesser black-backed gulls. The abundance of black-headed gulls and herring gulls was signi®cantly correlated with the volume of sewage discharged. Sewers supported only a small portion of the gull populations present in both areas, and a higher proportion of juvenile birds were present than at other feeding sites. Sewage comminution increased the numbers of black-headed gulls feeding, but infrequent intermittent discharge reduced them by over a half. Gulls selectively consumed waste foodstus from sewage and thus helped recycle some of its organic constituents. However, some individuals carried bacterial pathogens, and could thus have contaminated nearby bodies of freshwater, or grassland, by washing and roosting there. Full sewage treatment, as planned for most of the discharges in both study areas is likely to provide the most eective means of gull control. 7 2000 Elsevier Science Ltd. All rights reserved Key wordsÐgulls, sewage outfalls, sewage discharge, Salmonella, public health
INTRODUCTION
Gulls have been observed feeding at coastal sewage outfalls since at least the end of the last century (Yarrell, 1882±84), yet there is little information available about the numbers involved or the foods they consume. The aim of the present study is to determine the abundance and feeding behaviour of gulls at sewage outfalls at contrasting sites in South Wales and in southern England. In the former area, a considerable volume of raw sewage is discharged into the Bristol Channel via relatively short estuarine outfalls. In the latter, smaller amounts of sewage are discharged further out to sea. The diet of these gulls has been determined, and tests for the carriage of Salmonella undertaken. In addition, trials have been conducted to determine whether gull numbers are aected by comminution of the sewage or by dierent rhythms of discharge. STUDY AREAS AND METHODS
The main South Wales study area extended along ca. 150 km of coast from Porthcawl (Vale of Glamorgan) in the west, to Newport (Gwent) in the east (Fig. 1(a)). A total of 252 counts of gulls were made during 48 days of
*Author to whom all correspondence should be addressed; e-mail: fernspn@cardi.ac.uk
observations at the 17 sewers in this area between 1972 and 1999. A less extensive survey was carried out at six outfalls along more than 230 km of coast near Weymouth and the Isle of Portland in Dorset (114 counts during 18 days) (Fig. 1(b)). The 24 outfalls in the two study areas varied considerably in their average ¯ow rates and their patterns of discharge (Table 1). At only seven of them was any form of sewage treatment employed, and this consisted of comminution and grit removal. Although discharge was supposed to be continuous at 15 of the sewers, in practice there was considerable curtailment of ¯ow at high tide due to hydraulic back-pressure in the pipes or to the presence of tidal ¯aps. All but three of the sewers normally discharged subtidally. On all occasions, separate counts were made of feeding and non-feeding gulls. Most feeding birds were stationed near the mouth of the outfall, but some also occurred at leaks in the pipe and along the tide edge. Gulls that were close to the outfall, but which were feeding on intertidal invertebrates, were excluded. Gull age was recorded as ®rst winter (juvenile) or adult in the cases of black-headed gulls Larus ridibundus and common gulls L. canus, and ®rst/second winter (juvenile) or adult in the larger species. Trials were conducted on the eects of sewage comminution and intermittent discharge on gull numbers at outfall nos 18 and 24. In the former trials, the comminutor was removed on two days (9 and 11 November 1976) so that raw sewage was discharged. Three days during which the comminutor was in place and operating normally served as controls (1, 3 and 10 November 1976). In the intermittent discharge trials, sewage was diverted from a sewage treatment works to outfall no. 24 either continuously
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Peter N. Ferns and Gregory P. Mudge
(4 days), or for repeated ®xed periods of time each day (4 days). The ®xed periods varied between 12 and 1 12 h on dierent days. Gulls were counted at least twice an hour during these trials. The birds' diet was determined by analysing the gut contents of 10 black-headed gulls (eight adults and two juveniles) shot under licence at outfall no. 19 in November 1976, and a further 24 black-headed gulls (nine adults and 16 juveniles) at outfall nos 13 and 15 between December 1976 and March 1977. The number of guts containing dierent food items was counted after sorting, and the percentage volume occupied by each category estimated by eye. Black-headed gull droppings were collected at low tide from the vicinity of outfalls nos 13 and 15 in July 1976, January 1989 and February 1994. A total of 780 individual fresh droppings were analysed for Salmonella at Veterinary Investigation Centres in Carmarthen, Bristol and Aberystwyth. Gull counts were transformed to logarithms if this was necessary to achieve normality. If normality could not be achieved, resampling statistical methods were used. Repeated measures ANOVA was used when analysing series of counts made at the same sewer during the course of single days (Sokal and Rohlf, 1981).
RESULTS
Overall gull abundance During winter in the 1970s, a maximum of about 15,500 gulls was observed feeding at 21 of the outfalls (nos 5, 6 and 24 were not counted), of which 87% were black-headed gulls. Average counts during discharge were much lower, amounting to 6288 (84% black-headed gulls). By the 1990s, the only signi®cant change in numbers was in lesser black-backed gulls L. fuscus, which increased on average from 19 to 34 (289%). The probability of an increase as large as this being due to chance was 0.041, based on 10,000 resamplings of the pooled counts on which the means were based. Since this change in abundance only involved the least abundant species, counts were combined for the whole of the 27 year study period (Table 1). On average, throughout this period of nearly three decades, 84% of the gulls at sewers in South Wales were black-headed, compared with 79% in southern England. The equivalent ®gures for her-
Fig. 1. Location of the study areas in (a) South Wales, and (b) southern England (the scale is the same in both maps). The sewage outfalls are numbered as in Table 1.
