BACKGROUND
pathogens and parasites can have major direct impacts on host population dynamics through increases in mortality and morbidity  <cit> , sometimes leading to host extinction  <cit> .
however, they can also have more subtle effects on host physiology  <cit> , behaviour  <cit>  and ecology  <cit> , which can also affect host survival and population dynamics  <cit> .
the impacts of pathogens on their hosts are dependent upon the ecology, behaviour and life history of both host  <cit>  and parasite  <cit>  species.
environmental factors such as variation in ambient temperature can increase or decrease host condition and therefore susceptibility, as well as parasite behaviour and virulence, leading to a critical influence on the outcome of host-parasite interactions, even over relatively small temperature ranges  <cit> .
environmental stress, such as that caused by extreme temperature events  <cit> , reduced food availability  <cit> , exposure to pesticides  <cit>  or anthropogenic disturbance  <cit>  may thus amplify the costs of parasitism  <cit>  through impacts on the costs of an immune response  <cit>  through increased energy demands  <cit> .
any impacts of parasitic infection may be particularly important in declining populations, which are often under additional pressure from factors such as loss of habitat and food  <cit> .
multiple stress-inducing factors can have synergistic effects  <cit> , with both physiological  <cit>  and ecological consequences  <cit> .
declining populations may thus be at greater risk than stable populations from the sub-lethal effects of pathogens and parasites.
previous studies of avian blood parasites have mainly investigated impacts of parasitism during the breeding season, when environmental stress tends to be relatively low but hormones may reduce the efficacy of the host immune system leading to relapses of infection  <cit> .
these studies have shown consistent negative impacts of blood parasite infection on reproductive performance across all stages of breeding  <cit> , as well as associations with physiological variables such as feather length and bill colour  <cit>  which are likely to be determined outside the breeding period.
allander and sundberg  <cit>  suggested that the possible costs of parasites outside the breeding season required further study.
despite this, the potential impacts of blood parasites during the non-breeding season have seldom been investigated.
two exceptions are recent work by cosgrove et al.
<cit> , who found plasmodium spp.
to be absent from a population of blue tits cyanistes caeruleus during the winter months, and by barnard et al.
<cit> , who found haematozoa to be present in wintering populations of the declining rusty blackbird euphagus carolinus and suggest a non-seasonal relapse of infections among overwintering birds.
martínez-de la puente et al.
<cit>  found a reduction in survival between infected and medicated blue tits, suggesting differential mortality outside the breeding season.
we suggest that, in temperate regions, the impacts of parasites and pathogens may be just as severe during the winter months, when food is scarce and temperatures are lower than during the breeding season, leading to higher energetic trade-offs between immune function and thermostatic maintenance e.g.
<cit> .
here, we carry out an exploratory study into the potential for blood parasites to impact their avian hosts outside the breeding season.
we use a population of yellowhammers emberiza citrinella, a declining farmland specialist of conservation concern in the uk  <cit> , infected with blood parasites of the genus haemoproteus.
haemoproteus parasites are generally transmitted during the breeding season by vectors of the families ceratopogonidae and hippoboscidae <cit> , and parasite intensity in passerine hosts peaks during the breeding season e.g.
<cit> .
hosts usually recover from infection but allander & sundberg  <cit>  point out that haemoproteus infections are likely to occur in their hosts long after the breeding season.
we examine associations with sub-clinical disease at the immunological and physiological levels, and we use a physiological trait linked with infection to examine potential population-level implications of infection.
whilst our data are correlative, our main aim here is to highlight the potential for such mechanisms to act outside of the breeding season , and to suggest directions and priorities for future research.
RESULTS
of the  <dig> samples from  <dig> birds that were screened for the presence of haematozoa, 47% of samples were positive for haemoproteus infection.
we found two strains of haemoproteus in our population  <cit> , but as we only sequenced a subset of positive samples, we grouped these two strains together for further analysis.
infection intensity is described elsewhere in more detail  <cit> , but mean infection intensity in a random sub-sample of birds confirmed as infected through pcr  was  <dig>  parasites per  <dig>  erythrocytes .
year-specific data summaries for all variables are provided in additional file  <dig>
immunological impacts of blood parasites
measures of both chronic stress and immune system activity  were influenced by parasite infection status .
controlling for lymphocyte numbers, infected birds had 35% lower heterophil counts on average than uninfected birds , resulting in a reduced h:l ratio.
similarly, controlling for wbc numbers, infected birds had fewer erythrocytes compared to uninfected birds, resulting in a 60% higher mean standardised wbc count .
for significant terms, parameter estimates with se are presented; for non-significant main effects, statistics follow reinsertion of the term into the minimum adequate model  and subsequent model comparison.
parameter estimates for two level factors are for the stated factor compared to the other factor; estimates for month are for the stated month when compared to april.
