CHAPTER 13
Enemies
PREDATORS, PARASITES AND DISEASES are topical issues in grouse management. British and Irish grouse face these enemies on land that has been greatly modified by humans. While we fashioned moors that benefited red grouse, we deprived our other three grouse species of much natural habitat and altered the set of enemies with which all four must now contend. Some natural enemies have been reduced or exterminated, some have increased, and new ones have been introduced.
PREDATORS OF GROUSE
In Britain and Ireland, the natural balance between predators and prey is distorted. To understand the consequences of this, we revisit principles of predator-prey relationships and compare our situation with more natural ecosystems. Academic students of predator-prey relationships use confusing jargon but the underlying ideas are simple. We also discuss an ethical basis for the killing of predators.
Some principles of predator-prey relationships
Predators and prey evolved together. From the shifting tricks of mutual survival emerge patterns that ecologists call rules. A good rule of thumb from island biogeography is that larger land masses support more species. Ireland now has only one grouse species while Britain has four, fewer than in Europe. Our grouse also have fewer predator species.
Two shibboleths attend academic discussions on predators and prey. First, the impact of a predator species upon the abundance of its prey depends partly upon the ratio of predator to prey. Changes in this ratio, due to the predator’s reproduction, death or movement, are called the predator’s ‘numerical response’. Second, the impact on the prey depends also upon the proportion of that prey in the predator’s diet. Changes in this proportion are termed the predator’s ‘functional response’.
Grouse populations can be cropped by predators, because prey populations can compensate for losses. When some grouse are killed, others live longer or rear bigger broods. If survival or reproduction fully compensates for deaths, the impact of predation upon prey numbers is negligible, and the ratio between predator and prey remains unchanged.1 If deaths are wholly or partially additive,2 the predator-prey ratio can increase, until the predators starve or leave the area (numerical response) or turn to other prey (functional response).
Grouse avoid predators by taking cover. In summer, a cryptically coloured rock ptarmigan hides from gyrfalcons by sidling up to a rock of its own colour and freezing next to it. A willow ptarmigan escapes a goshawk by diving under a bush, into which the hawk, clumsy-footed and fearing for its delicate wings, dares not venture. Red grouse prefer feeding on short heather but usually keep close to tall heather, where they take cover when a raptor approaches. Hill shepherds, especially in western Scotland and Ireland, often burn large tracts of heather every few years to give sheep better food, but incidentally reduce stocks of red grouse by depriving the birds of cover in tall heather. Similarly, wind-thrown trees in plantations provide cover for capercaillie and black grouse, but are commonly removed by tidy-minded foresters.
Another way of avoiding predators is shown by rock ptarmigan in the Cairngorms. They live on large, infertile tracts where prey such as rodents, hares and birds are few, and hence predators, mainly foxes and golden eagles, are scarce. Enriching such infertile ground, however, destroys its value as a refuge from predators, as illustrated by the ski development at Cairn Gorm. Here, tourists’ food scraps attracted carrion crows and gulls, generalist predators alien to this habitat but common on lower ground nearby.3
Grouse also live on richer soils where there are more rodents and other prey that in turn support more predators (numerical response) than in the Cairngorms. In such dangerous conditions, avoidance of predators involves a third consideration. If grouse have good cover and are scarce relative to other prey, they can survive because predators concentrate on the other prey (functional response). Thus, foxes and pine martens depend largely upon small rodents, the main biomass in many grouse habitats.4
Predators such as hen harriers and goshawks often move far in response to variations in prey abundance. The idea that prey move to reduce their risk of being eaten is less well established. Borchtchevski,5 however, proposed that capercaillie densities in the Ilexa River basin in northern Russia were regulated by emigration and immigration, even though predation accounted for almost all their deaths. By moving, he suggested, birds kept their densities low enough to keep residents relatively safe from predation.6
The conclusion that a natural balance between grouse and their predators can depend upon large tracts of uninterrupted habitat has practical consequences. More predators from richer habitats can encroach upon woodland or moors fragmented by developments. Grouse habitat worldwide is increasingly fragmented and enriched by agriculture, by planting and fertilising trees, or by tourist developments, leading to more grassy vegetation, more prey such as rodents or rabbits and, in the case of tourist developments, more food scraps. In Britain and Ireland, all this has led to a perceived need to kill predators.
The distinction between predator and prey is not clear-cut. Grouse chicks eat caterpillars and so grouse are predators of moths and sawflies. Also, smaller predators often fall prey to bigger ones. Ecologists call this ‘intra-guild’ predation. Thus, lynxes eat foxes, and foxes eat pine martens. Golden eagles kill foxes, pine martens, stoats, weasels, buzzards, hen harriers and crows.7 In semi-natural ecosystems that retain their top predators, smaller predators are often scarcer than in disturbed habitats, probably because smaller predators are displaced or eaten by bigger ones.8 Thus increases in goshawks, or declines in their preferred prey, have been associated with local extirpations of kestrels, sparrowhawks and long-eared owls.9
When bigger predators are removed, smaller predators often increase, a process termed ‘meso-predator release’.10 A general observation is that foxes are more abundant where lynxes and wolves have been exterminated. Without wolves and lynxes, foxes often become the dominant mammalian predator. When sarcoptic mange suppressed foxes in Fennoscandia, pine martens increased (see ‘Pine Martens and Capercaillie’, below).11
Iceland – a simple semi-natural predator-prey system
In Iceland, rock ptarmigan form the main prey of gyrfalcons. In the grouse world, this is as close as it gets to a single predator species depending upon a single prey. Gyrfalcon numbers certainly depend upon ptarmigan numbers. Nielsen12 found that the total number of gyrfalcon territories followed ptarmigan density with a three-year time lag. In mathematical models, such lags can lead to unstable, cyclic dynamics. In practice, gyrfalcons ate a greater percentage of the ptarmigan population during the decline and low phases of the ptarmigan population cycle, but the evidence did not establish that falcons caused the decline.
