Bracken (Pteridium aquilinum): Its distribution and animal health implications

BT. uet. ]. (1990). "6, 316

REVIEW BRACKEN (PTERIDIUM A QUILINUM ): ITS DISTRIBUTION AND ANIMAL HEALTH IMPLICATIONS

A. HOPKINS AFRC Institute for Grassland andEnmronmmtal Research, North Wykt, Okthampton,

Deoon EX20 2SB

INTRODUCTION Bracken (Pteridium aquilinum L.) has long been known to have deleterious effects when eaten by livestock and it has been implicated in several animal health problems throughout the world. In Britain, reported cases of bracken poisoning of cattle in recent years have averaged about 20 a year, with considerably greater numbers in particular years such as 1984 (Ministry of Agriculture, Fisheries and Food (MAFF), 1985). However, the extent of bracken-related animal health disorders is probably greater than these data alone suggest. In the UK bracken is by far the most common of the fern species and occurs in a range of environments-woodland, heathland, open moorland, enclosed pasture and on coastal headlands, field margins, commons and roadside verges. The widespread geographical distribution of bracken is indicated by records of its occurrence in most of the 10 km grid squares in the British Isles (Perring & Walters, 1962). Several studies have reported increases in bracken for different areas of Britain, e.g. Birnie (1985), Taylor (1985) and Brown (1986) for Scotland, Wales and North Yorkshire, respectively. Bracken is reported to be extending its range into wet and exposed habitats at its climatic limits. Estimates of encroachment rates have been put at 1%, and sometimes 3% per annum (Taylor, 1985). Concern at the spread of bracken has been expressed for several reasons. As a result of successful competition with herbage species it reduces the quantity and quality of the herbage for grazing livestock. Second, bracken fronds and rhizomes, and also its spores, contain toxic substances which can prove fatal to livestock and pose animal and human health risks. Third, bracken harbours a number of parasites including the sheep tick tLxodes ricmus), injurious to both sheep and grouse (Hudson, 1986).

TOXICITY AND HEALTH CONSIDERATIONS Detailed reviews of the chemical composition of bracken and diseases attributed to bracken have been reported elsewhere (e.g. Cooper &Johnson, 1984; Fenwick, 1988; W. C. Evans, 1989). The acute and chronic diseases associated with bracken poisoning may be summarized as follows.

BRACKEN

31 7

Acute effects Avitaminosis BI is caused by an enzyme in bracken, thiaminase. The condition, whose effects are essentially those of vitamin BI deficiency , is more likely to occur in monogastric animals which are dependent on dietary thiamine, though it has been produced experimentally in mature ruminating sheep fed a diet containing 15-30% bracken rhizome (W. C. Evans, 1986). The condition has been described for the horse (Roberts et aL, 1949) and the pig (LA. Evans etaL , 1963). Acute haemorrhagic syndrome is attributed to toxins other than thiaminase and is associated with a severe depression in bone marrow activity. The condition is cumulative and usually results from consumption of young bracken fronds or rhizome for a period of 2-4 weeks (W. C. Evans, 1989). Cattle are reported to be more vulnerable than sheep, though losses in sheep have been reported (Parker & McCrea, 1965).

Chronic effects Bovine enzootic haematuria (BEH) is a chronic form of bracken poisoning found in ruminants and is characterized by haemorrhages in the urinary bladder and, in some cases, by tumours of the bladder wall. The condition has been reported in Britain and several other countries where livestock are exposed to bracken, including New Zealand and Latin America Garrett et al. , 1978; Smith et al. , 1988; Villalobos-Salazar et al., 1989). The condition may occur in association with neoplasia of the alimentary tract. Jarrett et aL (1978) have described a possible interaction between bracken carcinogen(s) and a bovine papilloma virus. Carcinoma of the upper digestive tract of cattle has also been reported from bracken affected areas of northern Britain Garrett et al., 1978; Grimshaw, 1983). Further evidence of carcinogenic, mutagenic and teratogenic effects of bracken toxins has been reviewed by LA. Evans (1986, 1987). Pamukcu et aL (1978) and Villalobos-Salazar et aL (1989) cite evidence that deliberate feeding of bracken or bracken extracts has produced lung, bladder and intestinal tumours in a range of laboratory animals, including cows, rats , mice, guinea-pigs and qu ails. McCrea & Head (1978, 1981) have described work on experimental tumour formation in sheep; the commonest tumours associated with bracken consumption are fibrosarcomas affecting the mandible, leading to facial distortion and tooth loss. Bright blindness had been known to affect sheep on hill land before the condition was formally recogn ized by Watson et aL (1965) and subsequently reproduced experimentally by feeding a diet containing bracken to sheep (Watson et al., 1972; McCrea & Head, 1981).

