Ecology 2002 39, Cotrol of parasite burdes i wild red grouse Lagopus Blackwell Sciece, Ltd lagopus scoticus through the idirect applicatio of athelmitics D. NEWBORN ad R. FOSTER The Game Coservacy Trust Uplad Research Group, Swale Farm, Satro, Guerside, Richmod, North Yorkshire DL11 6JW, UK Summary 1. Red grouse Lagopus lagopus scoticus populatios i Britai exhibit cyclic fluctuatios i abudace with periodic populatio crashes. Substatial evidece exists to suppose that parasitic worms are the major factor causig these populatio crashes. 2. This experimetal study was udertake betwee 1996 ad 2000 o two areas of moorlad i the orth Peies, UK, to evaluate the efficacy of the idirect applicatio of athelmitic drugs i the cotrol of the caecal ematode Trichostrogylus teuis. 3. O oe area, grouse were give access to athelmitic drugs icorporated ito grit (medicated grit) to cotrol T. teuis umbers, while o the secod cotrol area the birds had access to grit without athelmitic drugs icorporated (plai grit). I the witer of 1998 99 the treatmet was reversed betwee the two areas. 4. Adult grouse from the experimetally treated area had sigificatly lower ifectios of T. teuis tha grouse from the cotrol area. He grouse, which had access to athelmitic drugs, did ot produce sigificatly more eggs or have a greater hatchig success tha hes with access oly to plai grit. Chick survival was sigificatly greater o the medicated grit areas, with a sigificat differece i breedig success. Hes that had access to athelmitic drugs reared more tha twice as may chicks as cotrol hes. 5. No sigificat differece was foud i red grouse survival betwee grit treatmets. 6. The icrease i grouse umbers arisig from the use of medicated grit ehaces the viability of red grouse shootig because the cost of treatmet appears to be low relative to the retur from a icreased harvest. Key-words: athelmitic treatmet, breedig success, medicated grit, Trichostrogylus teuis. Ecology (2002) 39, Ecological Society Itroductio The cause of the regular crashes i red grouse Lagopus lagopus scoticus (Short 1967) umbers has fasciated ad frustrated biologists ad sportsme alike for may years. The caecal threadworm parasite Trichostrogylus teuis (Eberth.) causes high levels of mortality i red grouse ad may cotribute to this cyclic patter (Lovat 1911). The debate o the role of parasites i the populatio cycles of red grouse has cotiued for more tha 100 years (MacDoald 1883; Lack 1954; Chitty 1967). However, the biology of the parasite ad its relatioship with its Correspodece: D. Newbor, The Game Coservacy Trust Uplad Research Group, Swale Farm, Satro, Guerside, Richmod, North Yorkshire DL11 6JW, UK (fax +44 1748 886594; e-mail dewbor@gct.org.uk). host has oly bee studied i detail relatively recetly (Jekis, Watso & Miller 1963; Potts, Tapper & Hudso 1984; Hudso, Dobso & Newbor 1985; Hudso 1986a; Shaw, Moss & Pike 1989; Hudso, Dobso & Newbor 1992). Of particular sigificace is the importat role that parasites have i reducig the breedig potetial of red grouse, a actio that has a highly destabilizig effect o grouse populatio dyamics (Hudso 1986a; Dobso & Hudso 1992; Hudso, Dobso & Newbor 1992). Recet largescale experimets have established that a reductio i T. teuis ifectio dampes populatio cycles, idicatig that parasites are a major cause of populatio cycles (Hudso, Dobso & Newbor 1998). Approximately 3 8 millio ha of heather Callua vulgaris-domiated moorlad are maaged for sport shootig of red grouse i Britai (Hudso 1995). The