In the Cairngorms, ptarmigan also show ten-year cycles, but there are no gyrfalcons or other predators that specialise in eating ptarmigan. This and other evidence suggests that ptarmigan show unstable population dynamics naturally, and are not dependent upon a predator to drive them.13 Nielsen, however, suggested that the Icelandic fluctuations are a simple predator-prey cycle. We reach two conclusions. First, even simple, well-documented predator-prey relationships are difficult to fathom without experiments. Second, rock ptarmigan in Iceland are often abundant, despite a ferocious predator that specialises in eating them.
The number and variety of predator species that kill rock and willow ptarmigan in the Arctic and on continental areas exceeds that in Iceland. In northern Canada, adults suffer predation by gyrfalcon, peregrine falcon, snowy owl, Arctic fox and red fox, and their chicks and eggs by long-tailed skua, gulls, rough-legged buzzard, raven, short-tailed weasel (stoat) and Arctic ground squirrel.14 Again, this shows that, on large tracts of unfragmented habitat, well-adapted grouse can survive when beset by such enemies, without protection from game preservers. Conversely, introduced Arctic foxes became a severe predator in the Aleutian Islands, even exterminating ptarmigan on some islands.15 On extensive mainland habitats, local depletions are often made good by birds moving in from elsewhere, but on small islands, or on fragments of mainland habitat isolated by agriculture or development, the population may not be rescued by immigration.
The boreal forest – complex predator-prey relationships
In virgin boreal forest in Russia, the biomass of prey available to predators is roughly 150kg per km2, with perhaps 60 per cent of this comprising rodents and 25 per cent grouse.16 Rodent density in different regions varies broadly with the amount of grassy vegetation, and this in turn is dependent upon soil fertility. There is also annual variation because many populations of small rodent show cycles of abundance every three to five years. Grouse rear fewer young in years of rodent scarcity, probably because predators such as pine martens eat fewer rodents and more grouse in such years,17 thereby embodying the functional response.
Predatory mammals in Russian boreal forest include brown bear, wolf, red fox, lynx, glutton (wolverine), badger, European otter, polecat, sable, pine marten, European and American mink, stoat, weasel and the introduced raccoon dog. To have an appreciable impact on grouse numbers, however, a predator must be relatively abundant and must eat grouse regularly. According to studies in the Russian Lapland and Pechora-Illych nature reserves (Table 27), only glutton, fox, pine marten and stoat fall into this category, while in the Ilexa River basin18 only glutton and pine marten qualify. Foxes and stoats are quite rare at Ilexa, where their rodent prey are scarce over the infertile soils.
TABLE 27. Grouse (capercaillie, hazel grouse, willow ptarmigan, black grouse and rock ptarmigan combined) in the diet of mammalian predators in two Russian boreal forest nature reserves, percentage frequency of remains in scats (number of scats in sample is given in parentheses). From Semenov-Tyan-Shanskiy (1960).
TABLE 28. Relative impact of predatory birds on grouse species (capercaillie, black grouse, willow ptarmigan and hazel grouse, plus rock ptarmigan in the Lapland reserve) in three Russian forest nature reserves. The figure on the left is the percentage of all records of grouse being eaten by a given species of bird of prey. The middle figure in parentheses is the average density of each predator (individuals per km2). The figure in bold on the right is an index of the impact on grouse per individual predator, calculated by dividing the left figure by the middle one.
Note
o means that this predator species was present but no grouse were recorded in its diet; + indicates a trace was found in its diet; – indicates the predator species was not in the original tables and so was presumably scarce or absent; and
t indicates a trace impact (close to zero). Other species of raptors, not shown to eat grouse, were present but are not included here. Compiled from tables in Semenov-Tyan-Shanskiy (1960).
There are more species of predatory birds (see Table 28) than mammals in boreal forest. As with mammals, the abundance of each raptor varies from place to place. Of the raptors, goshawk, golden eagle, white-tailed eagle, eagle owl and gyrfalcon take most grouse. Although individual buzzards, and to a lesser extent black kites, eat grouse less frequently, they can be abundant and so kill appreciable numbers of grouse.
In the Lapland reserve, predatory mammals and birds accounted for roughly equal numbers of kills of each of the five grouse species (capercaillie, black grouse, hazel grouse, willow ptarmigan and rock ptarmigan). In the Ilexa study, the main predator of capercaillie was goshawk (75 per cent of recorded kills), followed by golden eagle (9 per cent), pine marten (6 per cent), glutton, eagle owl and white-tailed eagle (each with 3 per cent), and spotted eagle, buzzard and black kite (1 per cent combined).19 The rarity of foxes at Ilexa explains why few capercaillie kills were attributed to mammals.
Britain and Ireland lie in the temperate zone, not the boreal one, and so might be more comparable with the Russian Lake Ilmen, in the zone of mixed forestjust south of the boreal (see Table 28).20 Here, individual eagles and goshawks ate fewer grouse than in the boreal forest, perhaps because of the greater variety of other prey. Overall, however, eagles and goshawks in this temperate reserve were more abundant than in the boreal forest, and so killed similar numbers of grouse.