Milk pathways The passage of bracken toxicity into milk was demonstrated by l.A. Evans et aL (1972) and subsequent studies have confirmed that milk from cows fed on a diet which includes bracken contains carcinogenic, toxic and mutagenic metabolites not present in the milk of normal cows (Pamukcu tl al., 1978; l.A. Evans, 1987). This has implications for the health of livestock reared in areas of bracken affected pastures. Consumption of milk or milk products from cows fed on bracken affected pasture has also been identified as a potential human health hazard (Galpin & Smith, 1986). l.A. Evans et aL (1971) and l.A . Evans (1986) refer to high rates of human gastric cancer with obscure aetiology prevalent in Japan and north Wales , and to a high incidence of leukaemic cancer in north Wales and recommend that milking cows should be denied access to bracken infested pastures, especially if the milk is to be retailed locally rather

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than bulked with other supplies. North Wales formerly had the greatest density of milk producer-retailing farms in England and Wales supplying unbulked milk to local customers (Galpin & Smith, 1986). In Costa Rica, Villalobos-Salazar (1985) and Villalobas-Salazar et al: (1989) have described a positive correlation between the incidence of gastric cancer and consumption of milk contaminated with bracken-derived carcinogens, with marked differences between populations in bracken infested and bracken free regions of the country.

DISTRIBUTION OF BRACKEN IN BRITAIN AND ITS RELATIONSHIP WITH LIVESTOCK FARMING Estimates of the extent of bracken in Great Britain have been made by Taylor (1985, 1986) and by Birnie (1985) using data from various sources. Taylor quotes areas ofland affected by bracken of 1241 km 2 in Wales and 4720 km 2 in Scotland with rates of spread of up to 3% per year in some localities (e.g. western Powys and parts of Kincardineshire). Some other estimates are lower (Bunce et al; 1980). However, both Taylor and Birnie acknowledge that the extent and spread of bracken has not been well documented, particularly for England and Scotland. Information on the incidence of bracken in pastures and enclosed rough grazings has been recorded in a series of farm surveys conducted by the Institute for Grassland and Animal Production (IGAP) formerly the Grassland Research Institute. Surveys of grassland farms covering the whole of England and Wales were carried out in 1970-72 (Green, 1982) and in 1974-77 (Forbes et al., 1980) which included field-by-field botanical assessments on 1829 farms, representing 96 000 hectares of grassland. More recent information was collected in a regional survey of farms in south-west England in 1983 (Hopkins et al., 1985) and of upland districts of England and Wales in 1986 (Hopkins et al., 1988). These later surveys covered 18000 hectares, the majority of which had been included in the 1970-72 sample, enabling some assessment of changes over time . The incidence of farms and fields affected by bracken is summarized in Table 1. Bracken was recorded if its contribution amounted to at least 5% of the vegetation in each field surveyed. In the 1986 upland survey, provision was made for recording lesser amounts (2-5% of the vegetation) though if bracken was present it usually contributed in excess of this amount. There were marked differences in the incidence of bracken between the national surveys, where an average of 10% of farms had bracken recorded in one or more fields, and the two regional surveys. Approximately half of the farms in south-west England had bracken recorded, and one-third of those in the upland sample had some pasture which contained bracken. The high incidence of bracken in south-west England and in Wales is also ind icated by an analysis of the geographical distribution of farms with bracken in the two national surveys from 1970-72 and 1974-77. Of the 187 farms where bracken was recorded 96 were in Wales or the Welsh border counties and 34 were in south-west England. Evidence of an increase in bracken has been provided by a comparison of records from the 1986 survey with those for the same farms included in the 1970-72 survey. The number of swards where bracken was present was about 30% greater than when the same farms were surveyed 15 years earlier (Hopkins et al., 1988). The extent to which livestock may be exposed to bracken is probably greater than the survey data suggest, as it frequently occurs on field margins which would not necessarily have been recorded.

319

BRACKEN

Table I Incidence of bracken in grassland and enclosed rough grazing in England and Wales as recorded in surveys 1970-86

(1) 7970-72 All England & Wales

(2) 7974-77 All England & Wales Permanent grassland farms

(3) 1983 South-west England

(4) 7986 Upland areas of of England & Wales

1327 68000

502 28000

127 8000

145 10000

No. farms where bracken was recorded: dairy non-dairy

50 67

10 60

34 33

23 34

No. of fields where brackenwas recorded: dairy non-dairy

104 179

14 152

61 172

32 159

Survey

No. farms surveyed Area surveyed (ha)

Source: (1) Green (1982), (2) Forbes et al: (1980),(3) Hopkins et al: (1985),(4) Hopkins et al: (1988).