‘na’ indicates that this term was not included in the model.
morphological associations with parasitism
wing length was associated with both an interaction between age and sex , and an interaction between haemoproteus infection status and year .
post hoc analyses indicated that in the winter of 2007/ <dig>  birds infected with haemoproteus had shorter wings than uninfected birds  but in the winter of 2008/ <dig>  this was not the case .
when the lowest maximum temperature prior to the sampling date during each winter was substituted into the minimum adequate model  in place of year, the model explained the same amount of variation as that containing year , with mean population wing length decreasing as lowest maximum temperature increases.
no association with infection status was found for either head-beak length  or tarsus length .
for significant terms, parameter estimates with se are presented; for non-significant terms, statistics follow reinsertion of the term into the minimum adequate model  and subsequent model comparison.
survival analysis
using the most parsimonious recapture model , survival models were estimated .
the ∆qaicc between the top three models was < <dig>  so we used model averaging to produce parameter estimates .
survival was positively affected by wing length and sex , and recapture probability decreased with time, although not linearly .
Φ  remains as a constant in this model; npar shows the number of parameters; qaicc is the adjusted aic value following correction for overdipersion, and ∆qaicc shows the difference between the specified model and the ‘best’ model.
models with a ∆qaicc <  <dig> are considered not to differ from the best model.
the model with time alone was found to be the best model for predicting the probability of recapture , and thus p remains as a constant in this model; npar shows the number of parameters; qaicc is the adjusted aic value following correction for overdipersion, and ∆qaicc shows the difference between the specified model and the ‘best’ model.
models with a ∆qaicc <  <dig> are considered not to differ from the best model.
discussion
understanding the drivers of population dynamics is a major challenge in population biology, particularly when populations are declining and require mitigation strategies to prevent extinction.
many european farmland birds have declined following farmland intensification and this has been hypothesised as being due to combinations of loss of habitat, shortages of summer and winter food, or a multiplicity of causes  <cit> .
here we add a further potential cause as we show, for the first time, high parasite prevalence in winter, a season associated with significant mortality.
this is coupled with evidence suggestive of immunological challenge and a physiological response that may potentially impact upon survival, and we suggest that declining populations may make good systems within which to examine this previously overlooked period in host-parasite ecology.
whilst results here are purely correlative, we discuss the potential implications of our data that warrant further, experimental, work.
the high prevalence of infection found in our population suggests either a high incidence of chronic infections, or stress-induced relapse of existing infections.
the vectors of blood parasites tend to be dormant during the winter months, considerably reducing the transmission of new infections  <cit> .
for haemoproteus parasites, microscopy and pcr techniques tend to provide similar prevalence estimates  <cit> , although fallon & ricklefs  <cit>  found 25-35% of pcr-detected haemoproteus infections to be undetected through examination of blood smears.
infection intensities within our population are relatively low when compared to other passerine-haemoproteus spp.
systems  during the summer months, possibly suggesting that our findings represent the chronic stages of infection, rather than relapses.
unfortunately infection intensity data from our study species during the breeding season is, to our knowledge, only presented in allander and sundberg  <cit>  but this paper measures parasites per  <dig> microscope fields and does not standardise measurements by erythrocyte abundance, so we are unable to make direct comparisons, although these data from our population would be valuable in assessing the relative effects of parasitism between the breeding and non-breeding periods.
however, as the non-infective asexual stages of haemoproteus reside in the tissues and only infective gametocytes are present in the peripheral circulation  <cit> , this suggests that our findings represent active infections  and has further implications for the over-winter ecology of avian blood parasites in temperate species.
haemoproteus infection was associated with both a reduced h:l ratio, and an increased wbc count.