Britain and Ireland
Bear, wolf, lynx, boar, white-tailed eagle, osprey, goshawk and black kite were exterminated from Britain in historical times, while polecat, pine marten, wildcat, red kite and hen harrier became confined to small enclaves. The intensive predator killing that was widely practised on the new sporting estates of the nineteenth century relaxed somewhat during the late twentieth century. This allowed ospreys to re-establish themselves, especially near fish farms, and goshawks to be restored by escapes from falconers and by unauthorised releases. Hen harriers spread unaided from their Orkney enclave; pine martens and polecats extended their ranges with the help of unsanctioned translocations; red kites from Wales were bred and released with government approval; and white-tailed eagles were re-established by importing youngsters from Norway. Wildcats also spread, but, reduced by recent snaring and swamped by interbreeding with feral domestic cats, there are probably few pure members of the species left in Britain.21
Crows and foxes are the main egg-robbers of British grouse, although crows are scarce in most ptarmigan habitat. Stoats and weasels are widespread egg-robbers, while the depredations of cats, pine martens, gulls and ravens are more local. All the above eat some chicks, as do the smaller raptors, hen harriers
especially taking many red grouse chicks. Hedgehogs occasionally take a few eggs of red grouse, although they do not usually destroy the whole clutch. Badgers and adders are also occasional predators of grouse eggs.
In Britain and Ireland, the main predator of adult grouse is the fox. In a ten-year study in east Scotland, foxes killed 38 per cent of radio-tagged red grouse hens on their nests.22 Although scarce over infertile granite, stoats and weasels are commoner over base-rich soils with patches of nutritious grass, which are favoured by voles and rabbits. These form their main prey, but in summer a few take eggs, chicks and adult grouse. Both predator species have increased along with recent increases in numbers of moorland rabbits, so their killing of moorland grouse can be considered more serious than formerly was the case.
A fox killing an adult grouse usually takes a roosting bird at night, whereas eagles, hawks, harriers and falcons kill in daylight, and avoid hunting in poor light near dawn and dusk. In their usual way of catching adult grouse, eagles and harriers fly low and surprise a bird, pouncing to catch it on the ground or as it takes wing. We see headlong chases by eagles so often, however, that they probably do catch some grouse by this method. Peregrines perch on a lofty crag as they watch for prey, but more often soar high in the sky before stooping upon their quarry.23 Sparrowhawks flit through woodland or across nearby moorland, perching briefly between flights, and catch their prey by surprise. Buzzards prefer to sit on a perch
FIG 158. Golden eagle’s nest on a branch of an old pine in a Caledonian forest. Red grouse and mountain hare are prey, seen alongside an unhatched eagle egg. (Desmond Dugan)
FIG 160. Female hen harrier feeding a red grouse to its three young. The chicks differ in size because they hatch a day or two apart and the biggest get fed first. The largest chick here has taken more than it can easily swallow. (N. Picozzi)
FIG 162. Red grouse killed by a peregrine, which was flushed by the photographer. (Adam Watson)
and wait for prey. Goshawks hunt like sparrowhawks but also use peregrine tactics, watching from exposed perches or soaring and then stooping.
Many predators are killed by game preservers and some by conservationists, although the interests of the two groups differ. Healthy grouse populations rear more offspring than is necessary to replace natural losses, and predators and hunters crop the surplus. However, game preservers want the surplus and regard predators as competitors. On grouse-moors, for example, it is generally reckoned that an autumn minimum of some 65 red grouse per km2 can sustain profitable driven shooting, though some put the figure higher. Predators can depress autumn densities below this threshold and so lose an estate a lucrative asset. Thus, eagles are scarce on many grouse-moors because of persecution by gamekeepers, who have almost eliminated the goshawk on Scottish sporting estates after its earlier increase in the 1970s. Hen harriers, buzzards and other raptors are also routinely killed by some keepers, as are pine martens and badgers.
Conservationists see predators differently. In most studies of the effects of predator killing on birds and mammals, the breeding success of the prey was found to increase with predator killing. In some studies the prey’s breeding density also increased, although in some it did not.24 Conservationists do not crop surplus birds for pleasure or economic benefit, and so see less need than game preservers to maximise the breeding success of gamebirds. They prefer a wider range of species and stress the economic benefits of wildlife tourism. Even so, the Royal Society for the Protection of Birds kills crows and foxes in Abernethy pinewood to benefit capercaillie, and Scottish Natural Heritage kills hedgehogs on North Uist to protect the nests of wading birds.
Can British uplands be managed to satisfy conservationists and game preservers alike? The Langholm experiment set out to measure the impact of raptors upon red grouse, providing facts upon which rational discussion about raptor killing could be based. The experiment entailed killing crows, foxes, stoats and weasels, but abandoning the usual, if illegal, killing of raptors.25
During 1992-6, hen harriers on the 48km2 Langholm moor increased from two to 14 breeding females, and peregrines from three to five or six pairs. Predation, especially of grouse chicks by harriers, apparently suppressed the number of red grouse. Past bag records at Langholm had fluctuated on a six-year cycle, but bags did not peak in 1996 as expected from these records. Bags from two other moors in the same region, which had previously fluctuated together with those at Langholm, did reach high numbers in 1996. Although this evidence did not attain rigorous scientific standards, it provided a reasonable case that raptors, especially harriers, had spoiled Langholm as a good grouse-moor. Autumn density in 1992-6 averaged 66 grouse per km2, barely enough for driven shooting.