Gulls and sewage outfalls
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Table 1. Sewage discharge and average winter counts of feeding gulls at sewage outfalls in the two study areas in 1973±1999 (C=comminution, G=grit removal, H=high tide discharge only, O=some discharge across the open shore at low tide, E=emergency use only). N = number of counts Outfall number
South Wales 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Southern England 18 19 20 21 22 23 24
Average ¯ow rate (Mldÿ1) (treatment and discharge rhythm in brackets) 1.1 1.5 13.6 2.6 1.7 0.5 0.2 4.5 11.4 27.7 1.4 1.8 36.8 24.1 90.9 39.4 73.0
(C) (H) (C, O) (G, C, H) (O) (G, C) (O) (G, C, H)
4.6 (C) 14.4 (C) 1.9 2.4 0.1 0.03 0.00 (E)
Black-headed gull2SE
Common gull
Lesser black-backed gull
Herring gull
N
150233 72229 372276 150225
125 40 22 0
0 0 0 0
51 11 110 76
7 7 10 7
50219 258244 5432103 108228 105224 33214 530276 476256 10692349 689240 497293
2 6 0 0 0 0 3 1 3 76 17
0 28 1 3 2 0 2 3 3 6 3
4 138 72 8 11 7 11 60 48 21 19
7 15 11 18 16 16 34 18 34 34 18
42213 78214 1322 1124 823 0
23 1 0 0 5 0
0 0 0 0 0 0
1 1 2 5 3 0
28 24 21 21 10 10
ring gulls L. argentatus were 11 and 6%, and for common gulls 5 and 15%. Common gulls only occurred in large numbers at outfalls close to coastal roosts of this species e.g. Porthcawl and Bridport. Common gulls were none the less the third most numerous species in both study areas (Tables 1 and 2). The only other species of gulls seen feeding at sewers were ®ve great black-backed gulls L. marinus in Wales, two little gulls L. minutus and two Mediterranean gulls L. melanocephalus in England. The relative importance of sewers to gulls in comparison with other feeding sites is indicated by the proportion of the total populations of each study area feeding there (Table 2). Sewers were obviously of greater importance in South Wales, which is not surprising given the fact that the total volume of euent discharged was 14 times greater than in southern England. A greater proportion of juvenile gulls was consistently recorded at sewage outfalls than at other feeding sites or at roosts (Table 3). Even the smallest dierence (proportion of juvenile herring gulls at sewers vs roosts) is statistically signi®cant (contingency w 2=114.4, P < 0.0001). The proportion of juveniles varied widely at dierent sewersÐfor example, juvenile herring gulls ranged between 19 and 58%. In this species, there was also a signi®cant correlation between the percentage juveniles and the number of black-headed gulls present (r = 0.571, n = 15, P = 0.026). The numbers of black-headed gulls were much lower during the summer months (April±August),
but the numbers of larger gulls increased. For example, between April and July, there were on average 238 2 86 (mean 2 SD) herring gulls at outfalls nos 1, 15 and 16 (the only ones counted regularly in summer), compared with 120264 in winter. Lesser black-backed gulls increased even more markedly, with 72 2 31 recorded in summer and only 9 2 8 in winter. Although large breeding colonies of both these species were situated in Gwent and Glamorgan, most of the birds at sewers were juveniles (39% of herring gulls and 22% of lesser black-backed gulls were second and third summer birds), and were therefore non-breeders. Numbers in relation to sewage ¯ow In the case of continuously discharging sewers, there were usually morning and/or evening peaks of feeding activity (e.g. Fig. 3). In many cases, gulls were already feeding at dawn, and continued to feed after dusk if sewage was ¯owing. Regardless of the time of day, peak numbers at intermittent outfalls usually occurred early in the discharge cycle and signi®cantly more birds were present when sewage was ¯owing. For example, averaging across all days of the intermittent discharge trial, 61% fewer black-headed gulls were present when ¯ow had stopped, and this reduction was statistically signi®cant (ANOVA of mean counts during each period of ¯ow; dierence between days, F = 11.0, df=3,24; P < 0.0001; ¯ow vs non-¯ow, F = 16.6, df=1,3; P = 0.027). The average ¯ow rates in Table 1 provide the only measure of the quantity of food likely to have
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Peter N. Ferns and Gregory P. Mudge
Table 2. Average counts (rounded to nearest 10) of the total wintering gull populations of the two study areas and the numbers feeding at sewers (1972±1999) Study area
Place counted
South Wales
Total Sewers % at sewers Total Sewers % at sewers
Southern England
Black-headed gull
Herring gull
Common gull
Lesser black-backed gull
44,970 5102 11 10,630 52 1
20,930 647 3 5700 12 0
4720 295 6 500 29 6
750 51 7 10 0 0
been available at each outfall, though they are only an index because of variations in the size of the catchment and human population served by each. There was a signi®cant correlation between these ¯ow rates and the average numbers of black-headed gulls feeding at each sewer (Fig. 2). ANCOVA showed no signi®cant dierence between the 1970s and 1990s regressions for those sewers counted in both decades and so the overall mean counts (Table 1) have been used. ANCOVA also showed no signi®cant eect of comminution and grit removal. Hierarchical ANOVA showed that there were signi®cantly fewer black-headed gulls at sewers that discharged only at high tide (F = 4.95, df=1,20; P < 0.0005). ANCOVA on continuously discharging sewers showed that the regression lines did not dier signi®cantly in slope in Wales and England, but did have a signi®cantly higher intercept in Wales (F = 29.54, df=1,18; P = 0.0004). The regressions for herring gulls were also signi®cant, and likewise diered in intercept (F = 16.80, df=1,18; P = 0.0007). There were no signi®cant correlations between numbers and sewage ¯ow in any other species. During the trial designed to determine the eects of comminution, the number of black-headed gulls feeding at outfall no. 18 between 1000 and 1400 h was 2327 (mean2SE) on control days and 2925 on comminuted days. They then rose to an evening peak (Fig. 3). Repeated measures ANOVA of the logarithmically transformed variables showed that there was a highly signi®cant dierence in abundance throughout the course of the day (F = 27.8, df=10, 30; P < 0.00001), and marginally more black-headed gulls were present when sewage was comminuted (F = 12.90; df=1, 3; P = 0.037). On average, this increase amounted to 55% (based on the arithmetic means). The numbers of feeding com-
mon gulls between 1000 and 1400 h was 31 2 4 (mean 2 SD) on control days and 30 2 6 on comminuted days. There was no signi®cant eect of comminution in this species. Relatively small numbers of black-headed gulls were present when no sewage was ¯owing during the intermittent discharge trial (13 2 3). There was no signi®cant dierence between the average numbers of black-headed gulls present on days of continuous ¯ow and those present when sewage ¯owed for 52% of the time, but there were signi®cantly fewer on the other days (Table 4; based on log numbers, during discharge only, t = 2.74, df=13, P = 0.017; whole day, t = 3.62, df=27, P = 0.001). A discharge rhythm of 1 12 h on and 1 12 h o thus did not signi®cantly reduce the number of blackheaded gulls feeding at a sewer, but less than 1 h on and 1 12 h or more o did. The reduction in numbers in the latter case amounted to about 65% during discharge, or 75% when averaged throughout the whole day (Table 4). Diet There were no signi®cant dierences in the gizzard and oesophageal contents of adult and juvenile gulls shot at sewers and so these age categories have been combined (Table 5). The most abundant item in the guts of black-headed gulls was plant debris. Most of this was grass, probably ingested by birds foraging for invertebrates on inland ®elds. Indigestible items found in gizzards included small fragments of plastic, string, matchsticks, sanitary towels and condoms. The small particle size of these items (<0.5 cm) suggests that gulls may have mistaken them for fragments of food. When only digestible items are considered, the most important component of the diet of blackheaded gulls was plant seeds (27% by volume), fol-
Table 3. Percentage of juvenile gulls in feeding and roosting winter ¯ocks in both study areas (numbers rounded to nearest 10) Site
Black-headed gulls Average number of birds
Sewage outfalls Refuse tips Fields Roosts
Herring gulls
Number aged
% ®rst winter
5150
3480
30
2480 41,770 55,600
250 2970 6560
4 4 4
Average number of birds
Number aged
% ®rst and second winter
660
930
36
17,980 4640 26,630
6020 2280 4310
18 7 20
Gulls and sewage outfalls
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of the sewers we studied was situated only 500 m from a boating lake that was used by the gulls feeding at the sewer for washing and preening. Clearly, a risk of contamination of such waters exists under these circumstances.