910 D. Newbor & R. Foster primary objective of red grouse maagemet is to provide a sustaiable harvest of grouse to shoot. This is doe by employig gamekeepers to provide optimal habitat by burig small patches of heather i a rotatio to give a mix of ages ad heights, with both youg shoots for food ad older stads as cover. Gamekeepers also cotrol predators, pricipally red fox Vulpes vulpes, crows Corvus spp. ad some mustelid species (Hudso & Newbor 1995). The majority of grouse shootig is leased, providig both icome ad employmet of great value to the uplad ecoomy (Hudso 1992). To reduce the severity of populatio crashes, grouse maagers attempt to cotrol grouse parasites. Grouse aturally eat available quartz grit to aid the physical breakdow ad hece digestio of heather, the pricipal compoet of their diet. Red grouse pass out grit ad replace it o a daily basis (Hudso 1992). This demad for grit ca be used as a route to admiister a athelmitic drug to the grouse. I this study, mied pieces of quartz grit, 2 4 mm i diameter, were covered with a thi layer of kerel fat impregated with Febedazole hydrochloride (sold uder the trade ame of Paacur; Hoechst Aimal Health, Milto Keyes, UK) at a cocetratio that would apply a low but steady dose of athelmitic (Hudso 1992). This medicated grit has four major advatages. 1. It is a safe drug, with sheep give 1000 times the recommeded dose rate i trials displayig o adverse symptoms. 2. Febedazole is a broad-spectrum athelmitic reported to be effective agaist eggs, adults ad immature larval stages of several species of trichostrogyle worms. 3. Febedazole is a stable product that does ot break dow i light ad is ot soluble i water. 4. Low cocetratios have a impact o gut parasites ad are particularly effective whe applied as a split dose. Eve small doses will cause some damage to gastroitestial worms (Hudso 1992). This last poit is of particular sigificace because mior reductios i the fecudity of the parasitic worm will reduce both trasmissio rate ad the rapid build up of parasites characteristic of populatio crashes (Hudso & Dobso 1989). Iitial trials with paired moorlad sites, i which oe site received medicated grit ad the secod received plai grit, showed that medicated grit was associated with a 44% reductio i worm burdes (Hudso 1992). However, the effects o grouse breedig success were ot cosidered. This study was udertake to ivestigate the impact of medicated grit o the breedig desities, breedig success ad survival of red grouse ad its impact o T. teuis umbers i the followig autum. Methods The study was coducted o moorlad at two sites o the Strathmore Estate i the orth Peies, couty Durham, UK. Both sites were predomiately south facig at a altitude of 400 580 m a.s.l. The sites comprised heather-domiated vegetatio, chiefly o blaket bog, but with some stads of freely draiig heather, mixed with bilberry Vacciium myrtillus o the steeper slopes. The uderlyig rock was predomiatly millstoe grit with outcrops of limestoe. Medicated grit has bee applied to the moor aually sice the late 1980s, i regularly distributed heaps o a lattice patter each of about 1 kg of grit approximately every 200 m. Hece grouse were used to takig artificially preseted grit. Two areas, each approximately 400 ha, were selected for the trial ad were maaged by the same gamekeeper. Each of the areas had either medicated grit or plai grit applied at the same rates ad heap frequecy i November or December ad repleished i late witer each year. Withi each block, a area of 100 ha was selected towards the cetre ad marked at the corers with posts for dog couts. The two 400-ha areas were less the 1 km apart; the two dog cout areas were approximately 2 km apart. The area receivig the medicated grit was switched betwee the areas after 3 years. This resulted i oe area receivig medicated grit for 3 years while the secod area received it for 2 years, to help cotrol for ay site effect withi the data. To cosider potetial differeces i clutch size ad hatchig success betwee grit treatmets, a sample of 10 female red grouse was captured i February each year ad equipped with a 15-g radio-trasmitter. Birds were caught at ight by lampig i the cetre of each 400-ha study area (Hudso & Newbor 1995). Each he was give 2 ml of a oral athelmitic, Levamisole hydrochloride (sold uder the trade ame Nilverm, Scherig Plough Aimal Health, Welwy Garde City, UK), to flush all or most worms from the caeca (Hudso 1986a), so that