Regrettably, Langholm was not a typical grouse-moor and so did not provide the intended basis for rational discussions about raptor killing on grouse-moors in general. Grazing by sheep and outbreaks of heather beetle had led to about half the heather-dominated vegetation becoming grass-dominated between 1948 and 1988. The grassier moorland supported higher densities of small rodents and meadow pipits, which in turn provided abundant food for harriers. Without sheep-induced grassy swards, Langholm might well have been able to sustain better shooting.26
Had the study continued, golden eagles might have returned to Langholm. Golden eagles kill hen harriers and anecdotal observations suggest that harriers tend to avoid eagle hunting grounds.27 Golden eagles, like harriers, kill grouse and are persecuted for that reason. A golden eagle needs some 230g of food a day while a harrier needs about 80g.28 On this basis alone, one pair of eagles is equivalent to about three pairs of harriers. Eagles, however, take much carrion, prefer mountain hares to grouse, and do not usually take small grouse chicks. Hence a pair of eagles might have much the same impact on a grouse-moor as a pair of harriers. At Langholm, by reducing harrier numbers, eagles might have allowed driven shooting to continue unabated.
Is it possible for driven grouse shooting to thrive within the law, with keepers killing foxes, crows, stoats and weasels, but not persecuting eagles, harriers and other protected species? A few successful grouse-moors have been operated largely within the law, and fewer still wholly so. Gamekeepers who tolerate raptors or suggest that raptors might be tolerated, however, have been victimised by some of their less open-minded brethren and find it difficult to speak openly.29
It is likely that raptors suppress grouse stocks below what is possible on a raptor-free moor. But high stocks on a raptor-free moor might lead to an increased incidence of parasitic disease, a threat that keepers sometimes try to counter by treating grouse with anthelmintic (worming) drugs coated on grit eaten by grouse. Medicated grit, however, cannot always prevent outbreaks of grouse disease. If excessive grouse densities lead to disease, irrespective of medication, the killing of raptors might lead to greater fluctuations and lower average bags. It is often suggested that, by killing the most heavily parasitised grouse, raptors keep disease at bay without the use of drugs. Furthermore, if owners of grouse-moors continue to instruct keepers to kill raptors or prevent their successful breeding, they may find that society will eventually ban their sport outright.
In British and Irish conditions, some predator control is a necessary part of conservation. Discussion would be cooler if predator control had an agreed ethical basis. Few people have ethical objections to killing pests such as rats, although many would rather leave it to somebody else. Most conservationists accept that foxes, crows, stoats and weasels can be pests. So, too, is the American mink, an introduced creature that has been blamed for the near extermination of water voles throughout most of lowland Britain. Game preservers additionally regard raptors and martens as pests, whereas conservationists regard them as a part of our natural heritage that should be there for all to enjoy. A reasonable start to any discussion would be that foxes and crows, for example, are much more abundant in Britain and Ireland than in more natural landscapes. An ethical case for culling a predator, therefore, would be made if it could be shown that the predator is unnaturally abundant and is suppressing desired creatures to unacceptably low levels.
PINE MARTENS AND CAPERCAILLIE
Pine martens are woodland predators that eat mainly small mammals, but they also feed on the eggs, chicks and adults of birds, including woodland grouse. Some argue that martens contributed to the decline of, and threaten the future of, the endangered capercaillie in Scotland, and that their killing should be made legal. But what is the evidence for this?
FIG 163. Young pine marten with finch prey. (Stuart Rae)
During the heyday of predator killing in Britain, pine martens were reduced to a few small enclaves, the main one in the west of Scotland. During the last few decades of the twentieth century, with help from translocations, the animals regained much of their former range in the Highlands and northeast Scotland. The spread of the pine marten and decline of the capercaillie occurred at roughly the same time.
In much of their range, however, capercaillie were already in steep decline before pine martens arrived in any number. Capercaillie in the woods of Kinveachy estate in Speyside, for example, began to decline in 1979-80,30 yet pine martens were not noted there until 1986.31 Similarly, in mid-Deeside pine martens were not seen regularly until the 1990s,32 by which time the capercaillie decline was well underway.
A survey compared the breeding success of capercaillie with the abundance of various predators, including pine martens, in 14 Scottish woods in the mid-1990s.33 Capercaillie reared fewer chicks where crows, foxes and raptors (mostly buzzards and sparrowhawks) were more abundant. An index of marten abundance, however, was not related to breeding success of capercaillie. Also, the average nationwide capercaillie breeding success in 2001-3 exceeded that in the late 1990s, and capercaillie numbers increased between nationwide population estimates in the winters of 1998/9 and 2003/4. Hence capercaillie and pine martens seem able to coexist in Scotland, as they do in the rest of their joint range.34 But keepers kill pine martens, albeit illegally, and some argue that capercaillie would have declined further had pine martens been left unchecked.
During the large absence of pine martens for much of the twentieth century, few studies of them were carried out in Scotland, and then mostly in the west, where there are now no capercaillie. Therefore we look abroad for better information on the relationship between numbers of pine marten and capercaillie.
The staple food of pine martens and many other woodland predators is typically small rodents.35 More of the alternative foods such as berries, nuts, seeds, insects, worms, frogs, hares, squirrels, carrion and birds, including capercaillie and other grouse species, are taken when rodents are scarce. Thus, during the periodic lows of a typical three- to four-year vole cycle, martens take more of the alternative foods and woodland grouse rear fewer young.36 Studied in the Pechora-Illych reserve in Russia (Fig. 164), scats of pine martens showed that they usually ate more grouse when small rodents were scarce; but in one year with few rodents, grouse were spared because martens ate many berries and pine nuts.