DISCUSSION
Fig. 2. Average numbers of black-headed gulls feeding at continuously discharging sewage outfalls in relation to the quantity of sewage discharged by each (d ). The regression equations were as follows: Wales, log nos=0.474logd + 1.937 (r 2=0.68, P = 0.0001); England, log nos=0.583logd + 1.123 (r 2=0.84, P < 0.01).
lowed by meat (15%). Rice grains, melon seeds and grape pips were all taken, but the commonest seed was peanuts. A peanut packaging company discharged its waste into outfall no. 15. Potato peelings were the commonest type of vegetable peelings encountered. In the case of seeds, bread, meat and fat, the particle size was small (generally < 0.5 cm diameter), but vegetable peelings were usually larger than this. Bacterial contamination Salmonellae were isolated from 49 of the 780 samples of black-headed gull droppings, giving an overall occurrence rate of 6.3%. Identi®ed serotypes (number of isolates in brackets) included S. bredeney (19), S. heidelberg (13), S. typhimurium (10), S. virchow (8), S. hadar (2), S. derby (1). All these serotypes have previously been isolated from herring gulls in Dyfed and Scotland (Williams et al., 1976; Monaghan et al., 1985). Contrary to previous results for herring gulls, however, signi®cantly more black-headed gull droppings contained salmonellae in the breeding season (12.5%) compared with winter (4.1%) (contingency w 2=19.1, P < 0.001). One
Fig. 3. Average numbers of black-headed gulls at outfall no. 18 during the comminution trial (+ or ÿ1 SE).
Despite the fact that it has a coastline that is only 65% as long, the South Wales study area supported many more gulls than the English one. This may be one reason for the higher intercept of the regression line relating black-headed gull numbers to sewage ¯ow in Wales. Another may be the fact that the English sewers discharged into relatively deep water where less food is made available to gulls than is the case with sewers discharging into shallower estuarine waters (and at three sewers across the intertidal area). The fact that there was little change in gull abundance at sewers during the 27 years of this survey re¯ects the stability of both the food supply and gull populations during this period. The increase in lesser black-backed gulls between the 1970s and 1980s was broadly in line with that recorded nationally at winter roosts during approximately the same period (Bowes et al., 1984). While 11% of the wintering population of blackheaded gulls in South Wales fed at sewers, this compares with about 5% at refuse tips, 12% on the shore and 70% on ®elds. Refuse tips are of greater importance to herring, lesser black-backed and great black-backed gulls, supporting 43±75% of their populations. Only 1.3% by volume of the foods taken by herring gulls to their chicks on Steep Holm consisted of material derived from sewers. None was fed to chicks at other colonies by this species or by lesser and great black-backed gulls (Mudge and Ferns, 1982). In the only previous quantitative study, Fitzgerald and Coulson (1973) found that sewage outfalls along the River Tyne were widely utilised by black-headed and herring gulls, but to a smaller extent by lesser black-backed gulls, common gulls and kittiwakes Rissa tridactyla. Hulscher (1985) has suggested that the occurrence of a high percentage of juvenile black-headed gulls is an indication of a poor feeding site. Juvenile gulls generally have a lower rate of foraging success than adults (Verbeek, 1977; Greig et al., 1983), either because they are less experienced or because adults aggressively interfere with their feeding, sometimes forcing them to feed in less favoured sites. The fact that relatively more juvenile gulls occurred at sewage outfalls than at other feeding sites therefore suggests that sewers may be less preferred areas. One reason why relatively more juvenile herring gulls are attracted to sewers with large numbers of black-headed gulls may be that they specialise in kleptoparasitising the smaller species (c.f. Fitzgerald
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Peter N. Ferns and Gregory P. Mudge
Table 4. Average numbers of black-headed gulls present at outfall no. 24 under dierent discharge conditions. N = number of days (number of counts in brackets) Discharge
Percentage of time for which sewage ¯owed
Continuous Intermittent
Average numbers of black-headed gulls (2SE)
100 52a 27b
N
Whole day
N
During discharge only
4 (50) 1 (25) 3 (27)
5226 4525 1321
4 (50) 1 (14) 3 (33)
5226 5527 1823
a 1
1 2 h on, 1 12 h o. 3 1 2 ± 4 h on, 1 2 ±3 h o.