worm burdes were similar betwee birds both withi ad betwee study areas irrespective of grit applicatio. A estimate of the bird s coditio was made from a subjective score (1 5) of the quatity of pectoral muscle. A coditio score of 1 was ascribed to a bird i a very emaciated coditio, with very little pectoral muscle ad sterum very obvious. Coversely a coditio score of 5 was ascribed to birds i a very fat rouded coditio with pectoral muscle promiet above the sterum. Further assessmets of body coditio were ot made, so ay possible improvemet i bird coditio through access to medicated grit could ot be assessed. Parasite burdes i radio-tagged grouse were cosidered at the level of the bird i relatio to site, year, treatmet ad the date that each bird was shot. Tagged grouse were subsequetly located o average every 10 days to verify that the grouse stayed withi the allotted 400-ha treatmet areas. No birds were located outside of their allotted treatmet areas durig the study. Nests were located durig early icubatio i late April, but hes were ot flushed to establish clutch size util they were estimated to be at least half way through their icubatio period i late/mid-may Each est was
911 Cotrol of parasites i grouse marked by placig a bamboo cae 10 m away o a predetermied radom compass bearig, to allow relocatio. A idex of hatchig success was obtaied by coutig the umber of remaiig uhatched eggs ad relatig this to the clutch size. Each radio-collared he was located i the first week of July ad the umber of chicks accompayig her were couted with the aid of traied poitig dogs. This provided a estimate of overall breedig success. A sample 100-ha area towards the middle of each 400-ha study area was selected to miimize ay possible iterferece from the cotrastig grit treatmet. Withi this area, red grouse were couted, usig poitig dogs, every sprig ad agai i July, to obtai estimates of sprig desities ad breedig success (Hudso & Newbor 1995). Care was take to exclude all radio-collared hes from this estimate. I this way grouse that had bee treated orally to reduce worm burdes were excluded. Idices of grouse survival were calculated by two methods. First, from differeces betwee successive couts usig poiter dogs. Breedig survival was estimated from the differece betwee sprig ad proceedig couts i July of the same year, ad over-witer survival from the differece betwee the total cout of adults plus youg i July i year t ad the followig sprig cout i year t + 1. Secodly, survival was estimated betwee February ad August from the radio-tagged birds. Each year durig the shootig seaso itesties were collected from samples of grouse shot off each 400-ha area, ad the itesity of worm ifectio was determied for each bird (Hudso & Newbor 1995). I each case the itesity of worm ifectio was determied by removig oe of the pair of caeca from the birds ad extractig the worms. Worm itesities betwee the two caeca withi the same bird do ot differ sigificatly (Lovat 1911; H. Watso, upublished data). The cotets of the caeca were washed over a 210-µm sieve ad the material collected i this way was diluted with 300 ml of water, mixed ad subsampled ito 3 10 ml; the total umber of worms per caeca is the estimated from these couts. (Wilso & Wilso 1978; Hudso 1986a). Mea values for each of the depedet variables, clutch size, chicks he 1, grouse km 2, grouse survival ad parasite burde, were calculated for each site i each year. Differeces betwee mea values of each variable i relatio to grit treatmet were cosidered by three-way ANOVA models with grit treatmet, year ad site etered simultaeously as idepedet categorical variables. Differeces i sprig survival were aalysed betwee treatmets, havig bee corrected for site ad year, usig ANCOVA with treatmet, site ad year etered simultaeously ito the model as categorical variables ad adult desity i sprig as a cotiuous variable. The desig of the experimet with oe measure per site per year meat that at the moor-level iteractios