On the poor soils of the Ilexa River basin near Archangel in Russia, rodents are scarce and predators rely heavily on woodland grouse. Pine martens are the most abundant mammalian predator of grouse, killing 0.1-1.3 per cent of the population of capercaillie.37 This is a very small fraction, but does not include
FIG 164. Grouse remains (per cent occurrence) in winter scats of pine marten in relation to an index of vole abundance in the Pechora-Illych nature reserve in 1949-58 (from Fig. 75 in Semenov-Tyan-Shanskiy, 1960). There was a clear inverse relationship except in 1958 (open symbol), the sole year when berries and pine nuts formed the biggest single category in the martens’ diet. Other categories were: invertebrates, frogs, birds’ eggs, grouse, other birds, small rodents and other mammals.
their depredation of eggs and chicks, so leaving open the question of how great an impact they have upon the capercaillie population.
Capercaillie have long been hunted and pine martens killed for fur in Europe. Records from three large estates in southern Bohemia during 1750-1890 provide a useful example from less industrial times.38 Here, there was no association between the numbers of pine martens killed for fur and the numbers of capercaillie shot for sport.39
In Finland, as one travels from north to south, fairly continuous forest gives way to an increasingly agricultural and fertile land, where forest is more fragmented. This change in landscape is associated with decreasing breeding success of capercaillie and black grouse, increasing abundance of red foxes and pine martens, and decreasing abundance of stoats.40 Many have concluded that foxes and martens cause the poorer breeding success of woodland grouse in south Fennoscandia. Supporting this view, experimental killing of foxes and martens on a Swedish island increased the breeding success of grouse.41
The island experiment, however, did not distinguish the separate impacts of fox and marten. Nor did it explain the role of stoats, which are more abundant in north Finland, where grouse breed better. Perhaps conditions in north Finland favour both grouse and stoats.
We use data from the Finnish study to check whether year-to-year variations in grouse breeding success were related to the abundance of pine martens. In the south of Finland there was no significant association. In the north, the raw data (Fig. 165) also suggested no association, but after one allows for annual variations in vole and marten abundance, breeding success was better in years with few foxes. It was also better in years with more voles, which fits the idea that predators kill fewer grouse when there are more voles to eat. However, after allowing for annual variations in vole and fox abundance, it appeared that grouse breeding success was better in years with more pine martens, the opposite of what one might expect.
That woodland grouse rear more young when there are more pine martens may seem surprising. Other evidence reveals a likely mechanism. An outbreak of sarcoptic mange among red foxes in Norway, Finland and Sweden reduced fox numbers, whereupon pine martens increased, probably because foxes kill martens or compete with them for food.42 Small game, including capercaillie, black grouse, willow ptarmigan and mountain hares, also increased. This suggests not only that foxes depressed martens and grouse, but also that martens have less impact than foxes upon grouse abundance.43
A scarcity of foxes benefits both pine martens and capercaillie. Moreover, pine martens are less likely to eat capercaillie when small rodents are abundant. Hence capercaillie and pine martens should be able to coexist where there are few foxes and also many small rodents and other foods. Also, the taking of capercaillie eggs and small chicks by foxes and pine martens is probably opportunistic,44 and so good ground cover, especially for nests and broods, could allow coexistence between woodland grouse and pine martens.
PARASITIC WORMS
Grouse intestines are home to several species of tapeworms, roundworms and threadworms. Large tapeworms Paroniella urogalli45 are flat, segmented worms, well known to anyone who flushes red grouse in late summer. As young grouse take flight, lengths of creamy-white worm spurt from their backsides to dangle grotesquely before breaking off in egg-laden segments. The large roundworm Ascaridia compar is often found in the small intestines of Old World grouse, but is
FIG 165. Capercaillie breeding success (proportion of hens with broods) in relation to marten abundance (index from tracks in snow) in part of northern Finland in 1989-94. Top: raw data. Bottom: the relationship between breeding success and marten abundance, after allowing for the effects of vole and fox abundance (this is a ‘partial residual’ plot).
rarely reported in grouse in Britain.46 Caecal threadworms, intestinal threadworms Capillaria spp. and the diminutive tapeworm Hymenolepis microps are barely visible to the naked eye.47
In Britain, the main research has been on the caecal threadworm Trichostronaylus tenuis, agent of ‘grouse disease’ in red grouse. Otherwise, the occurrence and effects of parasitic worms in British grouse have been little studied. The tapeworms Paroniella urogalli and Hymenolepis microps are common in red grouse, and are widespread in ptarmigan and capercaillie in other European countries, and hence presumably in Britain.48 The roundworm Ascaridia compar, however, seems to be found mostly in more continental climates, which may explain why it is seldom seen in Britain.
The caecal threadworm Trichostronaylus tenuis, conversely, seems to be confined to mild climates. It occurs in small numbers in the willow and rock ptarmigan of coastal Scandinavia, but not in more continental parts.49 The temperate conditions of moorland Britain seem to favour this parasite. Ubiquitous in red grouse, it also occurs in Scottish ptarmigan, but heavy burdens are unusual in ptarmigan and have been reported mostly at low altitudes. It has not been reported in black grouse or capercaillie, probably because it cannot establish itself in these species.50
Red grouse on many moors are routinely treated with anthelmintic drugs. These can be administered by catching birds and dosing them directly through the mouth, but the easiest method is to lay out medicated grit, which birds can pick up in their own time. Such treatments are aimed primarily at Trichostronaylus tenuis but must also affect other parasites. Direct dosing can increase the breeding success of red grouse, and in a five-year study on a grouse-moor in county Durham,51 where average burdens of T. tenuis were in the thousands, medicated grit reduced burdens and increased the average number of chicks reared from 3.5 per hen to 5.6.52
Tapeworms
The tiny tapeworm Hymenolepis microps occurs in the duodenum of grouse and is widely distributed in Britain and Europe, although none was found in a sample of 1,065 red grouse from the Scottish Highlands.53 During a study of willow ptarmigan on the Norwegian island of Karlsøy, the percentage of chicks infected with H. microps jumped from less than 10 per cent to almost 50 per cent between August and September, while the percentage of infected adults was falling.54 This might have been because the most infected young chicks were being killed by worms, but we know of no direct evidence that H. microps affects breeding success in grouse.