b1
and Coulson, 1973; Verbeek, 1977). Such behaviour was also observed at many of our sewers. Comminution increased black-headed gull numbers by 55% in this study. This is probably because it increased the amount of sewage solids in the size range consumed by black-headed gulls (<0.5 cm diameter) from 53 to 72% (measured at outfall no. 18). Smaller particles may also be swept to the surface more readily and may spread out over a wider area. Intermittent discharge reduced numbers by more than half when the discharge period was less than 1 h, and the interval between discharges lasted at least 1 12 h. However, as a potential method of reducing gull numbers, it is doubtful whether intermittent discharge is viable. Few outfalls could be operated in such a way, given the practical diculties of switching ¯ow on and o, and the consequent reduction in discharge time. The use of diusers at sewage outlets (not used at any of the outfalls in the present study) can substantially reduce the tendency of the freshwater, in which the sewage solids are suspended, to ¯oat to the surface and this form of management might therefore be worth investigating. The gizzard and oesophagus contents of gulls at sewers showed that many of them also fed on intertidal or inland invertebrates. This was most marked in black-headed gulls in southern England, where 9% of the diet consisted of invertebrates which could have been obtained inland. There was no evidence from this examination of gut contents, or from direct observations of feeding birds, that gulls consumed material derived from human faeces. This is despite the fact that
other species have been observed consuming animal faeces, notably glaucous gulls L. hyperboreus eating seal droppings (Ryder, 1957) and ivory gulls Pagophila eburnea eating polar bear droppings (Bateson and Plowright, 1959). Gulls appear to be opportunist feeders at sewers, just as they are at other sites, choosing whatever waste foods happen to be available. The average particle size of food items available at sewers was very small and presumably does not often provide an adequate return for the larger species. This helps to explain why black-headed gulls are the commonest gulls at outfalls even though larger species, such as herring and lesser black-backed gulls, are capable of displacing them from the best feeding positions. Food processing wastes, such as the peanuts at outfall no. 15, can be of considerable importance and such wastes are known to be exploited by other species. For example, wintering ducks in Scotland fed on spent barley discharged by distilleries in the 1970s (Campbell, 1978), but their numbers declined as soon as this source of food was no longer available. The other main categories of food taken by gulls (seeds, meat, vegetable peel and bread) may be of both domestic and commercial origin. Small particles of such materials are ¯ushed down the drains of most households and catering establishments. The diet at sewers is remarkably similar to that at refuse tips, and diers more in particle size than in the nature of the particles consumed. The overall rate of occurrence of salmonellae in the black-headed gull droppings we collected near sewers (6.3%) was lower than that recorded for herring gulls in both Dyfed (22.2%) (Williams et al., 1976) and the Clyde area of Scotland (10.1%)
Table 5. Gizzard and oesophagus contents of 34 black-headed gulls shot whilst feeding at sewage outfall nos 13, 15 and 19 Type of food Plant debris Plant seeds Meat Arthropods (Diptera, Coleoptera, Araneae) Indigestible material Bread Unidenti®ed organic matter Vegetable peelings Other invertebrates (Lumbricidae, Oniscidea) Fish bones
Number of guts containing item
Percentage volume
30 29 23 16 15 6 4 3 6 3
34.3 27.2 15.3 8.9 5.5 2.9 2.8 2.5 0.4 0.2
Gulls and sewage outfalls
(Monaghan et al., 1985). In the former case, S. bredeney was the commonest isolate, as in the present study. In the latter case, it was S. virchow, and there was a signi®cant positive relationship between the rate of occurrence of salmonellae in gulls and the number of human cases reported by local hospitals. In both of these earlier studies, the herring gulls tested scavenged at refuse tips, rather than at sewage outfalls and the relationship was presumably a consequence of humans and gulls consuming the same contaminated foods. Monaghan et al. (1985) considered that the reason herring gulls at breeding colonies carried more salmonellae than those at refuse tips was that they had been feeding at sewage outfalls. This is supported by the high rates of occurrence recorded near sewage outfalls by Fenlon (1983) (17±21%), and at sewage works (55%) (Fenlon, 1981). Our results indicate that for blackheaded gulls at least, the occurrence rate is not always high at sewers, at least during winter when the largest numbers of gulls are present. Gulls represent a potential route for the transmission of pathogens and parasites by gulls to playing ®elds, pastures and reservoirs. For example, gulls have been implicated in the transmission of the eggs of the human tapeworm Taenia saginata and salmonellae from sewage to cattle (Silverman and Griths, 1955; Reilly et al., 1981), and in the contamination of reservoirs with faecal streptococci, salmonellae and Escherichia coli (Fennell et al., 1974; Monaghan et al., 1985). A range of other disease-causing organisms, such as Bacteroides fragilis, are also present in sewage and can remain viable for 48 h, even after dilution in fresh water (Shoop et al., 1990), and these too could be transferred by gulls from sewers to lakes and reservoirs. Of perhaps the greatest concern is the fact that E. coli 0157 has been identi®ed in the droppings of gulls at a land®ll site in Morecambe Bay (Wallace et al., 1997). Even if it were desirable to do so, there is no easy way of preventing gulls from feeding at sewage outfalls, short of complete euent treatment. In both study areas, considerable changes in sewage disposal are already taking place. For example, full treatment for all the South Wales outfalls should be in place by 2002, though the existing outfalls will still have to be used during storm conditions. In southern England, a large storage tank has been constructed at Hengistbury Head, and a membrane treatment plant has just been completed at Swanage. Welsh Water Plc has indicated that all coastal and estuarine discharges will eventually receive at least secondary treatment. This will not necessarily remove all faecal indicators from such coastal waters, since birds (including gulls, waders and wildfowl) which excrete faecal coliforms, streptococci and perhaps Campylobacter lari have been implicated in the continued contamination of Morecambe Bay after the introduction of secondary sew-
2659
age treatment (Obiri-Danso and Jones, 1999). These changes should lead to a substantial improvement in water quality, however, and the loss of feeding opportunities for birds is unlikely to have serious consequences for local gull populations. AcknowledgementsÐThe early surveys in South Wales were commissioned by the Nature Conservancy Council (South Wales Region) and in southern England by D.A.F. Coney and Sons Ltd. GPM was in receipt of a NERC studentship during part of this work. We are grateful to Welsh Water Plc for supplying details of all the sewers in South Wales, and to Wessex Water Plc for their cooperation during the experiments in southern England. We would also like to thank M. K. Brummage, G. P. Green, J. M. Hope, C. Prescott, J. Rees, I. S. Robertson, J. B. A. Rochard, D. Roscoe, A. G. J. Tacon, K. Thomas, W. A. Venables and J. Woodworth for help with various aspects of the ®eldwork and S. A. Hinsley and C. Johnson for commenting upon drafts of this paper. REFERENCES
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Shoop D. S., Myers L. L. and LeFever J. B. (1990) Enumeration of enterotoxigenic Bacteroides fragilis in municipal sewage. Appl. Environ. Microbiol. 56, 2243±2244. Silverman P. H. and Griths R. B. (1955) A review of methods of sewage disposal in Great Britain, with special reference to the epizootiology of Cysticercus bovis. Ann. of Trop. Med. Parasit. 49, 436±450. Sokal R. R. and Rohlf F. J. (1981) Biometry. W. H. Freeman, San Francisco. Verbeek N. A. M. (1977) Comparative feeding behaviour
of immature and adult Herring Gulls. Wilson Bull. 89, 415±421. Wallace J. S., Cheasty T. and Jones K. (1997) Isolation of Vero cytotoxin-producing Escherichia coli 0157 from wild birds. J. Appl. Microbiol. 82, 399±404. Williams B. M., Richards D. W. and Lewis J. (1976) Salmonella infection in the herring gull (Larus argentatus ). Vet. Rec. 98, 51. Yarrell W. (1882±84) A History of British Birds. J. Van Voorst, London.