the h:l ratio is generally expected to increase in response to infection  <cit> , whereas our data suggest the opposite.
similarly to our data however, other systems have also found a reduction in h:l ratio associated with haemoproteus infection  <cit> , and galeotti and sacchi  <cit>  suggest that the reduction in h:l ratio is explained by the higher concentration of lymphocytes overall, triggered by an increase in immune system activity  <cit> .
this is demonstrated in our data by the increased wbc count in infected individuals, and suggests a direct immune cost of haemoproteus infection in this species.
h:l ratio is also strongly positively correlated with corticosterone levels  <cit> , but increases with increasing environmental stress, so these data do not support the idea that increased corticosterone, induced by food stress or poor weather, induces relapses of active parasite infection  <cit> .
however, an increase in immune activity also carries costs  <cit> : for example, in the house sparrow passer domesticus, haemoproteus infection reduces immune response to a second immune challenge  <cit> .
increased immune activity leads to an increased short-term energy consumption which, even at the levels of a 5-15% increase in energy expenditure calculated by hasselquist & nilsson  <cit>  may amplify the impacts of sub-clinical disease at times of food- or weather-related stress, or in populations already under environmental pressure.
we found year-dependent associations between parasite infection and reduced feather length, with no such relationship with skeletal measures of size, suggesting that under certain conditions, parasites can influence feather length through competition for host resources during moult  <cit> , although we acknowledge that this relationship may be mediated by a third, unknown, factor such as body condition during moult.
whilst our parasite data are from the winter months, rather than from months when moult was occurring, the presence of parasites during winter suggests that they were also present during the preceding post-breeding moult , as post-breeding tends to be the time when infection rates are highest in other systems  <cit> .
in addition, parasite intensities between peak parasite intensity and chronic infections can be correlated  <cit>  and novel infections between the end of moult and the winter months may be relatively unlikely due to cessation of vector activity, although further work would be required to confirm this.
a larger dataset of repeat within-individual data between years would be of great value in elucidating whether this association with wing length occurs at an individual level in relation to infection intensity.
the replacement of year with lowest maximum temperature explained a similar amount of variation in the statistical model, suggesting that temperature may underlie the relationship between parasitism, wing length and year.
parasite prevalence was higher during the second year of the study, coinciding with fewer birds sampled despite similar sampling effort  <cit> , suggesting fewer birds in the population.
this is unlikely to be due to birds moving out of the study area during the second year, as yellowhammers in the uk show very low dispersal  <cit>  and our population showed a relatively high winter-summer fidelity as estimated through colour-ring re-sightings .
instead, this may have been due to an early cold spell during autumn  <dig> , leading to an increase in energy requirements and consequently food requirements, thus resulting in increased over-winter mortality.
given the association between infection and wing length was found only during the first year of sampling when the weather was mild and more birds were caught, and that our survival analysis indicated that birds with longer wings had an enhanced survival probability, it seems plausible that those birds susceptible to physiological effects of parasitism may be more likely to succumb to food stress during a cold winter such as that of the second year of the study and thus be removed from the population.
however, this suggestion is speculative and requires further investigation, preferably by inclusion of blood parasite intensity data in the survival analysis.
farmland birds more generally are under pressure from reduced nesting habitat availability, reduced quality of available nesting habitat, and reductions in both summer and winter food availability  <cit> .
here, we suggest that parasites may also play a significant role in the ecology of declining populations, potentially by interacting with other environmental stressors.
these interactions have the potential to occur both within and outside the breeding season, and we suggest that declining populations, especially those such as ours that remain resident outside the breeding season, would make excellent study systems for the examination of such relationships within and between seasons.
CONCLUSIONS
whilst our data are correlative and thus our results are speculative in terms of causality, we show associations between parasite infection and immune function, and between parasite infection and a physiological trait that we show to be of ecological significance.
our data suggest that the impacts of parasites outside the breeding season may be more important than previously thought, especially in species already under stress due to other ecological factors, such as food stress.
consequently, we also suggest that future experimental research on the ecological impacts of parasitism should examine potential impacts outside the breeding season, and should focus on populations already under pressure due to other ecological factors where these effects are likely to be more pronounced.
our results further suggest that considering sub-clinical disease may be critical when examining the conservation of declining populations.