In boreal Russia, tapeworms were not found in capercaillie and willow ptarmigan from November to January, but were present in most birds during summer.55 In Scotland, the large tapeworm Parionella urogalli occurred in over 70 per cent of red grouse in summer and winter. More worms were gravid (full of eggs) in summer, however, when they were three to four times their winter weight.56
The large Parionella urogalli seems to be less pathogenic than Hymenolepis microps, even though the swollen gut of a bird heavily infected with P. urogalli bulges with worms. In Scotland, tapeworm burden was not related to the host bird’s condition. In Canada, very high burdens of Parionella species did not appear to affect the growth of ruffed grouse.57 In Canada again, the condition (protein and fat reserves) of willow ptarmigan did not differ between birds parasitised with Parionella species and those not parasitised.58
Caecal threadworms
Outbreaks of ‘grouse disease’ in red grouse seem more frequent in the milder conditions of north England than in north Scotland, although this may be related also to higher densities of grouse on English moors. Cobbold59 first associated heavy burdens of caecal threadworms with disease, and Leiper60 investigated the simple life history of the worm (see Fig. 166). The Committee of Inquiry on Grouse Disease61 subsequently identified the worm in over 2,000 birds dissected during outbreaks of disease, so providing a firm basis for grouse disease being trichostrongylosis.
Adult worms reside in the birds’ caeca and are remarkably long-lived, such that most die only when their host dies.62 Eggs laid by female worms are voided in the semi-liquid caecal droppings of grouse. After a few days, or longer in colder conditions, first-stage larvae hatch and begin feeding on micro-organisms in the droppings. They grow and moult, losing their outer cuticle like a snake shedding its skin, into second-stage larvae. These develop further into third-stage larvae, which do not feed but migrate out of the caecal droppings, retaining their second-stage cuticle as protection against desiccation. These infective third-stage larvae are ready to enter a host, and move onto heather tips in the hope of being ingested by a feeding grouse.
The odds against success for a third-stage larva are enormous. An adult female worm produces about 100,000 eggs a year. Of these, on average less than ten must establish themselves in another grouse to maintain the worm population. So, when conditions for transmission are favourable, there is ample scope for rapid increases in worm burdens and consequent outbreaks of grouse disease. If the proportion of eggs that become established as adult worms (the transmission rate) is fairly constant, parasite burdens will be largely determined by the density of hosts and the worms in them. Conversely, transmission rates
might be determined by environmental conditions that vary widely, causing worm burdens to fluctuate independently of host density. In reality, both density and environment affect worm burdens,63 so that high grouse density and wet summer weather are each conducive to increased burdens.64
Following the Committee of Inquiry on Grouse Disease, the next scientific study to document grouse disease was at Glen Esk in 1957-61.65 Emaciated hens with large worm burdens were found lying dead on their nests in 1958 and 1959, and the breeding population declined between 1958 and 1960. Despite this, surviving birds reared enough young to ensure that in autumn all the ground was occupied by territorial birds and that some were denied territories. Hence the decline was associated with pathological worm burdens, but the declining population was limited by territorial behaviour.
At the time of the Glen Esk study, interpretation was hindered by two complications. First, birds shot in autumn with large worm burdens, similar to those found in emaciated and moribund birds in spring and summer, were in good condition. Only later did it transpire that adult worms are relatively benign.66 The main damage is done by developing larvae as they burrow into the birds’ caecal walls during their two-week development period.
A few developing larvae do little damage to their host’s caeca, but there is a twist. During autumn, many ingested larvae do not develop, but remain buried in the caecal walls in a state of arrested development or hibernation. A stock of arrested larvae builds up in the caeca. In spring, these develop simultaneously and, if they number in the hundreds or thousands, cause massive damage. This explains why outbreaks of grouse disease usually begin in spring, although diseased birds, emaciated and unable to fly, can be seen throughout summer. It also explains why the same burden of adult worms can appear innocuous in autumn but fatal in spring.
Caecal threadworms are long-lived and so a grouse accumulates an increasing burden of worms during its lifetime. Hence old birds often have many more worms than young ones. But, because arrested larvae that are developing in spring do most of the damage, old suffer no more than young during outbreaks of grouse disease.67
A second complication during the Glen Esk study was severe ‘browning’ of the birds’ heather food in the springs of 1958 and 1959. In frosty dry conditions, green heather foliage can become so desiccated that it turns brown and dies, reducing the amount and quality of the birds’ food. Because worm larvae tend to concentrate on the remaining edible green shoots (see Fig. 167), heather browning probably accentuates trichostrongylosis.
With hindsight, we can disentangle the complexities of the Glen Esk study. Removing parasites with anthelmintic drugs can moderate cyclic declines in the numbers of red grouse, but it does not prevent the declines (see ‘Parasites and population cycles’, below). This fits the idea that, by increasing mortality and reducing breeding success, worms and heather damage together modified the Glen Esk birds’ social structure (see Chapter 14). This may have caused cocks to take larger territories, with the result that numbers declined more than they would have done without parasites. Hence worms, heather browning and
FIG 167. Caecal threadworm larvae (Trichostrongylus tenuis) on living (green) and dead (brown, frosted) heather plants. Out of 3,000 larvae put on the ground, similar numbers moved onto each type of plant, but about three times as many ended up on the shoot tips of green plants as on those of brown plants. (Note: the bars represent standard errors uncorrected for differences between the nine paired replicates.)68
territorial behaviour all probably played a role in the Glen Esk decline. More generally, cyclic declines associated with changes in the birds’ social behaviour certainly occur without heather browning or trichostrongylosis. Conversely, the severest outbreaks of disease on overstocked grouse-moors probably kill so many birds that limitation of numbers by social behaviour may be temporarily suspended.