betwee the categorical variables year ad treatmet could ot be cosidered. Furthermore, the reductio i degrees of freedom by iclusio of such a iteractio withi the model preveted the aalysis. Data were aalysed with respect to treatmet i both year t ad treatmet i year t 1. The latter was icluded to cosider ay effect of treatmet i the previous year o he coditio, breedig performace ad parasite burde i the followig year. Iclusio of treatmet i the precedig year, either o its ow, or i combiatio with treatmet i year t, did ot improve the explaatory power of ay of the models tested. No measure of he coditio, breedig performace or parasite burde varied sigificatly i relatio to treatmet i year t 1, hece all results quoted are from models that icluded treatmet i year t oly as a explaatory variable. Results BODY CONDITION AND BREEDING SUCCESS OF RADIO-TAGGED BIRDS A idex of he grouse coditio did ot differ either betwee grit applicatios (F 1,2 = 1 47, P = 0 35) or betwee sites (F 1,2 = 0 06, P = 0 83). However, there teded to be a differece betwee years (F 3,2 = 14 96, P = 0 06; Table 1). Mea clutch size did ot differ betwee years (F 3,2 = 0 99, P = 0 54), site (F 1,2 = 0 05, P = 0 84) or treatmet (F 1,2 = 0 01, P = 0 95) ad averaged 9 6 (± 0 3 SE) eggs (rage 6 15) for hes with access to medicated grit ad 9 4 (± 0 3 SE; rage 6 13) for hes with access to plai grit. Hatchig success did ot differ betwee years ( χ 3 2 = 0 04, P = 0 99),betwee site ( χ 1 2 = 0 01, P = 0 91) or betwee treatmet ( χ 1 2 = 0 12, P = 0 73). Mea hatchig success for eggs from hes with access to medicated grit was 90%, compared with 94% for eggs from hes with access to plai grit. Breedig success (chicks reared per he) differed betwee treatmets (F 1,2 = 45 37, P = 0 02; Table 2), with more tha twice as may chicks reared per he o the plot with medicated grit tha o the plot with plai grit. Breedig success teded to be positively correlated with body coditio i the sprig (r 7 = 0 57, P = 0 11) but ot sigificatly. Similarly, couts usig poiter dogs of o-radio-tagged hes withi the 100-ha areas showed breedig success to be 38% higher o the area with medicated grit tha o the area with plai grit Table 1. Body coditio of he grouse (mea ± SE) caught i February medicated grit plai grit 1997 10 3 7 ± 0 1 10 3 8 ± 0 1 1998 10 3 6 ± 0 1 10 3 3 ± 0 3 1999 10 3 4 ± 0 1 10 3 3 ± 0 1 2000 10 2 9 ± 0 2 10 2 7 ± 0 1
912 D. Newbor & R. Foster Table 2. Red grouse breedig success from radio-tagged birds ad from couts usig poitig dogs for both medicated ad plai grit areas i July Medicated grit Plai grit Radio-birds Dog couts Radio-birds Dog couts 1996 23 5 4 ± 0 3 23 4 0 ± 0 5 1997 10 6 6 ± 0 4 36 5 4 ± 0 3 10 4 8 ± 0 5 35 4 5 ± 0 3 1998 9 5 2 ± 1 0 25 5 5 ± 0 3 9 2 1 ± 0 7 18 2 6 ± 0 8 1999 10 7 1 ± 0 9 18 6 7 ± 0 5 9 2 9 ± 0 6 17 3 7 ± 0 7 2000 7 4 9 ± 1 3 23 4 9 ± 0 4 8 1 9 ± 0 7 24 2 8 ± 0 4 Table 3. Grouse desities (birds km 2 ) i sprig ad summer o medicated ad plai grit areas 1996 2000 Medicated grit Plai grit Sprig adults July adults July youg Sprig adults July adults July youg 1996 73 48 123 68 50 92 1997 83 75 194 86 74 161 1998 50 50 137 60 38 35 1999 28 36 122 45 34 63 2000 58 46 112 56 48 68 oly (F 1,3 = 24 77, P = 0 01). Breedig success did ot differ i relatio to either site or year for either radiotagged or o-radio-tagged hes. GROUSE DENSITIES Differeces i sprig ad July desities were aalysed i relatioship to site, treatmet ad year. Sprig grouse desities did ot differ either betwee sites (F 1,3 = 0 29, P = 0 63) or betwee treatmets (F 1,3 = 1 27, P = 0 34) but differed betwee years (F 4,3 = 13 24, P = 0 03; Table 3). The pre-harvest July desities did ot differ betwee sites (F 1,3 = 0 01, P = 0 91) but differed sigificatly betwee years (F 4,3 = 9 53, P = 0 05) ad betwee treatmets (F 1,3 = 13 15, P = 0 04). GROUSE SURVIVAL Two idices of red grouse survival were calculated to assess whether providig medicated grit affected survival. These were over-witer survival (July March) ad