 pathogens and parasites can have major direct impacts on host population dynamics through increases in mortality and morbidity, sometimes leading to host extinction. however, they can also have more subtle effects on host physiology, behaviour and ecology, which can also affect host survival and population dynamics. the impacts of pathogens on their hosts are dependent upon the ecology, behaviour and life history of both host and parasite species. environmental factors such as variation in ambient temperature can increase or decrease host condition and therefore susceptibility, as well as parasite behaviour and virulence, leading to a critical influence on the outcome of host-parasite interactions, even over relatively small temperature ranges. environmental stress, such as that caused by extreme temperature events, reduced food availability, exposure to pesticides or anthropogenic disturbance may thus amplify the costs of parasitism through impacts on the costs of an immune response through increased energy demands. any impacts of parasitic infection may be particularly important in declining populations, which are often under additional pressure from factors such as loss of habitat and food. multiple stress-inducing factors can have synergistic effects, with both physiological and ecological consequences. declining populations may thus be at greater risk than stable populations from the sub-lethal effects of pathogens and parasites. previous studies of avian blood parasites have mainly investigated impacts of parasitism during the breeding season, when environmental stress tends to be relatively low but hormones may reduce the efficacy of the host immune system leading to relapses of infection. these studies have shown consistent negative impacts of blood parasite infection on reproductive performance across all stages of breeding, as well as associations with physiological variables such as feather length and bill colour which are likely to be determined outside the breeding period. allander and sundberg suggested that the possible costs of parasites outside the breeding season required further study. despite this, the potential impacts of blood parasites during the non-breeding season have seldom been investigated. two exceptions are recent work by cosgrove et al., who found plasmodium spp. to be absent from a population of blue tits cyanistes caeruleus during the winter months, and by barnard et al., who found haematozoa to be present in wintering populations of the declining rusty blackbird euphagus carolinus and suggest a non-seasonal relapse of infections among overwintering birds. martínez-de la puente et al. found a reduction in survival between infected and medicated blue tits, suggesting differential mortality outside the breeding season. we suggest that, in temperate regions, the impacts of parasites and pathogens may be just as severe during the winter months, when food is scarce and temperatures are lower than during the breeding season, leading to higher energetic trade-offs between immune function and thermostatic maintenance e.g.. here, we carry out an exploratory study into the potential for blood parasites to impact their avian hosts outside the breeding season. we use a population of yellowhammers emberiza citrinella, a declining farmland specialist of conservation concern in the uk, infected with blood parasites of the genus haemoproteus. haemoproteus parasites are generally transmitted during the breeding season by vectors of the families ceratopogonidae and hippoboscidae, and parasite intensity in passerine hosts peaks during the breeding season e.g.. hosts usually recover from infection but allander & sundberg point out that haemoproteus infections are likely to occur in their hosts long after the breeding season. we examine associations with sub-clinical disease at the immunological and physiological levels, and we use a physiological trait linked with infection to examine potential population-level implications of infection. whilst our data are correlative, our main aim here is to highlight the potential for such mechanisms to act outside of the breeding season, and to suggest directions and priorities for future research.  of the samples from birds that were screened for the presence of haematozoa, 47% of samples were positive for haemoproteus infection. we found two strains of haemoproteus in our population, but as we only sequenced a subset of positive samples, we grouped these two strains together for further analysis. infection intensity is described elsewhere in more detail, but mean infection intensity in a random sub-sample of birds confirmed as infected through pcr was parasites per erythrocytes. year-specific data summaries for all variables are provided in additional file immunological impacts of blood parasites measures of both chronic stress and immune system activity were influenced by parasite infection status. controlling for lymphocyte numbers, infected birds had 35% lower heterophil counts on average than uninfected birds, resulting in a reduced h:l ratio. similarly, controlling for wbc numbers, infected birds had fewer erythrocytes compared to uninfected birds, resulting in a 60% higher mean standardised wbc count. for significant terms, parameter estimates with se are presented; for non-significant main effects, statistics follow reinsertion of the term into the minimum adequate model and subsequent model comparison. parameter estimates for two level factors are for the stated factor compared to the other factor; estimates for month are for the stated month when compared to april. ‘na’ indicates that this term was not included in the model. morphological associations with parasitism wing length was associated with both an interaction between age and sex, and an interaction between haemoproteus infection status and year. post hoc analyses indicated that in the