Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse

The causes of population cycles fascinate and perplex ecologist. Most work have focused on single processes, whether extrinsic or intrinsic, more rarely on how different processes might interact to cause or mould the unstable population dynamics. In red grouse (Lagopus lagopus scoticus), two causal mechanisms have been supported: territorial behaviour (changes in autumn aggressiveness) and parasites (parasite induced reduction in fecundity). Here, we report on how these two regulatory processes might interact, by testing whether the parasite suspected to cause the grouse cycles, the nematode Trichostrongylus tenuis, reduces male autumn territorial behaviour. We either treated males with an anthelmintic, to remove parasites (dosed or D-males), or challenged them with infective T. tenuis larvae, to increase parasite intensity (challenged or C-males). We first show that dosing was effective in removing T. tenuis parasites, while parasite intensities increased in challenged birds during the autumn. Because old males initially had more parasites than young males, the treatments generated greater differences in parasite intensity in old than in young males. We also show that various aspects of territorial behaviour (increase in testosterone-dependent comb size in autumn, territorial call rate, likelihood of winning territorial interactions and over-winter survival) were significantly higher in dosed than in challenged males, but in old birds only. Our data thus supported the hypothesis that parasites reduce male aggressiveness during the autumn territorial contests, and could thereby influence recruitment. Our results also highlight that the territorial behaviour of young males, which have fewer parasites, is not as limited by parasites as that of old, previously territorial males. We discuss the implications of these findings for our understanding of the processes regulating red grouse populations and causing their complex, unstable population dynamics.     

Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance

Extravagant ornaments evolved to advertise their bearers'' quality, the honesty of the signal being ensured by the cost paid to produce or maintain it. The oxidation handicap hypothesis (OHH) proposes that a main cost of testosterone-dependent ornamentation is oxidative stress, a condition whereby the production of reactive oxygen and nitrogen species (ROS/RNS) overwhelms the capacity of antioxidant defences. ROS/RNS are unstable, very reactive by-products of normal metabolic processes that can cause extensive damage to key biomolecules (cellular proteins, lipids and DNA). Oxidative stress has been implicated in the aetiology of many diseases and could link ornamentation and genetic variation in fitness-related traits. We tested the OHH in a free-living bird, the red grouse. We show that elevated testosterone enhanced ornamentation and increased circulating antioxidant levels, but caused oxidative damage. Males with smaller ornaments suffered more oxidative damage than those with larger ornaments when forced to increase testosterone levels, consistent with a handicap mechanism. Parasites depleted antioxidant defences, caused oxidative damage and reduced ornament expression. Oxidative damage extent and the ability of males to increase antioxidant defences also explained the impacts of testosterone and parasites on ornamentation within treatment groups. Because oxidative stress is intimately linked to immune function, parasite resistance and fitness, it provides a reliable currency in the trade-off between individual health and ornamentation. The costs induced by oxidative stress can apply to a wide range of signals, which are testosterone-dependent or coloured by pigments with antioxidant properties.     

Testing the interactive effects of testosterone and parasites on carotenoid‐based ornamentation in a wild bird

Abstract Testosterone underlies the expression of most secondary sexual traits, playing a key role in sexual selection. However, high levels might be associated with physiological costs, such as immunosuppression. Immunostimulant carotenoids underpin the expression of many red‐yellow ornaments, but are regulated by testosterone and constrained by parasites. We manipulated testosterone and nematode burdens in red grouse (Lagopus lagopus scoticus) in two populations to tease apart their effects on carotenoid levels, ornament size and colouration in three time‐step periods. We found no evidence for interactive effects of testosterone and parasites on ornament size and colouration. We showed that ornament colouration was testosterone‐driven. However, parasites decreased comb size with a time delay and testosterone increased carotenoid levels in one of the populations. This suggests that environmental context plays a key role in determining how individuals resolve the trade‐off between allocating carotenoids for ornamental coloration or for self‐maintenance needs. Our study advocates that adequately testing the mechanisms behind the production or maintenance of secondary sexual characters has to take into account the dynamics of sexual trait expression and their environmental context.     

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.     