Wat. Res. Vol. 34, No. 10, pp. 2653±2660, 2000 7 2000 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0043-1354/00/$ - see front matter
www.elsevier.com/locate/watres
ABUNDANCE, DIET AND SALMONELLA CONTAMINATION OF GULLS FEEDING AT SEWAGE OUTFALLS PETER N. FERNS1* and GREGORY P. MUDGE2 1
School of Biosciences, Cardi University, PO Box 915, Cardi CF1 3TL, UK and 2Scottish Natural Heritage, The Governor's House, The Parade, Fort William, Inverness-shire, PH33 6BA, UK (First received 1 July 1999; accepted in revised form 1 December 1999)
AbstractÐThe abundance and activity of gulls at sewage outfalls in South Wales and southern England was studied between 1972 and 1999. In winter, the black-headed gull was the most abundant species, followed by herring, common and lesser black-backed gulls. The abundance of black-headed gulls and herring gulls was signi®cantly correlated with the volume of sewage discharged. Sewers supported only a small portion of the gull populations present in both areas, and a higher proportion of juvenile birds were present than at other feeding sites. Sewage comminution increased the numbers of black-headed gulls feeding, but infrequent intermittent discharge reduced them by over a half. Gulls selectively consumed waste foodstus from sewage and thus helped recycle some of its organic constituents. However, some individuals carried bacterial pathogens, and could thus have contaminated nearby bodies of freshwater, or grassland, by washing and roosting there. Full sewage treatment, as planned for most of the discharges in both study areas is likely to provide the most eective means of gull control. 7 2000 Elsevier Science Ltd. All rights reserved Key wordsÐgulls, sewage outfalls, sewage discharge, Salmonella, public health
INTRODUCTION
Gulls have been observed feeding at coastal sewage outfalls since at least the end of the last century (Yarrell, 1882±84), yet there is little information available about the numbers involved or the foods they consume. The aim of the present study is to determine the abundance and feeding behaviour of gulls at sewage outfalls at contrasting sites in South Wales and in southern England. In the former area, a considerable volume of raw sewage is discharged into the Bristol Channel via relatively short estuarine outfalls. In the latter, smaller amounts of sewage are discharged further out to sea. The diet of these gulls has been determined, and tests for the carriage of Salmonella undertaken. In addition, trials have been conducted to determine whether gull numbers are aected by comminution of the sewage or by dierent rhythms of discharge. STUDY AREAS AND METHODS
The main South Wales study area extended along ca. 150 km of coast from Porthcawl (Vale of Glamorgan) in the west, to Newport (Gwent) in the east (Fig. 1(a)). A total of 252 counts of gulls were made during 48 days of
*Author to whom all correspondence should be addressed; e-mail: fernspn@cardi.ac.uk
observations at the 17 sewers in this area between 1972 and 1999. A less extensive survey was carried out at six outfalls along more than 230 km of coast near Weymouth and the Isle of Portland in Dorset (114 counts during 18 days) (Fig. 1(b)). The 24 outfalls in the two study areas varied considerably in their average ¯ow rates and their patterns of discharge (Table 1). At only seven of them was any form of sewage treatment employed, and this consisted of comminution and grit removal. Although discharge was supposed to be continuous at 15 of the sewers, in practice there was considerable curtailment of ¯ow at high tide due to hydraulic back-pressure in the pipes or to the presence of tidal ¯aps. All but three of the sewers normally discharged subtidally. On all occasions, separate counts were made of feeding and non-feeding gulls. Most feeding birds were stationed near the mouth of the outfall, but some also occurred at leaks in the pipe and along the tide edge. Gulls that were close to the outfall, but which were feeding on intertidal invertebrates, were excluded. Gull age was recorded as ®rst winter (juvenile) or adult in the cases of black-headed gulls Larus ridibundus and common gulls L. canus, and ®rst/second winter (juvenile) or adult in the larger species. Trials were conducted on the eects of sewage comminution and intermittent discharge on gull numbers at outfall nos 18 and 24. In the former trials, the comminutor was removed on two days (9 and 11 November 1976) so that raw sewage was discharged. Three days during which the comminutor was in place and operating normally served as controls (1, 3 and 10 November 1976). In the intermittent discharge trials, sewage was diverted from a sewage treatment works to outfall no. 24 either continuously
2653
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Peter N. Ferns and Gregory P. Mudge
(4 days), or for repeated ®xed periods of time each day (4 days). The ®xed periods varied between 12 and 1 12 h on dierent days. Gulls were counted at least twice an hour during these trials. The birds' diet was determined by analysing the gut contents of 10 black-headed gulls (eight adults and two juveniles) shot under licence at outfall no. 19 in November 1976, and a further 24 black-headed gulls (nine adults and 16 juveniles) at outfall nos 13 and 15 between December 1976 and March 1977. The number of guts containing dierent food items was counted after sorting, and the percentage volume occupied by each category estimated by eye. Black-headed gull droppings were collected at low tide from the vicinity of outfalls nos 13 and 15 in July 1976, January 1989 and February 1994. A total of 780 individual fresh droppings were analysed for Salmonella at Veterinary Investigation Centres in Carmarthen, Bristol and Aberystwyth. Gull counts were transformed to logarithms if this was necessary to achieve normality. If normality could not be achieved, resampling statistical methods were used. Repeated measures ANOVA was used when analysing series of counts made at the same sewer during the course of single days (Sokal and Rohlf, 1981).
RESULTS
Overall gull abundance During winter in the 1970s, a maximum of about 15,500 gulls was observed feeding at 21 of the outfalls (nos 5, 6 and 24 were not counted), of which 87% were black-headed gulls. Average counts during discharge were much lower, amounting to 6288 (84% black-headed gulls). By the 1990s, the only signi®cant change in numbers was in lesser black-backed gulls L. fuscus, which increased on average from 19 to 34 (289%). The probability of an increase as large as this being due to chance was 0.041, based on 10,000 resamplings of the pooled counts on which the means were based. Since this change in abundance only involved the least abundant species, counts were combined for the whole of the 27 year study period (Table 1). On average, throughout this period of nearly three decades, 84% of the gulls at sewers in South Wales were black-headed, compared with 79% in southern England. The equivalent ®gures for her-
Fig. 1. Location of the study areas in (a) South Wales, and (b) southern England (the scale is the same in both maps). The sewage outfalls are numbered as in Table 1.