breedig survival (March July). No sigificat differece i over-witer survival was foud betwee sites (F 1,2 = 0 03, P = 0 88) or grittig treatmets (F 1,2 = 1 16, P = 0 39). Witer survival varied threefold betwee years, but this was ot sigificat (F 3,2 = 3 78, P = 0 22), probably due to idices oly beig derived for eight of the 10 site years ad the subsequet low power of ay resultat test. There was o differece i breedig survival of grouse betwee treatmet (F 1,2 = 0 22, P = 0 69), site (F 1,2 = 0 03, P = 0 89) or year (F 4,2 = 11 68, P = 0 08). Breedig survival did, however, differ i relatio to sprig desities of adults Table 4. Numbers of strogyle worms (mea ± SE) i shot adult grouse from medicated ad plai grit sites medicated grit (F 1,2 = 44 83, P = 0 02), with lowest survival i years of higher breedig desity. Over-witer survival did ot differ i relatio to July grouse desities. Data from radio-tagged birds supported observatios from couts, i.e. o differece betwee grittig treatmets. Survival of radio-collared birds was high, with a average of 90% of birds survivig the period February to the start of the shootig seaso i August of that year. PARASITE BURDENS I each year, grouse o the area with access to the medicated grit cotaied sigificatly lower parasite burdes tha the grouse with access to the plai grit, with the grouse o the medicated grit area havig 34% (± 2% SE) less worms (F 1,3 = 14 96 P = 0 03; Table 4). There were o differeces i worm burdes either betwee years (F 4,3 = 3 95, P = 0 14) or betwee sites (F 1,3 = 1 65, P = 0 29). No betwee-treatmet differeces, however, were foud amogst the radio-tagged hes, [F 1,13 = 0 88, P = 0 37; plai grit (5638 ± 2174 SE, = 9), medicated grit (3158 ± 1696 SE, = 11)]. plai grit 1996 12 2128 ± 818 4 4149 ± 4375 1997 16 6714 ± 1272 20 8629 ± 1005 1998 20 6309 ± 650 16 6714 ± 795 1999 14 2747 ± 1702 21 6516 ± 1199 2000 19 3828 ± 738 19 6382 ± 1072
913 Cotrol of parasites i grouse Discussio Access to medicated grit did ot sigificatly affect either clutch size, hatchig success or idices of grouse survival. He grouse with access to medicated grit, however, reared more chicks ad had lower parasite burdes i the autum followig treatmet. The mechaism that resulted i the icreased ability to rear chicks caot be deduced from this study. Oe explaatio could be that hes with access to medicated grit had, by reducig their worm burdes, improved their overall body coditio, which allowed them to care for ad rear their youg better (Hudso 1986a). It was also a possibility that the palm oil o the medicated grit was providig the birds with eergy ot available to the birds o the plai grit diet, thus icreasig their body coditio. However, the calories available to the birds from their daily itake of palm oil would be very low. Palm oil has a calorific value of approximately 7000 kcal kilo 1. The palm oil compoet of medicated grit is 2 5% of the total weight (Strathclyde Nutritio, Johstoe, Refrewshire, UK). Grouse take i a maximum of 2 g grit day 1 (Hudso 1992), 2 5% of which would be palm oil, givig a palm oil itake of 0 05 g; this i tur represets a calorific value of less tha half a calorie per day. From previous studies the daily calorie itake by red grouse for maiteace was foud to be betwee 88 ad 112 kcal day 1 (Moss & Parkiso 1972); the calorific value of palm oil therefore represets a very small percetage of their daily itake. Also, if the palm oil was cotributig to the calorie itake of the birds o the medicated area, a icrease i clutch size ad hatchig success may have bee recorded; o such icrease was foud. We do, however, ackowledge that palm oil may have made a small cotributio to the birds overall coditio. It has bee demostrated that reducig parasite burdes i grouse may help improve their coditio ad reduce scet emissio, makig the birds less vulerable to mammalia predators (Hudso, Dobso & Newbor 1992). However, Moss et al. (1990) did ot fid that hes with more T. teuis worms were more likely