winter of 2007/ birds infected with haemoproteus had shorter wings than uninfected birds but in the winter of 2008/ this was not the case. when the lowest maximum temperature prior to the sampling date during each winter was substituted into the minimum adequate model in place of year, the model explained the same amount of variation as that containing year, with mean population wing length decreasing as lowest maximum temperature increases. no association with infection status was found for either head-beak length or tarsus length. for significant terms, parameter estimates with se are presented; for non-significant terms, statistics follow reinsertion of the term into the minimum adequate model and subsequent model comparison. survival analysis using the most parsimonious recapture model, survival models were estimated. the ∆qaicc between the top three models was < so we used model averaging to produce parameter estimates. survival was positively affected by wing length and sex, and recapture probability decreased with time, although not linearly. Φ remains as a constant in this model; npar shows the number of parameters; qaicc is the adjusted aic value following correction for overdipersion, and ∆qaicc shows the difference between the specified model and the ‘best’ model. models with a ∆qaicc <  are considered not to differ from the best model. the model with time alone was found to be the best model for predicting the probability of recapture, and thus p remains as a constant in this model; npar shows the number of parameters; qaicc is the adjusted aic value following correction for overdipersion, and ∆qaicc shows the difference between the specified model and the ‘best’ model. models with a ∆qaicc <  are considered not to differ from the best model. discussion understanding the drivers of population dynamics is a major challenge in population biology, particularly when populations are declining and require mitigation strategies to prevent extinction. many european farmland birds have declined following farmland intensification and this has been hypothesised as being due to combinations of loss of habitat, shortages of summer and winter food, or a multiplicity of causes. here we add a further potential cause as we show, for the first time, high parasite prevalence in winter, a season associated with significant mortality. this is coupled with evidence suggestive of immunological challenge and a physiological response that may potentially impact upon survival, and we suggest that declining populations may make good systems within which to examine this previously overlooked period in host-parasite ecology. whilst results here are purely correlative, we discuss the potential implications of our data that warrant further, experimental, work. the high prevalence of infection found in our population suggests either a high incidence of chronic infections, or stress-induced relapse of existing infections. the vectors of blood parasites tend to be dormant during the winter months, considerably reducing the transmission of new infections. for haemoproteus parasites, microscopy and pcr techniques tend to provide similar prevalence estimates, although fallon & ricklefs found 25-35% of pcr-detected haemoproteus infections to be undetected through examination of blood smears. infection intensities within our population are relatively low when compared to other passerine-haemoproteus spp. systems during the summer months, possibly suggesting that our findings represent the chronic stages of infection, rather than relapses. unfortunately infection intensity data from our study species during the breeding season is, to our knowledge, only presented in allander and sundberg but this paper measures parasites per microscope fields and does not standardise measurements by erythrocyte abundance, so we are unable to make direct comparisons, although these data from our population would be valuable in assessing the relative effects of parasitism between the breeding and non-breeding periods. however, as the non-infective asexual stages of haemoproteus reside in the tissues and only infective gametocytes are present in the peripheral circulation, this suggests that our findings represent active infections and has further implications for the over-winter ecology of avian blood parasites in temperate species. haemoproteus infection was associated with both a reduced h:l ratio, and an increased wbc count. the h:l ratio is generally expected to increase in response to infection, whereas our data suggest the opposite. similarly to our data however, other systems have also found a reduction in h:l ratio associated with haemoproteus infection, and galeotti and sacchi suggest that the reduction in h:l ratio is explained by the higher concentration of lymphocytes overall, triggered by an increase in immune system activity. this is demonstrated in our data by the increased wbc count in infected individuals, and suggests a direct immune cost of haemoproteus infection in this species. h:l ratio is also strongly positively correlated with corticosterone levels, but increases with increasing environmental stress, so these data do not support the idea that increased corticosterone, induced by food stress or poor weather, induces relapses of active parasite infection. however, an increase in immune activity also carries costs: for example, in the house sparrow passer domesticus, haemoproteus infection reduces immune response to a second immune challenge. increased immune activity leads to an increased short-term energy consumption which, even at the levels of a 5-15% increase in energy expenditure calculated by hasselquist & nilsson may amplify the impacts of sub-clinical disease at times of food- or weather-related stress, or in populations already under environmental pressure. we found year-dependent associations between parasite infection