These surveys have also shown that bracken was not confined to sheep and beefrearing farms but was present on a significant number of farms that had dairy cows. However, where it occurred on dairy farms its contribution was generally low, and the dairy animals did not necessarily have access to the bracken affected fields. However, there were some notable exceptions to this and in the 1986 survey there were several dairy farms in west Wales where infestations of bracken affected up to 40% of the pasture. Some general features can be identified which are associated with grassland affected by bracken. Fields where bracken occurs are mainly old permanent pastures, usually agrostis and fescue grassland. The majority are at elevations above 150 m and on relatively steep slopes (> 8 degrees) in many cases with additional limitations to grassland management (outcrops, ground irregularities, etc.) which result in land being subject to extensive management for grazing rather than mowing. Nevertheless, in southwest England there is a greater incidence of bracken at low elevations, in grassland not affected by physical problems, in some cases having been reseeded in recent years. No comparable grassland survey data exist for Scotland though an earlier indication of the distribution of areas with bracken infestation was provided by Hendry (t 958). This showed the greatest incidence in Dumfries and Galloway, Argyll and parts of Grampian and the Borders. A current programme to map the extent and spread of bracken on Scottish hill land was described by Birnie & Miller (1986). Birnie (1985) reported that preliminary results of a remote sensing-based survey indicated that the bracken area of Scotland had increased since the 1950s and that locally this increase had been dramatic. Remote sensing has also been used to monitor bracken encroachment in the North York Moors (Weaver, 1986), an area which was not well represented in the IGAP grassland

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BRITISH VETERINARY JOURNAL, 146, 4

surveys. Brown (1986) has noted that the distribution of bracken in the North York Moors is mainly associated with marginal steep slopes and moorland valley sites but that it is now spreading on to some wetter peaty soils; at least 20% of the existing moorland is now dominated by the species. Information from the Soil Survey of England and Wales (SSEW) provides further evidence of the association between bracken and soil type. Thompson et al. (1986) note that bracken is now widespread on brown podzolic soils of the Manod and related series on slopes in excess of 5 degrees. These comprise about 20% of the land in Wales and coincide, in part, with the largest dairying areas of Dyfed and adjacent counties. The authors note that bracken in Wales currently occupies only a small part of the potential range. Unfortunately, SSEW do not have comparable information on the distribution of bracken in England, the land use data for Wales having been recorded in greater detail (T.R.E. Thompson, personal communication). However, descriptions of soils and land use in SSEW Regional Bulletins accompanying the 1:250000 national soil map (Soil Survey of England and Wales, 1983) describe soil types on which bracken occurs (Findlay et al., 1984; Hodge et al., 1984; M.G. Jarvis et al., 1984; R.A.Jarvis et al., 1984; Ragg et al., 1984; Rudeforth et al., 1984). These sources provide an indication of the distribution and potential area of bracken prone soils. The area occupied by these soil types is considerably less for England as a whole (about 7%) than for Wales (about 20%) (Hopkins, 1988). The Manod association, which accounts for about 70% of the Welsh bracken prone land, and about 50% of the smaller area of bracken prone land in south-west England, is less extensive elsewhere in England. In England bracken may be present on soils of the Bangor, Belmont, Denbigh 1, Moor Gate, Moretonhampstead, Shirrel Heath and Curtisden associations. Its potential distribution is wide though apparently not as extensive as in Wales. Grazing management offers some scope for the partial control of bracken; the tramping action of cattle is more effective than that of sheep in crushing young bracken plants. However, the spread of bracken in recent years, particularly on enclosed land in upland areas, may have been hastened by the increase in sheep numbers and a corresponding reduction in cattle. Between 1971 and 1986 the number of breeding ewes in Wales increased by 42% (MAFF, 1972, 1987). Pasture reseeding and more intensive management through fertilizing and mowing have kept bracken out of the better lowland pastures. In previous generations bracken was also partly controlled by cutting, the plant having been used as a thatching and bedding material and for some industrial products (Rymer, 1976). Future changes in British agriculture, with a decrease in the intensity of management, may lead to more marginal land taken out of production or farmed at a lower level of output. This could lead to a greater spread of bracken in some areas and a potential for more bracken-related livestock disorders.