Gulls and sewage outfalls
2655
Table 1. Sewage discharge and average winter counts of feeding gulls at sewage outfalls in the two study areas in 1973±1999 (C=comminution, G=grit removal, H=high tide discharge only, O=some discharge across the open shore at low tide, E=emergency use only). N = number of counts Outfall number
South Wales 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Southern England 18 19 20 21 22 23 24
Average ¯ow rate (Mldÿ1) (treatment and discharge rhythm in brackets) 1.1 1.5 13.6 2.6 1.7 0.5 0.2 4.5 11.4 27.7 1.4 1.8 36.8 24.1 90.9 39.4 73.0
(C) (H) (C, O) (G, C, H) (O) (G, C) (O) (G, C, H)
4.6 (C) 14.4 (C) 1.9 2.4 0.1 0.03 0.00 (E)
Black-headed gull2SE
Common gull
Lesser black-backed gull
Herring gull
N
150233 72229 372276 150225
125 40 22 0
0 0 0 0
51 11 110 76
7 7 10 7
50219 258244 5432103 108228 105224 33214 530276 476256 10692349 689240 497293
2 6 0 0 0 0 3 1 3 76 17
0 28 1 3 2 0 2 3 3 6 3
4 138 72 8 11 7 11 60 48 21 19
7 15 11 18 16 16 34 18 34 34 18
42213 78214 1322 1124 823 0
23 1 0 0 5 0
0 0 0 0 0 0
1 1 2 5 3 0
28 24 21 21 10 10
ring gulls L. argentatus were 11 and 6%, and for common gulls 5 and 15%. Common gulls only occurred in large numbers at outfalls close to coastal roosts of this species e.g. Porthcawl and Bridport. Common gulls were none the less the third most numerous species in both study areas (Tables 1 and 2). The only other species of gulls seen feeding at sewers were ®ve great black-backed gulls L. marinus in Wales, two little gulls L. minutus and two Mediterranean gulls L. melanocephalus in England. The relative importance of sewers to gulls in comparison with other feeding sites is indicated by the proportion of the total populations of each study area feeding there (Table 2). Sewers were obviously of greater importance in South Wales, which is not surprising given the fact that the total volume of euent discharged was 14 times greater than in southern England. A greater proportion of juvenile gulls was consistently recorded at sewage outfalls than at other feeding sites or at roosts (Table 3). Even the smallest dierence (proportion of juvenile herring gulls at sewers vs roosts) is statistically signi®cant (contingency w 2=114.4, P < 0.0001). The proportion of juveniles varied widely at dierent sewersÐfor example, juvenile herring gulls ranged between 19 and 58%. In this species, there was also a signi®cant correlation between the percentage juveniles and the number of black-headed gulls present (r = 0.571, n = 15, P = 0.026). The numbers of black-headed gulls were much lower during the summer months (April±August),
but the numbers of larger gulls increased. For example, between April and July, there were on average 238 2 86 (mean 2 SD) herring gulls at outfalls nos 1, 15 and 16 (the only ones counted regularly in summer), compared with 120264 in winter. Lesser black-backed gulls increased even more markedly, with 72 2 31 recorded in summer and only 9 2 8 in winter. Although large breeding colonies of both these species were situated in Gwent and Glamorgan, most of the birds at sewers were juveniles (39% of herring gulls and 22% of lesser black-backed gulls were second and third summer birds), and were therefore non-breeders. Numbers in relation to sewage ¯ow In the case of continuously discharging sewers, there were usually morning and/or evening peaks of feeding activity (e.g. Fig. 3). In many cases, gulls were already feeding at dawn, and continued to feed after dusk if sewage was ¯owing. Regardless of the time of day, peak numbers at intermittent outfalls usually occurred early in the discharge cycle and signi®cantly more birds were present when sewage was ¯owing. For example, averaging across all days of the intermittent discharge trial, 61% fewer black-headed gulls were present when ¯ow had stopped, and this reduction was statistically signi®cant (ANOVA of mean counts during each period of ¯ow; dierence between days, F = 11.0, df=3,24; P < 0.0001; ¯ow vs non-¯ow, F = 16.6, df=1,3; P = 0.027). The average ¯ow rates in Table 1 provide the only measure of the quantity of food likely to have
2656
Peter N. Ferns and Gregory P. Mudge
Table 2. Average counts (rounded to nearest 10) of the total wintering gull populations of the two study areas and the numbers feeding at sewers (1972±1999) Study area
Place counted
South Wales
Total Sewers % at sewers Total Sewers % at sewers
Southern England
Black-headed gull
Herring gull
Common gull
Lesser black-backed gull
44,970 5102 11 10,630 52 1
20,930 647 3 5700 12 0
4720 295 6 500 29 6
750 51 7 10 0 0
been available at each outfall, though they are only an index because of variations in the size of the catchment and human population served by each. There was a signi®cant correlation between these ¯ow rates and the average numbers of black-headed gulls feeding at each sewer (Fig. 2). ANCOVA showed no signi®cant dierence between the 1970s and 1990s regressions for those sewers counted in both decades and so the overall mean counts (Table 1) have been used. ANCOVA also showed no signi®cant eect of comminution and grit removal. Hierarchical ANOVA showed that there were signi®cantly fewer black-headed gulls at sewers that discharged only at high tide (F = 4.95, df=1,20; P < 0.0005). ANCOVA on continuously discharging sewers showed that the regression lines did not dier signi®cantly in slope in Wales and England, but did have a signi®cantly higher intercept in Wales (F = 29.54, df=1,18; P = 0.0004). The regressions for herring gulls were also signi®cant, and likewise diered in intercept (F = 16.80, df=1,18; P = 0.0007). There were no signi®cant correlations between numbers and sewage ¯ow in any other species. During the trial designed to determine the eects of comminution, the number of black-headed gulls feeding at outfall no. 18 between 1000 and 1400 h was 2327 (mean2SE) on control days and 2925 on comminuted days. They then rose to an evening peak (Fig. 3). Repeated measures ANOVA of the logarithmically transformed variables showed that there was a highly signi®cant dierence in abundance throughout the course of the day (F = 27.8, df=10, 30; P < 0.00001), and marginally more black-headed gulls were present when sewage was comminuted (F = 12.90; df=1, 3; P = 0.037). On average, this increase amounted to 55% (based on the arithmetic means). The numbers of feeding com-
