Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning

Summary

Pesticides are widely used in agriculture but many have adverse effects on non-target wildlife. Most rodenticides are anticoagulants and recent studies from around the world have demonstrated extensive exposure of many non-target species to such poisons which are commonly used to control or eradicate pest species such as rats Rattus spp. Anticoagulants are toxic to all vertebrates. Anticoagulant rodenticides are categorized as either second-generation (1970–1980s) anticoagulants e.g. difenacoum, bromadiolone, brodifacoum and flocoumafen, or first-generation (1940–1960s) e.g. warfarin, pindone and coumatetralyl. Second-generation rodenticides are more potent. Use of rodenticides on farms in the UK increased from 74% in 1992 to 89% in 2000.

This study investigated the impact of secondary poisoning during routine brown rat Rattus norvegicus control on non-target small mammal species.

Study areas: The study was undertaken at two rural farmland localities in central England.

Farm 1 - a mixed (arable and sheep) farm and game estate in Leicestershire; brown rat Rattus norvegicus infestations were less severe than farm 2 and were controlled once or twice a year. Pheasant (Phasianus colchicus)-feeder sites were present on the farm adjacent to arable fields: feeder sites 1 and 2 were near streams bordered by thick hedgerows interspersed with deciduous trees and scrub grassland; feeder site 3 was within a mixed deciduous-coniferous copse. Each pheasant-feeder site contained several feeders and grain spilled by pheasants was accessible to rats.

Farm 2 - an intensive pig farm in Northamptonshire Farm with severe brown rat Rattus rattus infestations within pig units and along field boundaries. Rats were controlled using rodenticide in large-scale operations, three to four times a year.

Rat baiting: Sites were surveyed for rat activity in order to determine best baiting sites. Bait points were set close to burrows and in areas of concentrated activity, revealed by rat runs and droppings. Studies were conducted as follows (dimensions define areas with intensive rat activity and where small mammal populations were studied):

Farm 1 (190 × 100 m), February 2002; pheasant feeder 1 (10 × 150 m), March–April 2002

Farm 2 (100 × 115 m), June 2002; pheasant feeder 2 (15 × 160 m), July–August 2002; pheasant feeder 3 (50 × 80 m), September–October 2002

There were 15–30 bait points per site (number and spacing dependent on extent and density of rat populations). Bait points comprised plastic bait trays inside a wooden box (40 × 15 × 15 cm) open at each end. Weighted rectangles of hardboard set against the ends of bait boxes at an angle prevented entry by birds. The active ingredient in the rodenticide used was coumatetralyl (375 mg/kg; trade name Racumin), a first-generation rodenticide with a half-life of 55 days in rat liver and of relatively low toxicity to birds. This was important as red kites Milvus milvus (a protected species and subject of a reintroduction programme in the UK) were present.

Bait points were pre-baited for 1 week, then for 10 days (typical practice) baited with 100 g coumatetralyl. Bait points were checked daily. If all bait was consumed (complete take), the quantity of bait was doubled to 200 g. Where takes were partial, they were topped up to 100 g or 200 g every 4 days to maintain a surplus. This surplus-baiting strategy is a standard approach.

Mammal trapping: Small mammals were live-trapped using Longworth traps to monitor bait exposure and estimate small mammal populations. Fifty traps were placed in pairs in a grid system, located according to habitat and marked with a numbered cane within and around the baited area independent of bait points. Traps were filled with hay for bedding and warmth, and rolled oats for food. Fly castors were provided in case shrews (Sorex spp.) were accidentally captured. Traps were set at dusk and checked at dawn to cover active periods of study species (wood mouse Apodemus sylvaticus, bank vole Clethrionomys glareolus and field vole Microtus agrestis). Animals were identified, sexed, weighed, marked by hair-clipping and released.

Population estimation: Population estimates were made before and after baiting. Following a trap pre-bait period of two to three nights, trapping was carried out for five nights and population size was estimated using mark–release–recapture (MRR). Identical trapping sessions were carried out 5 days after application of bait. The Cormack–Jolly–Seber (CJS) method of population size estimation was applied to MRR data. Study areas were defined by extent of rat infestations and area of small mammal trapping; no site was isolated from surrounding small mammal habitat.