VETERINARY REPORTS OF BRACKEN POISONING IN CATTLE Reported incidents of bracken poisoning are published by the Ministry of Agriculture, Fisheries and Food (MAFF, 1985). Further information on the distribution of these incidents was supplied by the Central Veterinary Laboratory and from Veterinary Investigation (VI) Centres covering areas with a high incidence of bracken poisoning.

BRACKEN

321

Between t 977 and t 987 there were 233 recorded incidents of bracken poisoning of cattle in Great Britain, some of which involved more than one animal. The geographic distribution of these is shown in Fig. t and for each of the successive years in Table II; over 50% were from Wales or south-west England.

-'" <,~ales,94

....

.:

\

.. , -. ".

;" ."

:'.. ..

r> •... , ' ,"

"

"

.':..

\

\

.. , .f "

.:. 'f .''.' .f

\ .\ "'

South- west England, 33

\.

'.

~

South er n Englan d . 10

- 1. Midlands and eostern England, 7

Fig. 1. Regional distribution of 233 incidents of bracken poisoning of cattle, 1977-87. Source: Ministry of Agriculture, Fisheries and Food VIDA Statistics.

The number of reported incidents of bracken poisoning in cattle varied considerably between years, e.g. from five in t 987 to 68 in t 984, suggesting that weather conditions may affect the likelihood of cattle ingesting bracken. In Table III the April-September rainfall is given for sites in each of the areas shown in Table II; for many of these sites rainfall was lower in t 984 than for other years for which data are presented. Schoental (1984) has also referred to severe outbreaks of fatal intestinal damage in t 893 after a prolonged drought and suggested that low nutritional levels might have made cattle more susceptible to toxic agents in bracken. Hunger during periods oflow availability of herbage may cause animals to graze plants that they would otherwise avoid. An improved understanding is needed of factors likely to result in livestock eating bracken and the causes of outbreaks in particular seasons. As a result of the relatively high incidence of bracken poisoning of cattle in Wales and south-west England, the location and type of cattle involved were examined for the incidents covered by the VI centres at Bangor and Carmarthen (Wales) and Starcross (Devon). The Starcross records were for t 983-85 only and related to 10 incidents, two of which involved dairy cattle in north Devon. A cluster of incidents on the eastern side of Dartmoor involved beef cattle only. Data for the two Welsh VI centres covered 68 incidents, at least 29 of which involved dairy cattle. They cover the period 1977-87. The incidents were well distributed within the areas covered by these two VI centres and the

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BRITISH VETERINARY JOURNAL, 146, 4

Table II Incidents of bracken poisoning in cattle in Great Britain, 1977-87 77

Wales Scotland Northern England· Midland and east Englandj Southern Englandj South-west England Total

8 11 1 2 1 3 26

78 11 6 5 1 1

79 9 4

24

14

80 5

6

81 3 6 1 3 13

82 3 8 1 1 1 14

83 7 3 1

84 31 12 6

6 17

5 14 68

86 3 7 1 1 1 2 15

87 1 4

85

86

87 478 446

85 18 7 1 1 4 31

5

·VI centres at Newcastle, Penrith & Thirsk. tVI centres at Sutton Bonington, Shrewsbury & Worcester. *VI centres at Reading, Winchester, Wye & Cambridge. Table III April-September rainfaII (mm) for successive years 1977-87

Wales 1. (Bangor) 2. (Carmarthen) Scotland 1. (Dumfries) 2. (Fortrose) Northern (Leeming) Midlands (Sutton Bonington) Southern (Hurley) South-west (Starcross)

77

78

79

81

82

417 263

426 291

421 435

370 400 526 617

423 517

519 349 554 496 346 711

371 614

374 291 342 261

416 272

479 412

491 283

401 325

392 241 324 197

480 578 278 337

214

301

317

321

295

307 320 210 375

339

321

272

283

281

316

313

398

299 299

334

297

332

367

298

318

368

382

301

280 305

349 302

309

237

213

296

314

373

347

369 207

282

281

80

83

84

681 312

372

Source: AFRC Meteorological Data System.

location of the farms on which they arose has been compared with published SSEW maps (1983). It was earlier noted that in Wales bracken was most widespread on podzolic brown earth soils of the Manod and related series (Thompson et al., 1986). In the north Wales area at least half of the reported incidents of bracken poisoning were on farms where Manod soils occurred. In the Carmarthen area only about a quarter of the incidents were from farms on this soil, a high number being on land mapped as Denbigh 1 and Milford associations. Incidents of bracken poisoning in Devon were mainly from areas where podzolic brown earth soils (Manod, Moretonhampstead and Denbigh 2 associations) occurred. Whilst this information is subject to the limitations of interpretation of soil maps and other variable factors (e.g. livestock being grazed on land away from the farm) it may be concluded that bracken poisoning of cattle occurs predominantly in areas on podzolic brown soils.