Parasites and population cycles
If grouse disease causes population cycles, as claimed for over a century,69 removal of parasites with anthelmintic drugs should stop the cycles. An experiment in north England aimed to test this prediction. The authors claimed that ‘Treatment of the grouse population prevented population crashes, demonstrating that parasites were the cause of the cyclic fluctuations’.70 Their own data (Fig. 168) show that this claim was overstated.75 Although anthelmintics can improve breeding success and survival, population cycles continued despite the treatment. Better work in Scotland and England confirms this conclusion.76 Grouse disease
FIG 168. Parasite removal experiment.71 Bags (birds shot in autumn on six different moors) as originally presented (top left). When plotted on a logarithmic scale as in the original, bags show apparent differences between treated and untreated (control) populations (red lines indicate grouse treated with anthelmintic drugs in spring 1989 only; blue lines indicate grouse treated in 1989 and 1993). Note that differences among moors depended mostly on years without shooting, when of course there was no bag (and hence no sample). When bags were plotted on a linear scale (top right), differences were less apparent and it was clear that bags on all areas had continued to show cycles, irrespective of the treatment. Normalising72 the data (bottom left) removed differences in amplitudes among moors, and showed a similar cyclic pattern on all moors. To remove bias due to inclusion of years with no shooting as zeros, we estimated what the bags would have been if shooting had taken place in such years.73 The result (bottom right) is on the same scale as the first plot (top left), and comparing the two reveals distortions in the first plot due to inclusion of years with no bag as zeros. Indeed (bottom right), bags from some of the treated populations declined more than those from controls.74
certainly causes population crashes on overstocked moors, especially after wet summer weather enhances parasite transmission, but population cycles occur even when parasites are removed.
Parasites and behaviour
In red grouse, parasites interact with bird quality and condition to influence a bird’s aggressive behaviour, and this in turn influences the birds’ density. The subtle interactions now being unravelled can be understood by assuming that each bird has physiological resources that it can invest in various ways.77 To resist parasites, for example, a bird invests in its immune system. To gain a territory and attract a hen, a cock invests in its own aggressiveness via testosterone production. More testosterone imparts less immunity against parasites, and vice versa. By sacrificing its condition, a cock can invest more into immunity and testosterone, but then has fewer reserves against hard times. A better-quality cock, however, can invest more into immunity and testosterone while remaining in good condition.
This brings us to the ‘immunocompetence handicap principle’. To rear more young, a cock needs a better-quality hen. He attracts her by being more aggressive, getting a bigger territory, and signalling his quality by displaying bigger combs. These require more testosterone, a costly investment. Overcoming this handicap proves him a better-quality cock, which can provide his hen with a bigger territory and with offspring that are better able to resist parasites.78
LOUPING ILL
The disease
Louping ill, a disease of the central nervous system, can wreak havoc on red grouse. Caused by a virus transmitted by the sheep tick Ixodes ricinus, it is primarily a disease of sheep, but it also affects wildlife and humans.79 Mortality in sheep is typically about 10 per cent. Many animals develop a characteristic ‘louping’ gait, in which the front legs move forward together, followed by the back legs.80
The louping-ill virus is the most westerly member of the tick-borne encephalitis group of viruses. After a one- to two-week incubation period, humans infected with tick-borne encephalitis get a fever that abates within a few days. Several days later, a second fever develops, often associated with confusion, reduced consciousness, fits or limb weakness. In humans, louping ill is the mildest form of tick-borne encephalitis, and is seldom fatal.81 However, in red grouse about 80 per cent of birds experimentally infected with the virus died of it.82
The virus
Louping-ill virus was probably brought into the Irish and British uplands by sheep. Molecular analysis shows at least three genetically distinct types, namely Irish, Welsh and British.83 The virus seems to have first appeared less than 800 years ago in Ireland, whence a descendant spread into Wales and subsequently to the Scottish Borders. From there it dispersed throughout Scotland, northern England and Norway. The main spread apparently coincided with livestock movements over the last 300 years.
The tick
Sheep ticks have four stages in their life history. An adult female tick lays about 2,000 eggs in the mat of moist, decomposing plant litter that forms the upper layer of many woodland and moorland soils. This protects ticks from winter frost and in summer provides moisture for their rehydration. Having overwintered in the mat, eggs hatch in spring. Newly hatched larvae are tiny (the size of a pinhead), six-legged, translucent and hard to see. Hungry, they climb the vegetation and await a host. This can be a bird or a mammal ranging in size from a small rodent to a red deer.
Successful larvae engorge themselves on blood and then drop off, burrowing again into the mat to develop into nymphs. Nymphs are much bigger than larvae (1.5-2mm long) and have eight legs. They climb again and wait for another host. On grouse, larvae and nymphs are usually found on the head, where the birds find it difficult to remove them by preening. They use their feet in clumsy efforts
FIG 169. Sheep ticks on English setter. (Desmond Dugan)
to scratch ticks from their heads but also scrape off tender, newly growing feathers. Bald patches of pink, featherless skin show that a bird has suffered many ticks.