to be killed by predators. I fact, their results idicated that maturig T. teuis larvae i the caeca made he grouse less vulerable to predatio by foxes. Although this study did ot aim to test this hypothesis, o radio-collared grouse, irrespective of treatmet, were predated by foxes either durig icubatio or while rearig chicks. Previous research by Aderso & May (1978) has highlighted the importace of parasite-iduced reductio i host fecudity. Replicated field trials have show that grouse with experimetally reduced itesities of ifectio with T. teuis, through oral dosig with athelmitics, have icreased breedig success (Hudso 1986a). Similarly, this study has foud that grouse provided with free access to athelmitics had a reduced T. teuis burde ad a higher breedig success. Other studies have demostrated itrisic factors that may be resposible for poor breedig success other tha parasites. They foud the plae of utritio measured as the itroge ad phosphorus cotet of heather to be a importat factor ifluecig the breedig success of red grouse (Moss, Watso & Parr 1975). Similarly, high parasite burdes have also bee related to severe weather-related damage to heather, the bird s food (Watso et al. 1988). This type of damage, ofte referred to as heather browig, has previously bee associated with outbreaks of T. teuis (Jekis, Watso & Miller 1963). However, o large-scale heather browig was experieced o either of the two plots durig the 5 years of the preset study. To take ito cosideratio potetial differeces i the utritioal qualities of the heather betwee the two plots, the treatmets were switched betwee the plots durig the 5 years of the study. This should have reduced ay potetial biases caused by utritioal discrepacies betwee the two plots. Thus the data demostrated that higher breedig success was most likely to have arise from a reduced T. teuis burde i he grouse. It is likely that hes that had access oly to plai grit cotiued to pick up T. teuis larvae at similar rates to those hes with access to medicated grit. The he grouse with access to medicated grit were, however, able to reduce their worm retetio by igestig treated grit throughout the witer ad early sprig. This reductio i worm retetio was reflected by the 34% lower worm burdes ecoutered i shot grouse that had access to medicated grit, a differece similar to the 44% foud by Hudso (1992). No sigificat differece was foud i the autum worm burdes i shot radio-tagged hes betwee grittig treatmets. However, the sample size may have bee too small to show ay statistical differece betwee the two groups. Athelmitics, by reducig worm burdes i he grouse, eabled more chicks to be reared ad thereby elevated umbers of grouse i the autum available for shootig. It is likely that icreased pre-shootig desities resulted i more birds shot, but this could ot be quatified as data o the umber of birds shot withi each discrete area were ot available. Icreased harvestig ad the likelihood of desity-depedet dispersal of juveiles, at least of hes, away from their atal area (Hudso 1992) probably largely explai the lack of a observed icrease i sprig desities i the followig year. Provisio of medicated grit resulted i a mea icrease of 2 chicks he 1. Give a mea sprig desity of 26 pairs grouse km 2 (± 2 5 SE), a extra 52 grouse km 2 would be available i August to be harvested. If 40% of the extra grouse were shot (Hudso 1986b) this would provide 21 (10 5 brace) more grouse i the bag per km 2. With the average curret lettig value of 80 brace 1, this would provide a additioal retur of 840 km 2. The curret recommeded medicated grit applicatio rate is 1 to to 16 km 2 (Hudso & Newbor 1995) ad the price per toe is 991.70 (Strathclyde Nutritio, persoal commuicatio). The cost without labour (which would be