CJS estimates are imprecise when number of marked animals in each sample is below 10, but as rodenticide treatment sometimes left insufficient marked animals for a species-specific CJS estimate, estimates were made for the total small mammal community. At Farm 1, estimates was repeated after 3 months in order to estimate population recovery.

Rodenticide exposure: Small mammals invariably defecate within the trap tunnel. Rodenticide exposure was shown by the presence of a bait marker dye, pre-mixed with rodenticide bait, in faeces. Although the bait was already dyed blue, an additional tasteless blue dye (Chicago Sky Blue 6B) was also added (700 mg/kg) to ensure exposure was reliably identified.

Inspections of rat bait boxes provided evidence of small mammal feeding (grain remains and faeces). Tracking tiles were also used to record footprints of animals entering. Small mammal trapping continued through the first 5 days of rodenticide application, in order to record bait exposure. The rodenticide effect is delayed, resulting in death 4–10 days after consumption of a lethal dose. Some exposed individuals would have died or been close to death after 5 days. During the second 5 days of rodenticide application, another small mammal population estimation was carried out.

Reference populations without rodenticide: Small mammal population densities fluctuate widely and numbers are influenced by short-term climatic extremes. Reference populations were therefore monitored simultaneously in order to distinguish effects of rodenticide treatment from natural fluctuations. Reference sites, 300–1,000 m from treated sites, were selected on the basis of similar habitat structure. Fifty traps were placed at reference sites in the same manner as in treatment sites and trapping was performed in tandem.

Small mammal exposure: Wood mice and bank voles were trapped at all five sites, field voles at two and house mice Mus musculus at farm 2 only. Small mammal visits to bait boxes were evident by tracks on tracking tiles. In every trial, both rat and small mammal footprints were found on individual plates. Small mammal faeces were found scattered in bait boxes and within bait, showing that they fed while sitting in the bait and from the tray edge. Small mammal feeding was also evident from scrutiny of feeding remains.

The primary indicator of bait ingestion was the presence of blue-coloured faeces in Longworth traps. Blue dye was generally obvious but when uncertain, closer investigation (squashing or breaking open droppings) confirmed the presence of dye. Overall, 48.6% (n = 938) of small mammals trapped had fed on the rodenticide. Proportions ranged from 32% (n = 129) at pheasant feeder 1 to 67% (n = 363) at pheasant feeder 3. All four species that were trapped had eaten bait, although apparently to different degrees: of those wood mice trapped, overall 57.4% (SD ± 14.5%) had eaten bait, bank voles 30.6% (± 12.6%), field voles 19.5% (± 2.1%) and house mice 30%.

Consequences of exposure: Following introduction of rodenticide (replacing pre-bait) a high proportion of traps contained dyed faeces the next day. The first signs of poisoning in small mammals were observed 2–3 days later. Bleeding from nose, ears, anus and vagina was noted in live wood mice and bank voles. They showed reduced escape responses, sometimes staggering and with unco-ordinated movement. Animals dead in traps accompanied by dyed faeces were considered to be rodenticide victims.

Population changes: There was a significant decrease in small mammal populations at all treated sites, averaging about 60%, as a result of rodenticide poisoning.
All but one reference population increased over the same period. Only the reference population at farm 1 declined, probably because of poor weather during February 2002, but this decline (44%) was less than at the corresponding rat treatment site (79%).

Population recovery: Population estimates made 3 months after each trial indicated longer-term effects of the rat control. At each pheasant-feeder site, small mammal populations had recovered or were at a level that may be expected, suggesting immigration from adjacent populations. At farm 1 no small mammals were found after 3 months. However at the time of year (April–May) when this survey was undertaken, bank vole and field vole populations are naturally normally at their lowest.

Population recovery data indicated that in all four cases, the rate of change was higher in the untreated reference populations than in the corresponding rodenticide treated populations, even when reference populations declined outside the breeding period. Effects of rat control were thus only partly offset by summer breeding, and outside the breeding period the two rat control sites (farm 1 and pheasant feeder 3) declined more than the untreated reference sites.

Conclusions: The results of this study demonstrate that routine rat control using rodenticide on farmland using generally accepted methods reduced local populations of non-target small mammals (wood mouse, house mouse, bank vole and field vole). This may be a significant route of exposure to secondary poisoning of predators and scavengers of small mammals. Rodenticides are applied on farms and game estates across the UK, thus the authors consider that the results of this study are probably indicative of non-target rodenticide exposure nationally.


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