mon gulls between 1000 and 1400 h was 31 2 4 (mean 2 SD) on control days and 30 2 6 on comminuted days. There was no signi®cant eect of comminution in this species. Relatively small numbers of black-headed gulls were present when no sewage was ¯owing during the intermittent discharge trial (13 2 3). There was no signi®cant dierence between the average numbers of black-headed gulls present on days of continuous ¯ow and those present when sewage ¯owed for 52% of the time, but there were signi®cantly fewer on the other days (Table 4; based on log numbers, during discharge only, t = 2.74, df=13, P = 0.017; whole day, t = 3.62, df=27, P = 0.001). A discharge rhythm of 1 12 h on and 1 12 h o thus did not signi®cantly reduce the number of blackheaded gulls feeding at a sewer, but less than 1 h on and 1 12 h or more o did. The reduction in numbers in the latter case amounted to about 65% during discharge, or 75% when averaged throughout the whole day (Table 4). Diet There were no signi®cant dierences in the gizzard and oesophageal contents of adult and juvenile gulls shot at sewers and so these age categories have been combined (Table 5). The most abundant item in the guts of black-headed gulls was plant debris. Most of this was grass, probably ingested by birds foraging for invertebrates on inland ®elds. Indigestible items found in gizzards included small fragments of plastic, string, matchsticks, sanitary towels and condoms. The small particle size of these items (<0.5 cm) suggests that gulls may have mistaken them for fragments of food. When only digestible items are considered, the most important component of the diet of blackheaded gulls was plant seeds (27% by volume), fol-
Table 3. Percentage of juvenile gulls in feeding and roosting winter ¯ocks in both study areas (numbers rounded to nearest 10) Site
Black-headed gulls Average number of birds
Sewage outfalls Refuse tips Fields Roosts
Herring gulls
Number aged
% ®rst winter
5150
3480
30
2480 41,770 55,600
250 2970 6560
4 4 4
Average number of birds
Number aged
% ®rst and second winter
660
930
36
17,980 4640 26,630
6020 2280 4310
18 7 20
Gulls and sewage outfalls
2657
of the sewers we studied was situated only 500 m from a boating lake that was used by the gulls feeding at the sewer for washing and preening. Clearly, a risk of contamination of such waters exists under these circumstances.
DISCUSSION
Fig. 2. Average numbers of black-headed gulls feeding at continuously discharging sewage outfalls in relation to the quantity of sewage discharged by each (d ). The regression equations were as follows: Wales, log nos=0.474logd + 1.937 (r 2=0.68, P = 0.0001); England, log nos=0.583logd + 1.123 (r 2=0.84, P < 0.01).
lowed by meat (15%). Rice grains, melon seeds and grape pips were all taken, but the commonest seed was peanuts. A peanut packaging company discharged its waste into outfall no. 15. Potato peelings were the commonest type of vegetable peelings encountered. In the case of seeds, bread, meat and fat, the particle size was small (generally < 0.5 cm diameter), but vegetable peelings were usually larger than this. Bacterial contamination Salmonellae were isolated from 49 of the 780 samples of black-headed gull droppings, giving an overall occurrence rate of 6.3%. Identi®ed serotypes (number of isolates in brackets) included S. bredeney (19), S. heidelberg (13), S. typhimurium (10), S. virchow (8), S. hadar (2), S. derby (1). All these serotypes have previously been isolated from herring gulls in Dyfed and Scotland (Williams et al., 1976; Monaghan et al., 1985). Contrary to previous results for herring gulls, however, signi®cantly more black-headed gull droppings contained salmonellae in the breeding season (12.5%) compared with winter (4.1%) (contingency w 2=19.1, P < 0.001). One
Fig. 3. Average numbers of black-headed gulls at outfall no. 18 during the comminution trial (+ or ÿ1 SE).
Despite the fact that it has a coastline that is only 65% as long, the South Wales study area supported many more gulls than the English one. This may be one reason for the higher intercept of the regression line relating black-headed gull numbers to sewage ¯ow in Wales. Another may be the fact that the English sewers discharged into relatively deep water where less food is made available to gulls than is the case with sewers discharging into shallower estuarine waters (and at three sewers across the intertidal area). The fact that there was little change in gull abundance at sewers during the 27 years of this survey re¯ects the stability of both the food supply and gull populations during this period. The increase in lesser black-backed gulls between the 1970s and 1980s was broadly in line with that recorded nationally at winter roosts during approximately the same period (Bowes et al., 1984). While 11% of the wintering population of blackheaded gulls in South Wales fed at sewers, this compares with about 5% at refuse tips, 12% on the shore and 70% on ®elds. Refuse tips are of greater importance to herring, lesser black-backed and great black-backed gulls, supporting 43±75% of their populations. Only 1.3% by volume of the foods taken by herring gulls to their chicks on Steep Holm consisted of material derived from sewers. None was fed to chicks at other colonies by this species or by lesser and great black-backed gulls (Mudge and Ferns, 1982). In the only previous quantitative study, Fitzgerald and Coulson (1973) found that sewage outfalls along the River Tyne were widely utilised by black-headed and herring gulls, but to a smaller extent by lesser black-backed gulls, common gulls and kittiwakes Rissa tridactyla. Hulscher (1985) has suggested that the occurrence of a high percentage of juvenile black-headed gulls is an indication of a poor feeding site. Juvenile gulls generally have a lower rate of foraging success than adults (Verbeek, 1977; Greig et al., 1983), either because they are less experienced or because adults aggressively interfere with their feeding, sometimes forcing them to feed in less favoured sites. The fact that relatively more juvenile gulls occurred at sewage outfalls than at other feeding sites therefore suggests that sewers may be less preferred areas. One reason why relatively more juvenile herring gulls are attracted to sewers with large numbers of black-headed gulls may be that they specialise in kleptoparasitising the smaller species (c.f. Fitzgerald
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Peter N. Ferns and Gregory P. Mudge
Table 4. Average numbers of black-headed gulls present at outfall no. 24 under dierent discharge conditions. N = number of days (number of counts in brackets) Discharge
Percentage of time for which sewage ¯owed
Continuous Intermittent
Average numbers of black-headed gulls (2SE)
100 52a 27b
N
Whole day
N
During discharge only
4 (50) 1 (25) 3 (27)
5226 4525 1321
4 (50) 1 (14) 3 (33)
5226 5527 1823
a 1
1 2 h on, 1 12 h o. 3 1 2 ± 4 h on, 1 2 ±3 h o.