Elevated spring testosterone increases parasite intensity in male red grouse

The expression of testosterone-dependent sexual traits mightsignal the ability of their bearers to cope with parasite infections.According to the immunocompetence handicap hypothesis (IHH),such signals would be honest because physiological costs oftestosterone, such as a reduced ability to control parasiteinfections, would prevent cheating. We tested whether testosteronewould affect the outcome of a standardized parasite challengein red grouse, using a main parasite of the species, the nematodeTrichostrongylus tenuis. We caught males in spring, removedtheir nematode parasites, and implanted them with testosteroneor empty implants, as controls. After 1 month, they were reinfectedwith a standard dose of infective T. tenuis parasites. Whenchallenged, testosterone males had relatively less globulinrelative to albumin plasma proteins than control males, an indicationthat they had experienced increased physiological stress. Testosterone-treatedmales had significantly more T. tenuis parasites than controlsin the next autumn and also had more coccidia and lost moreweight than controls. Testosterone-treated males neverthelessbenefited from their elevated spring testosterone: they hadbigger sexual ornaments than controls both in spring and autumn,and they tended to have a higher pairing and breeding successthan controls. Our results supported the IHH in showing thatelevated testosterone impaired the ability of males to copewith a standardized challenge by a dominant parasite. Testosteronethus plays a key role in mediating trade-offs between reproductiveactivities and parasite defense, and testosterone-dependentcomb size might honestly signal the ability of red grouse tocontrol T. tenuis infection.     

Physiological stress links parasites to carotenoid‐based colour signals

Vertebrates commonly use carotenoid‐based traits as social signals. These can reliably advertise current nutritional status and health because carotenoids must be acquired through the diet and their allocation to ornaments is traded‐off against other self‐maintenance needs. We propose that the coloration more generally reveals an individual’s ability to cope with stressful conditions. We tested this idea by manipulating the nematode parasite infection in free‐living red grouse (Lagopus lagopus scoticus) and examining the effects on body mass, carotenoid‐based coloration of a main social signal and the amount of corticosterone deposited in feathers grown during the experiment. We show that parasites increase stress and reduce carotenoid‐based coloration, and that the impact of parasites on coloration was associated with changes in corticosterone, more than changes in body mass. Carotenoid‐based coloration appears linked to physiological stress and could therefore reveal an individual’s ability to cope with stressors.     

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.     

Efficacy of acaricidal tags and pour-on as prophylaxis against ticks and louping-ill in red grouse

Abstract This paper examines the efficacy of 10% lambdacyhalothrin-impregnated plastic tags and a deltamethrin pour-on preparation in protecting red grouse chicks from parasitism by ticks and subsequent infection with the louping-ill virus. In 1995, ten red grouse hens ( Lagopus lagopus scoticus ) in a free-living population in north-east Scotland were fitted with lambdacyhalothrin-impregnated plastic tags, glued to radio transmitters. Chicks of more than 10 days of age from a further ten untreated radio-collared hens were caught and fitted with individual tags to the plagium. Both treatments significantly reduced tick burdens in the short term. The number of larvae and nymphs on chicks up to 45 days was less under both treatments than on control chicks and tagged chicks had fewer nymphs than chicks from treated hens. Nevertheless, treatments did not reduce viral infection rates nor increase survival to 10 weeks, possibly explained by incomplete treatment of tagged broods and/or direct or indirect mortality due to tags. In 1996 chicks in ten broods from hens with radio transmitters were individually treated at 14 days of age at a rate of lmg/kg of chick with a deltamethrin pour-on preparation. This preparation significantly reduced the number of larvae and nymphs on grouse chicks 7–10 days after application below the number on untreated controls. At 20 days from application, however, only larval numbers were lower on treated chicks. Nevertheless louping-ill virus infection prevalences were significantly reduced at 35 days of age and survival of chicks to 10 weeks increased.     

Rising burden of immature sheep ticks (Ixodes ricinus) on red grouse (Lagopus lagopus scoticus) chicks in the Scottish uplands

The sheep tick Ixodes ricinus (L.) (Acari: Ixodidae) is an ectoparasite of major economic and pathogenic importance in Scotland. Its distribution in the Scottish uplands is assumed to be governed by the abundance and distribution of its definitive hosts (deer and sheep) and climatic variables such as temperature and rainfall. As the numbers of its major host in Scotland, red deer, have increased dramatically and climatic conditions have become more favourable, the level of parasitism could have been expected to rise. We use data gathered from tick counts on over 4000 red grouse chicks Lagopus lagopus scoticus Latham (Galliformes: Tetraonidae) in various experiments over the past 19 years to ascertain whether the intensity and prevalence of parasitism has been increasing. From 1985 to 2003 the average tick burden of a parasitized red grouse chick has grown from 2.60 +/- 1.12 ticks per chick to 12.71 +/- 1.44. Over this period the percentage of chicks of a given brood parasitized has also increased from 4 +/- 2% to 92 +/- 3%. The possible implications of this increase in parasitism for red grouse production are discussed.     