914 D. Newbor & R. Foster provided by the gamekeeper) of medicated grit to cover 1 km 2 would be 62, hece yieldig a et profit of 772 km 1. Thus medicated grit ehaces the ecoomic viability of red grouse shootig ad the maagemet of grouse moors by icreasig the July grouse populatio. Ackowledgemets We would like to thak Sir Tom Cowie ad the Strathmore Estate keeperig team for allowig access to the moor ad providig additioal labour whe required. We thak David Baies for statistical assistace ad advice o the mauscript. Peter Hudso kidly provided helpful commets o the mauscript. Refereces Aderso, R.M. & May, R.M. (1978) Regulatio ad stability of host parasite iteractios. I. Regulatory processes. Joural of Aimal Ecology, 47, 219 249. Chitty, D. (1967) The atural selectio of self-regulatory behaviour i aimal populatios. Proceedigs of the Ecological Society of Australia, 2, 51 78. Dobso, A.P. & Hudso, P.J. (1992) Regulatio ad stability of a free-livig host parasite system, Trichostrogylus teuis i red grouse. II. Populatio models. Joural of Aimal Ecology, 61, 487 498. Hudso, P.J. (1986a) The effect of a parasite ematode o the breedig productio of red grouse. Joural of Aimal Ecology, 55, 85 94. Hudso, P.J. (1986b) Red Grouse. The Biology ad Maagemet of a Wild Gamebird. The Game Coservacy Trust, Fordigbridge, UK. Hudso, P.J. (1992) Grouse i Space ad Time. The Game Coservacy Trust, Fordigbridge, UK. Hudso, P.J. (1995) Ecological treds ad grouse maagemet i uplad Britai. Heaths ad Moorlads: Cultural Ladscapes (eds D.B.A. Thompso, A.J. Hester & M.B. Usher), pp. 282 293. HMSO, Ediburgh, UK. Hudso, P.J. & Dobso, A.P. (1989) Populatio biology of Trichosrogylus teuis, a parasite of ecoomic importace for red grouse maagemet. Parasitology Today, 5, 283 291. Hudso, P.J. & Newbor, D. (1995) A Maual of Red Grouse ad Moorlad Maagemet. The Game Coservacy Trust, Fordigbridge, UK. Hudso, P.J., Dobso, A.P. & Newbor, D. (1985) Cyclic ad o-cyclic populatios of red grouse: a role for parasitism? Ecology ad Geetics of Host Parasite Iteractios (eds D. Rolliso & R.M. Aderso), pp. 79 89. Academic Press, Lodo, UK. Hudso, P.J., Dobso, A.P. & Newbor, D. (1992) Do parasites make prey vulerable to predatio? Red grouse ad parasites. Joural of Aimal Ecology, 61, 681 692. Hudso, P.J., Dobso, A.P. & Newbor, D. (1998) Prevetio of populatio cycles by parasite removal. Sciece, 282, 2256 2258. Jekis, D., Watso, A. & Miller, G.R. (1963) Populatio studies of red grouse Lagopus lagopus scoticus i orth-east Scotlad. Joural of Aimal Ecology, 32, 317 376. Lack, D. (1954) The Natural Regulatio of Aimal Numbers. Claredo Press, Oxford, UK. Lovat, S.J. (1911) Grouse i Health ad Disease. Smith, Elder, Lodo, UK. MacDoald, D.G.F. (1883) Grouse Disease: Its Causes ad Remedies. W.H. Alle, Lodo, UK. Moss, R. & Parkiso, J.A. (1972) The digestio of heather (Callua vulgaris) by red grouse (Lagopus lagopus scoticus). British Joural of Nutritio, 27, 285 298. Moss, R., Treholm, I.B., Watso, A. & Parr, R. (1990) Parasitism, predatio ad survival of he red grouse (Lagopus lagopus scoticus) i sprig. Joural of Aimal Ecology, 59, 631 642. Moss, R., Watso, A. & Parr, R. (1975) Materal utritio ad breedig success i red grouse (Lagopus lagopus scoticus). Joural of Aimal Ecology, 44, 171 190. Potts, G.R., Tapper, S.C. & Hudso, P.J. (1984) Populatio fluctuatios i red grouse: aalysis of bag records ad simulatio model. Joural of Aimal Ecology, 53, 171 189. Shaw, J.L., Moss, R. & Pike, A.W. (1989) Developmet ad survival of free-livig stages of Trichostrogylus teuis, a caecal parasite of red grouse. Lagopus lagopus scoticus. Parasitology, 99, 105 113. Short, L.L. Jr (1967) A review of the geera of grouse (Ave, Tetraoiae). America Museum Novitates, 2289, 1 39. Watso, A., Moss, R., Parr, R., Treholme, I.B. & Robertso, A. (1988) Prevetig a populatio declie of red grouse (Lagopus lagopus scoticus) by maipulatig desity. Experietia, 44, 274 275. Wilso, G.R. & Wilso, L.P. (1978) Haematology, weight ad coditio of captive red grouse (Lagopus lagopus scoticus) ifected with caecal threadworm (Trichostrogylus teuis). Research i Veteriary Sciece, 25, 331 336. Received 18 Jauary 2002; fial copy received 28 August 2002