BRACKEN

323

Additional evidence which shows that the incidence of animal health problems associated with bracken toxicity varies with bracken distribution was reported by Grimshaw (1983). Cattle routinely admitted to the University of Glasgow Veterinary Department were found to be affected by upper alimentary squamous cell carcinoma and urinary bladder neoplasm. Neoplasms examined in detail exhibited various distinctive patterns of age prevalence and breed distributions and factors involved were considered to have acted continuously throughout the life of the animal. The geographical distribution of the farms of origin of 978 adult cattle was related to the distribution of bracken in Scotland using the map of Hendry (1958). Hendry had identified the western areas as containing 44% of the bracken infested land of Scotland. Grimshaw reports that 71% of upper alimentary papillomas were from areas with severe bracken infestation and only 12% from areas with light or nil infestations. Sixteen farms were identified from which two or more animals with malignant neoplasms were referred and the majority were concentrated in relatively localized areas with severe bracken infestation. Regional variations in the toxicity of bracken, as influenced of soil types or differences between genotypes, may also affect the distribution of bracken related disorders. Evidence for such variation has been reported from New Zealand; Smith et al. (1988) conducted laboratory trials with rats fed diets containing bracken from two sites (one site having a high local incidence of bovine enzootic haematuria). Very marked differences in carcinogenicity were recorded ; neoplasms occurred in 85% of rats fed from the BEH site compared with 11% of the other group. If similar regional variations in bracken toxicity existed in Britain the animal health implications would be considerable. Reported incidents of bracken poisoning of cattle in Britain are comparatively few in most years, though locally may be of importance and represent a considerable economic loss on affected farms. Other cases may not be diagnosed, or else recognized locally but not recorded in MAFF VIDA statistics. Reported figures for bracken poisoning of sheep are also very low. Hannam (1989) reported that farmers frequently recognize jaw tumours and bright blindness in the early stages so that affected animals may be sold at salvage value before too much body condition is lost. The full extent of bracken-related disorders may, therefore, be greater than the official statistics of poisoning incidents alone suggest.

CONCLUSIONS Bracken is widespread in the British Isles, affecting enclosed grassland as well as rough grazings. There is evidence that it has increased in recent years , particularly in Wales. If ingested, bracken can be responsible for a number of livestock disorders. Reported incidents of bracken poisoning are comparatively few, though may be of importance locally . However, the extent of bracken-related disorders is probably greater than official figures alone indicate. There is considerable between-years variation in the numbers of reported incidents of bracken poisoning. The extent to which weather conditions contribute is unclear, though the problem has been greater in years with below average summer rainfall, e.g. 1984. Surveys have shown that bracken occurs on enclosed grassland on about 10% of grassland farms in England and Wales; farms affected are predominantly in Wales, the Welsh border counties and south-west England. These regions also have the highest

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incidence of bracken poisoning of cattle. In upland areas bracken occurs on over 40% of beef/sheep farms and on 30% of farms with a dairy enterprise. On most farms where bracken occurs it affects only a small proportion of the grazing land, usually old permanent pastures on steep slopes. There is an association between bracken and soil type, it being most prevalent on brown podzolic soils. Bracken poisoning incidents coincide, in part, with these soils, though also occur on farms on other soil types. Future changes in British agriculture, with a decrease in intensity of farming in some areas, may lead to an increase in bracken and a potential for more incidents of brackenrelated livestock disorders.

ACKNOWLEDGEMENTS

The research upon which this review is based was funded by an open contract from the Ministry of Agriculture, Fisheries and Food. The author is grateful to colleagues in the MAFF Veterinary Investigation Centres who provided information on the incidence of bracken poisoning and to colleagues in many other organizations whom he consulted during the preparation of this review.

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ANNOUNCEMENT Fifth Congress of the European Association for Veterinary Pharmacology and Toxicology

Copenhagen, Denmark, 18th-22th August, 1991 The 5th Congress of the European Association for Veterinary Pharmacology and Toxicology will be held at the Royal Veterinary and Agricultural University, Copenhagen, from 18th-22nd August, 1991. Further information and registration forms can be obtained from: 5th Congress of the European Association for Veterinary Pharmacology and Toxicology, c/o Symposium International, Karlebogard, 91 Karlebovej, DK-3400 Hillerod, Denmark.