Distended nymphs drop again to the mat, where they develop into adults before once more climbing in quest of a host, the main ones being sheep, deer and mountain hares. Adults are the only stage in the life cycle when the sexes can be distinguished. Questing females are 3-4mm long but, once bloated, can reach 10mm. After feeding and mating with the much smaller males, they again drop to the litter where they lay their eggs. The tick life cycle can be completed in 18 months, but may take several years.
Epidemiology
Louping ill can spread in at least three ways. First, a tick that feeds on a host with high concentrations of virus in its blood can transmit the disease to its next host. This occurs mostly through sheep.84 Second, the virus can pass from infected to uninfected ticks that are feeding close to each other on mountain hares,85 but apparently not on deer or rabbits. Third, it can be spread directly from one host individual to another by droplet infection, without the intervention of a tick.86 Droplet infection could well occur among grouse chicks being brooded by their mother, but this has not been studied. Rabbits and small rodents are thought not to play an important role in the persistence of louping ill.87
On hills where hares and deer are scarce, the removal or routine vaccination of sheep can eliminate louping ill from grouse stocks. This has worked in parts of northern England. But in some regions of Scotland, louping ill has remained prevalent despite the vaccination of replacement ewes for over 30 years.88 Apparently, hares or deer are sufficient to sustain the disease and so depress grouse stocks.
Captive black grouse, capercaillie and pheasants that were experimentally infected with louping-ill virus all recovered, though some looked unwell for a few days.89 About 20 per cent of infected red grouse recovered, but Scottish rock ptarmigan and willow ptarmigan from Norway all died with high levels of virus in their blood. These dissimilar responses to infection probably reflect each bird race’s differing exposure to tick-borne encephalitis viruses during its evolution. The viruses and the ticks that transmit them occur naturally in woodland throughout the Palaearctic. Woodland birds have probably developed resistance from long association with tick-borne encephalitis viruses. But races of open ground, above or to the north of the timberline, have had less contact with the viruses and less opportunity to develop resistance.
The disastrous effects of louping ill upon red grouse follow two historical accidents. First, forest clearance allowed red grouse to occupy large tracts of artificially sustained heather moorland where the climate is mild enough for ticks to thrive. Second, sheep brought the disease onto moorland. Some healthy wild red grouse have antibody to the virus, suggesting that the bird has developed some immunity, and, with continued exposure, its resistance is likely to increase.90
Management
If hares or deer can sustain louping ill on grouse-moors, it seems rational to try the effect of removing them. Experimental reduction of hares on one moor in Speyside was followed by much reduced tick burdens on chicks of red grouse, but this had no effect upon the number of grouse available for shooting.91 In a separate trial on another Speyside moor where louping ill was a known problem, however, increased grouse bags followed mass killing of mountain hares and deer.92
Since the early 1990s, the disease seems to have been affecting red grouse in some areas where it was not previously recognised. This could be due partly to milder winters allowing better tick survival, and partly to increased numbers of hosts, notably red deer. Mass killing of mountain hares with the aim of protecting grouse from louping ill is becoming widespread. The Speyside trials may have been straws in a gathering wind that is already seeing mountain hares being greatly reduced on many Scottish moors.
Until the 1970s, red deer were regarded as vermin on many grouse-moors and shot on sight. This policy was relaxed as estates attempted to increase income by having deer stalking and grouse shooting on the same ground. This might have been counterproductive if it allowed grouse to become infected with louping ill. Managers who greatly reduce mountain hares to protect their grouse stocks might consider reverting to the traditional practice of treating red deer as vermin.
DISEASE AND CLIMATE CHANGE
Grouse evolved during a period of global cooling and so climate warming is unlikely to favour them (see Chapter 1). Milder and wetter weather might promote the transmission of caecal threadworms and louping-ill virus. Conversely, warmer and drier conditions might reduce transmission rates by lowering humidity and thus making worm larvae and ticks more prone to desiccation. At the moment, anecdotal evidence is that ticks are now found on dogs in every month of the year, quite unlike a few decades ago, and louping ill appears to be spreading amongst red grouse.
Further spread of ticks and louping ill to Alpine ground could be disastrous for the ill-prepared rock ptarmigan, which has no natural immunity to the virus. This seems less likely in the Cairngorms, where there are very low densities of mammalian hosts, but more likely on relatively fertile soils such as on the Cairnwell hills, where mountain hares, voles and red deer are abundant. Excessive numbers of red deer are a likely agent for spreading ticks and louping ill to previously unaffected moors and Alpine land (see Chapter 15).
SUMMARY
Humans have altered habitats and extirpated large predators in Britain and Ireland, thereby allowing medium-sized predators such as foxes and crows to become unnaturally abundant. The killing of such predators for the benefit of ground-nesting birds therefore has a rational and ethical basis. Some current practices, however, are controversial or illegal.
Pine martens kill capercaillie and are often said to threaten the bird’s future in Scotland. The evidence, however, is that the two species should be able to coexist in Scotland as in other countries.
The most damaging parasite of red grouse is the caecal threadworm Trichostrongylus tenuis. High grouse density and wet summer weather are each conducive to grouse disease, which is caused by this parasite, but threadworms are often blamed for declines that actually result from the birds’ own behaviour. Disease certainly causes population crashes on overstocked moors, especially after wet summer weather enhances parasite transmission, but population cycles continue even when parasites are removed.
The virus disease louping ill, transmitted by sheep ticks, is fatal to red grouse. Since the early 1990s, the disease seems to have been affecting red grouse in some areas where it was not previously recognised. This could be due partly to milder winters allowing better tick survival, and partly to increased numbers of hosts, notably red deer.
Climate change involving milder and wetter weather might increase both grouse disease and louping ill.