b1
and Coulson, 1973; Verbeek, 1977). Such behaviour was also observed at many of our sewers. Comminution increased black-headed gull numbers by 55% in this study. This is probably because it increased the amount of sewage solids in the size range consumed by black-headed gulls (<0.5 cm diameter) from 53 to 72% (measured at outfall no. 18). Smaller particles may also be swept to the surface more readily and may spread out over a wider area. Intermittent discharge reduced numbers by more than half when the discharge period was less than 1 h, and the interval between discharges lasted at least 1 12 h. However, as a potential method of reducing gull numbers, it is doubtful whether intermittent discharge is viable. Few outfalls could be operated in such a way, given the practical diculties of switching ¯ow on and o, and the consequent reduction in discharge time. The use of diusers at sewage outlets (not used at any of the outfalls in the present study) can substantially reduce the tendency of the freshwater, in which the sewage solids are suspended, to ¯oat to the surface and this form of management might therefore be worth investigating. The gizzard and oesophagus contents of gulls at sewers showed that many of them also fed on intertidal or inland invertebrates. This was most marked in black-headed gulls in southern England, where 9% of the diet consisted of invertebrates which could have been obtained inland. There was no evidence from this examination of gut contents, or from direct observations of feeding birds, that gulls consumed material derived from human faeces. This is despite the fact that
other species have been observed consuming animal faeces, notably glaucous gulls L. hyperboreus eating seal droppings (Ryder, 1957) and ivory gulls Pagophila eburnea eating polar bear droppings (Bateson and Plowright, 1959). Gulls appear to be opportunist feeders at sewers, just as they are at other sites, choosing whatever waste foods happen to be available. The average particle size of food items available at sewers was very small and presumably does not often provide an adequate return for the larger species. This helps to explain why black-headed gulls are the commonest gulls at outfalls even though larger species, such as herring and lesser black-backed gulls, are capable of displacing them from the best feeding positions. Food processing wastes, such as the peanuts at outfall no. 15, can be of considerable importance and such wastes are known to be exploited by other species. For example, wintering ducks in Scotland fed on spent barley discharged by distilleries in the 1970s (Campbell, 1978), but their numbers declined as soon as this source of food was no longer available. The other main categories of food taken by gulls (seeds, meat, vegetable peel and bread) may be of both domestic and commercial origin. Small particles of such materials are ¯ushed down the drains of most households and catering establishments. The diet at sewers is remarkably similar to that at refuse tips, and diers more in particle size than in the nature of the particles consumed. The overall rate of occurrence of salmonellae in the black-headed gull droppings we collected near sewers (6.3%) was lower than that recorded for herring gulls in both Dyfed (22.2%) (Williams et al., 1976) and the Clyde area of Scotland (10.1%)
Table 5. Gizzard and oesophagus contents of 34 black-headed gulls shot whilst feeding at sewage outfall nos 13, 15 and 19 Type of food Plant debris Plant seeds Meat Arthropods (Diptera, Coleoptera, Araneae) Indigestible material Bread Unidenti®ed organic matter Vegetable peelings Other invertebrates (Lumbricidae, Oniscidea) Fish bones
Number of guts containing item
Percentage volume
30 29 23 16 15 6 4 3 6 3
34.3 27.2 15.3 8.9 5.5 2.9 2.8 2.5 0.4 0.2
Gulls and sewage outfalls
(Monaghan et al., 1985). In the former case, S. bredeney was the commonest isolate, as in the present study. In the latter case, it was S. virchow, and there was a signi®cant positive relationship between the rate of occurrence of salmonellae in gulls and the number of human cases reported by local hospitals. In both of these earlier studies, the herring gulls tested scavenged at refuse tips, rather than at sewage outfalls and the relationship was presumably a consequence of humans and gulls consuming the same contaminated foods. Monaghan et al. (1985) considered that the reason herring gulls at breeding colonies carried more salmonellae than those at refuse tips was that they had been feeding at sewage outfalls. This is supported by the high rates of occurrence recorded near sewage outfalls by Fenlon (1983) (17±21%), and at sewage works (55%) (Fenlon, 1981). Our results indicate that for blackheaded gulls at least, the occurrence rate is not always high at sewers, at least during winter when the largest numbers of gulls are present. Gulls represent a potential route for the transmission of pathogens and parasites by gulls to playing ®elds, pastures and reservoirs. For example, gulls have been implicated in the transmission of the eggs of the human tapeworm Taenia saginata and salmonellae from sewage to cattle (Silverman and Griths, 1955; Reilly et al., 1981), and in the contamination of reservoirs with faecal streptococci, salmonellae and Escherichia coli (Fennell et al., 1974; Monaghan et al., 1985). A range of other disease-causing organisms, such as Bacteroides fragilis, are also present in sewage and can remain viable for 48 h, even after dilution in fresh water (Shoop et al., 1990), and these too could be transferred by gulls from sewers to lakes and reservoirs. Of perhaps the greatest concern is the fact that E. coli 0157 has been identi®ed in the droppings of gulls at a land®ll site in Morecambe Bay (Wallace et al., 1997). Even if it were desirable to do so, there is no easy way of preventing gulls from feeding at sewage outfalls, short of complete euent treatment. In both study areas, considerable changes in sewage disposal are already taking place. For example, full treatment for all the South Wales outfalls should be in place by 2002, though the existing outfalls will still have to be used during storm conditions. In southern England, a large storage tank has been constructed at Hengistbury Head, and a membrane treatment plant has just been completed at Swanage. Welsh Water Plc has indicated that all coastal and estuarine discharges will eventually receive at least secondary treatment. This will not necessarily remove all faecal indicators from such coastal waters, since birds (including gulls, waders and wildfowl) which excrete faecal coliforms, streptococci and perhaps Campylobacter lari have been implicated in the continued contamination of Morecambe Bay after the introduction of secondary sew-
2659
age treatment (Obiri-Danso and Jones, 1999). These changes should lead to a substantial improvement in water quality, however, and the loss of feeding opportunities for birds is unlikely to have serious consequences for local gull populations. AcknowledgementsÐThe early surveys in South Wales were commissioned by the Nature Conservancy Council (South Wales Region) and in southern England by D.A.F. Coney and Sons Ltd. GPM was in receipt of a NERC studentship during part of this work. We are grateful to Welsh Water Plc for supplying details of all the sewers in South Wales, and to Wessex Water Plc for their cooperation during the experiments in southern England. We would also like to thank M. K. Brummage, G. P. Green, J. M. Hope, C. Prescott, J. Rees, I. S. Robertson, J. B. A. Rochard, D. Roscoe, A. G. J. Tacon, K. Thomas, W. A. Venables and J. Woodworth for help with various aspects of the ®eldwork and S. A. Hinsley and C. Johnson for commenting upon drafts of this paper. REFERENCES
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