Testosterone, immunocompetence, and honest sexual signaling in male red grouse

The expression of sexual ornaments has been suggested to reliablyindicate individual quality, such as the ability to cope withparasites and diseases. The Immunocompetence Handicap Hypothesis(IHH) states that testosterone-dependent ornaments honestlysignal such quality because of physiological costs associatedwith testosterone, such as impaired immune function. We testedpredictions of the IHH both correlatively and experimentallyin red grouse Lagopus lagopus scoticus. Male grouse exhibitsupra-orbital red combs whose size is testosterone-dependent.We found that comb size was not correlated to infection intensityby two parasites (coccidia and the nematode Trichostrongylustenuis), but it was significantly positively correlated withcondition and T-cell-mediated immunity (the ability to mounta primary inflammatory response). We manipulated testosteroneby means of implants and re-caught males after a month to investigatethe effects on comb size, condition, immunity, and parasiteload. Males implanted with testosterone had increased comb size,lost more condition, and had lower T-cell-mediated immunitythan control males. Increased testosterone also resulted ina significant increase in coccidia infection intensity but hadno effect on T. tenuis burden. The results are consistent withpredictions of the IHH and suggest that comb size honestly indicatesimmunocompetence and males' ability to cope with certain parasites.Females could thus benefit from choosing mates based on theexpression of this sexual trait.     

Effects of Perennial Peanut (Arachis glabrata) Ground Cover on Nematode Communities in Citrus

The effects of perennial peanut (Arachis glabrata) ground cover on the nematode community in a citrus orchard were examined. Samples were taken from two different ground cover treatments (perennial peanut or bare ground) at each of three distances from the tree trunk. Richness, measured as total numbers of nematode genera per sample, and total numbers of nematodes were greatest in the perennial peanut treatment (P < 0.05). Abundance of many genera of bacterivores, fungivores, and omnivores were increased by the perennial peanut ground cover. Total numbers of plant parasites were greater in perennial peanut treatments on three of the five sampling dates (P < 0.05), mainly due to trends in numbers of Mesocriconema. Distance from a tree trunk and the interaction of ground cover treatments and proximity to a tree trunk were most influential for Belonolaimus and Hoplolaimus. Although differences among treatments were observed for nematode genera and trophic groups, ecological indices were not consistently sensitive to treatments. Among several ecological indices evaluated, richness was most often affected by ground cover treatment.     

Resistance of Cucumis spp. to the Root-knot Nematode,Meloidogyne incognita acrita

The nature of resistance in Cucumis ficifolius and C. metuliferus to the root-knot nematode, Meloidogyne incognita acrita, was studied under greenhouse conditions. Although as many larvae penetrated the roots of these species as those of the susceptible C. melo, few developed to the adult female stage. Resistance in C. ficifolius and C. metuliferus was associated with hindrance of larval development beyond the second stage, delayed development of larvae to adults and stimulation toward maleness. Tissue necrosis or hypersensitivity was not associated with larval penetration. Comparisons of the histopathology of 26-day-old infections of C. melo and C. metuliferus roots showed no observable differences in the type of giant cell development in regions of roots associated with adult females. However, in C. rnetuliferus immature nematodes were associated with small giant cells which were limited to a few cells near the head of the nematode.     

Detection and Description of Soils with Specific Nematode Suppressiveness

Soils with specific suppressiveness to plant-parasitic nematodes are of interest to define the mechanisms that regulate population density. Suppressive soils prevent nematodes from establishing and from causing disease, and they diminish disease severity after initial nematode damage in continuous culturing of a host. A range of non-specific and specific soil treatments, followed by infestation with a target nematode, have been employed to identify nematode-suppressive soils. Biocidal treatments, soil transfer tests, and baiting approaches together with observations of the plant-parasitic nematode in the root zone of susceptible host plants have improved the understanding of nematode-suppressive soils. Techniques to demonstrate specific soil suppressiveness against plant-parasitic nematodes are compared in this review. The overlap of studies on soil suppressiveness with recent advances in soil health and quality is briefly discussed. The emphasis is on methods (or criteria) used to detect and identify soils that maintain specific soil suppressiveness to plant-parasitic nematodes. While biocidal treatments can detect general and specific soil suppressiveness, soil transfer studies, by definition, apply only to specific soil suppressiveness. Finally, potential strategies to exploit suppressive soils are presented.