The utilization of heather moorland by territorial Red Grouse Lagopus lagopus scoticus

Although the breeding density of Red Grouse Lagopus lagopus scoticus is related to the density of burned patches of heather Calluna vulgaris , territories appear to offer surplus food, and other factors, especially the risk of predation, may be important. In order to determine how Red Grouse make use of heather moorland, an individually marked population was studied on a moor in northeast Scotland from 1992 to 1994. Territorial birds preferred stands of tall heather during the daytime in autumn and winter, but in spring they increased their use of heterogeneous heather/grass mixtures. Furthermore, in spring, females showed a very strong affinity for edges between heather stands of different ages, where they had easy access to nutritious young heather and good cover. When near the vegetation edge, territorial birds spent most time on the side of the edge providing greater cover. Broods occupied ranges in areas with rather more old heather and with more edge than was available over the entire study site. Within their ranges though, broods clearly preferred heterogeneous areas during the first month after hatching, and showed a further preference for vegetation edge. Their behaviour changed during the second month after hatching, when they utilized tall heather to a greater extent, but edge remained important.     

Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus

Populations of red grouse ( Lagopus lagopus scoticus ) undergo regular multiannual cycles in abundance. The 'kinship hypothesis' posits that such cycles are caused by changes in kin structure among territorial males producing delayed density-dependent changes in aggressiveness, which in turn influence recruitment and regulate density. The kinship hypothesis makes several specific predictions about the levels of kinship, aggressiveness and recruitment through a population cycle: (i) kin structure will build up during the increase phase of a cycle, but break down prior to peak density; (ii) kin structure influences aggressiveness, such that there will be a negative relationship between kinship and aggressiveness over the years; (iii) as aggressiveness regulates recruitment and density, there will be a negative relationship between aggressiveness in one year and both recruitment and density in the next; (iv) as kin structure influences recruitment via an affect on aggressiveness, there will be a positive relationship between kinship in one year and recruitment the next. Here we test these predictions through the course of an 8-year cycle in a natural population of red grouse in northeast Scotland, using microsatellite DNA markers to resolve changing patterns of kin structure, and supra-orbital comb height of grouse as an index of aggressiveness. Both kin structure and aggressiveness were dynamic through the course of the cycle, and changing patterns were entirely consistent with the expectations of the kinship hypothesis. Results are discussed in relation to potential drivers of population regulation and implications of dynamic kin structure for population genetics.     

Testosterone and autumn territorial behavior in male red grouse Lagopus lagopus scoticus

In many bird species, males exhibit territorial aggression outside the breeding season, when testosterone concentrations are low and may not regulate territorial behaviors. The hormonal regulation of aggression at this time of year has only been studied in passerine birds. Here, we investigated the role of testosterone in the regulation of aggression in a non-passerine bird, the red grouse Lagopus lagopus scoticus. Male red grouse are aggressive in early spring when breeding starts, in autumn when they establish territories, and sporadically through much of the winter. We first describe seasonal variations in plasma testosterone concentrations and in the size of males' sexual ornaments, their red combs, which relates to aggressiveness. Testosterone concentrations and comb size were correlated. Both increased in autumn to a peak in October, and then increased again in spring, to a greater peak in early April. Secondly, we experimentally investigated the effects of testosterone, and of an anti-androgen (flutamide) used in combination with an aromatase inhibitor (ATD), on autumn territorial behavior. Males were treated with either empty implants, as controls (C-males), testosterone implants (T-males), or with flutamide and ATD implants (FA-males). One month after implanting, both T- and FA-males had higher concentrations of testosterone than C-males. Comb size, aggressive call rate, and response to playbacks of territorial call all significantly increased in T-males. However, the increase in testosterone in FA-males did not increase comb size or aggressive behavior. In the following spring, after the content of implants was used, FA-males had significantly lower testosterone than C-males, and had a reduced seasonal increase in comb size. The results suggest that testosterone plays a significant role in regulating red grouse aggressive behavior in autumn. However, the observation that flutamide and ATD treatment did not reduce territorial behavior, suggests that estradiol may also be involved in the regulation of non-breeding aggression.     

Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus)

Hypotheses for the cause of population cycles have focused on the role of intrinsic mechanisms such as spacing behaviour and extrinsic mechanisms such as parasitism and predation. This paper examines the interaction between the two dominant hypotheses in the cycles of red grouse, parasitism and spacing behaviour. The influence of the caecal nematode, Trichostrongylus tenuis, on male aggressiveness was investigated using two approaches. First, the territorial behaviour of a group of male grouse experimentally treated with an anthelmintic to reduce parasite intensities was compared with a control group with natural intensities of infection. Second, the response of treated and control males to a novel conspecific territorial intruder were recorded using playback tests. Treated males, with reduced levels of parasitism, won significantly more territorial contests than control males and produced more aggressive behaviour in response to the playback recordings. These results show that parasite removal enhanced aggressive behaviour. Implications of these results on red grouse population dynamics are discussed.     

Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus

Sexual ornaments may enable females to discriminate amongst potential mates and choose those having either fewer parasites, or those which are more immunocompetent, or better able to cope with parasites. Tetraonid birds exhibit supra-orbital combs that function in both intra-sexual competition and mate choice. Through a correlative and experimental approach we investigated whether comb size of male red grouse Lagopus lagopus scoticus was related to infection intensity by their main parasite, the gastro intestinal nematode Trichostrongylus tenuis , and to immune function. We first looked at the relationships between immune function, parasite infection and condition. We found that spleen mass, an indirect measure of immune response, correlated positively with T. tenuis load, and negatively with condition. Cell-mediated immunity, a measure of immune defence, correlated positively with condition, and although not significantly related to T. tenuis load, increased when nematode parasites were experimentally reduced. Secondly, we investigated whether comb size was related to condition, T. tenuis load or immune function. Comb size was not significantly related to T. tenuis infection and did not change significantly after nematode parasite removal. However, males with bigger combs were in better condition, had a lighter spleen, a lighter spleen than expected from their T. tenuis load and had greater cell-mediated immunity. The findings suggest that comb size relates to immune function rather than T. tenuis parasite infection intensity. Males with bigger combs are likely to be of higher phenotypic quality because they are more immunocompetent and might be better able to cope with the detrimental effects of parasites.     

General properties of predictive population models in red grouse (Lagopus lagopus scoticus)

Summary The general properties of an empirical predictive model of population fluctuations in red grouse are discussed. The model incorporates two observed time-lagged relationships between (a) chick production and spring numbers two years earlier, and (b) overwinter survival and numbers in spring one year earlier. The model produced oscillations which were slowly damped with a period of nine years. The addition of randomly-imposed poor breeding sustained the amplitude of oscillations but did not affect the period. Incorporating immigration at low densities reduced the amplitude but preserved the period. Cycle length varied with the model parameters but was generally between 8–10 years. A model with reduced lags of one and zero years could produce shorter cycles of 4–6 years.     

Mate choice by hen Red Grouse Lagopus lagopus with an excess of cocks—role of territory size and food quality

In a breeding population of Red Grouse the ratio of cocks to hens was about 2:1. Cocks with hens had bigger territories and richer feeding sites than unmated cocks. Despite this, the size of a cock's territory was inversely related to the level of nitrogen in his food. The idea that this was because cocks defend a territory just big enough to meet the pair's food requirements seemed inapplicable, since territories were much bigger than this. In addition, it was inferred that hens took longer to choose a cock on a part of the area that had relatively poor feeding sites. Whether hens chose the cock or his territory was uncertain, but both probably played a part.     

The pervalence of caecal threadworms (Trichostrongylus tenuis) in red grouse (Lagopus lagopus scoticus)

Summary Ninety percent of wild red grouse examined carried threadworms in their intenstinal caeca. Old birds had 30 times as many worms as young birds. Some infections were as high as 30,000 worms. The occurrence of worms in old grouse conformed to the negative binomial distribution.     

Spatial distribution of genetic relatedness in a moorland population of red grouse (Lagopus lagopus scoticus)

Several aspects of the ecology and biology of red grouse (Lagopus lagopus scoticus) could prevent the complete admixture of genes within and between populations. Male red grouse display a high degree of natal philopatry, are territorial, and show less aggression to kin man to non-kin. Such factors acting in combination predict limited male-mediated gene flow, which will promote social structure within a population by the formation of stable kin clusters, and facilitate a rapid rise in allelic coancestry and/or inbreeding. In this study we utilize hypervariable microsatellite polymorphisms to examine the extent of social affiliation between relatives in a moorland population of grouse from NE Scodand. Levels of genetic relatedness between individual male red grouse occupying territories at Glas Choille in die spring and autumn of 1995 were examined, and kin clusters delimited. Nine kin groups (mean size = 2.4 individuals) were identified prior to breeding in the spring, which increased to 11 kin groups (mean size =4.0 individuals) when territories were reformed in the autumn. The majority of tiiose individuals that were recruited into the adult population during the autumn already had a first-order male relative established, supporting the hypothesis that recruitment is facilitated by behavioural interactions among relatives. The demographic and population genetic consequences of philopatric recruitment and kin clustering are examined and discussed.     

Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers

Allelic variation at seven hypervariable tri- and tetranucleotide microsatellite loci was used to determine levels of population differentiation between 14 populations of red grouse ( Lagopus lagopus scoticus ) in northeast Scotland, UK. Despite the potential for long-distance dispersal in grouse, and a semicontinuous habitat, significant population divergence was observed (mean R _ST = 0.153; P < 0.01) and an isolation-by-distance effect detected (Mantel test: P < 0.001). Examination of the spatial trend in principal component scores derived from allele frequencies among populations highlighted a barrier to gene flow that was confounding a simple isolation-by-distance effect. This barrier corresponded to an area of unsuitable habitat for grouse associated with a river system that bisected the study area. Mean genetic relatedness was higher for males than for females in all but one of the study populations, suggesting that the territorial behaviour and natal philopatry displayed by cocks have a manifold effect in generating the observed spatial genetic structure. Lower female relatedness values suggest a higher level of female-mediated gene flow, which is sufficient to prevent the loss of genetic variation from within populations and the onset of inbreeding effects. The potential consequences of local subdivision for red grouse populations are discussed.     

Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus

The reliability of different egg counting methods for estimating the intensity of Trichostrongylus tenuis infections in red grouse, Lagopus lagopus scoticus, was investigated in the autumn, when grouse may harbour high parasite intensities. Possible limitations to the use of these methods were also examined. Faecal egg counts were found to accurately estimate T. tenuis worm intensities, at least up to an observed maximum of c. 8000 worms. Two egg counting methods (smear and McMaster) gave consistent results, although the exact relationship with worm intensity differed according to the method used. Faecal egg counts significantly decreased with increasing length of sample storage time, but egg counts were reliable for estimating worm intensity for three weeks. The concentration of eggs in the caecum was also found to reliably estimate worm intensity. However, egg counts from frozen gut samples cannot be used to estimate worm intensities. These results conclude that, despite some limitations, faecal and caecum egg counts provide useful and reliable ways of measuring T. tenuis intensities in red grouse.     

Sequence Polymorphism in Candidate Genes for Differences in Winter Plumage between Scottish and Scandinavian Willow Grouse (Lagopus lagopus)

Background

Population variation in the degree of seasonal polymorphism is rare in birds, and the genetic basis of this phenomenon remains largely undescribed. Both sexes of Scandinavian and Scottish Willow grouse (Lagopus lagopus) display marked differences in their winter phenotypes, with Scottish grouse retaining a pigmented plumage year-round and Scandinavian Willow grouse molting to a white morph during winter. A widely studied pathway implicated in vertebrate pigmentation is the melanin system, for which functional variation has been characterised in many taxa.

Methodology/Principal Findings

We sequenced coding regions from four genes involved in melanin pigmentation (DCT, MC1R, TYR and TYRP1), and an additional control involved in the melanocortin pathway (AGRP), to investigate the genetic basis of winter plumage in Lagopus. Despite the well documented role of the melanin system in animal coloration, we found no plumage-associated polymorphism or evidence for selection in a total of ∼2.6 kb analysed sequence.

Conclusions/Significance

Our results indicate that the genetic basis of alternating between pigmented and unpigmented seasonal phenotypes is more likely explained by regulatory changes controlling the expression of these or other loci in the physiological pathway leading to pigmentation.     

Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflect nematode parasite intensity

In many birds, females prefer males with the biggest or brightest sexual ornaments, which might reflect a higher phenotypic quality, such as fewer parasites. Unlike humans, most birds detect near-ultraviolet (UV) light, and UV signals can play an important role in sexual signalling and mate choice. Using a spectrophotometer, we analysed the colour of red grouse Lagopus lagopus scoticus sexual ornaments (their combs). We first show that combs reflect both in the red (600–700 nm) and UV (300–400 nm) part of the spectrum. Second, we investigated whether comb size and colour, and UV reflectance in particular, reflected an aspect of individual quality: the intensity of infection by a main nematode parasite, the caecal threadworm Trichostrongylus tenuis . We first analysed comb size and colour variation, and parasite intensity variation, in relation to sex and age. Males had bigger and redder combs than females, but UV brightness was greater for female than for male combs. Comb colour also differed between age groups, with young birds of both sexes showing brighter UV than old birds. Young grouse also had fewer T. tenuis worms than old grouse. We further tested whether intensity of infection could be predicted from comb characteristics (size and colour) in male and female red grouse. We found that parasite intensity was not significantly related to comb size or red brightness, but fewer worms were predicted from brighter UV in combs, in both males and females. The results indicate that UV reflectance of combs have a quality revealing function and might play an important role in grouse mate choice: UV brightness of combs could enable both male and female red grouse to assess the parasite loads of a potential mate.