and reduced feather length, with no such relationship with skeletal measures of size, suggesting that under certain conditions, parasites can influence feather length through competition for host resources during moult, although we acknowledge that this relationship may be mediated by a third, unknown, factor such as body condition during moult. whilst our parasite data are from the winter months, rather than from months when moult was occurring, the presence of parasites during winter suggests that they were also present during the preceding post-breeding moult, as post-breeding tends to be the time when infection rates are highest in other systems. in addition, parasite intensities between peak parasite intensity and chronic infections can be correlated and novel infections between the end of moult and the winter months may be relatively unlikely due to cessation of vector activity, although further work would be required to confirm this. a larger dataset of repeat within-individual data between years would be of great value in elucidating whether this association with wing length occurs at an individual level in relation to infection intensity. the replacement of year with lowest maximum temperature explained a similar amount of variation in the statistical model, suggesting that temperature may underlie the relationship between parasitism, wing length and year. parasite prevalence was higher during the second year of the study, coinciding with fewer birds sampled despite similar sampling effort, suggesting fewer birds in the population. this is unlikely to be due to birds moving out of the study area during the second year, as yellowhammers in the uk show very low dispersal and our population showed a relatively high winter-summer fidelity as estimated through colour-ring re-sightings. instead, this may have been due to an early cold spell during autumn, leading to an increase in energy requirements and consequently food requirements, thus resulting in increased over-winter mortality. given the association between infection and wing length was found only during the first year of sampling when the weather was mild and more birds were caught, and that our survival analysis indicated that birds with longer wings had an enhanced survival probability, it seems plausible that those birds susceptible to physiological effects of parasitism may be more likely to succumb to food stress during a cold winter such as that of the second year of the study and thus be removed from the population. however, this suggestion is speculative and requires further investigation, preferably by inclusion of blood parasite intensity data in the survival analysis. farmland birds more generally are under pressure from reduced nesting habitat availability, reduced quality of available nesting habitat, and reductions in both summer and winter food availability. here, we suggest that parasites may also play a significant role in the ecology of declining populations, potentially by interacting with other environmental stressors. these interactions have the potential to occur both within and outside the breeding season, and we suggest that declining populations, especially those such as ours that remain resident outside the breeding season, would make excellent study systems for the examination of such relationships within and between seasons.  whilst our data are correlative and thus our results are speculative in terms of causality, we show associations between parasite infection and immune function, and between parasite infection and a physiological trait that we show to be of ecological significance. our data suggest that the impacts of parasites outside the breeding season may be more important than previously thought, especially in species already under stress due to other ecological factors, such as food stress. consequently, we also suggest that future experimental research on the ecological impacts of parasitism should examine potential impacts outside the breeding season, and should focus on populations already under pressure due to other ecological factors where these effects are likely to be more pronounced. our results further suggest that considering sub-clinical disease may be critical when examining the conservation of declining populations. 
infected birds had shorter wings during the first winter of sampling but not during the second, colder, winter; survival analysis of birds sampled across four winters indicated that increased wing length conferred a survival advantage. we suggest that the potential impacts of blood parasite infections on over-wintering birds may have been underestimated. further research should consider the potential impacts of sub-clinical parasite infections on the dynamics of vulnerable populations, and we suggest using declining populations as model systems within which to investigate these relationships as well as examining interactions between sub-clinical disease and other environmental stressors. we investigated the potential for blood parasites to impact upon their hosts at the immunological, physiological and population level during the non-breeding season using a declining population of yellowhammers emberiza citrinella as a model. pathogens and parasites can have major impacts on host population dynamics, both through direct mortality and via indirect effects. sub-clinical diseaseparasite ecologyfarmland birdsdeclining populationsemberiza citrinellayellowhammerhaemoproteus
 pathogens and parasites can have major impacts on host population dynamics, both through direct mortality and via indirect effects. both types of effect may be stronger in species whose populations are already under pressure. we investigated the potential for blood parasites to impact upon their hosts at the immunological, physiological and population level during the non-breeding season using a declining population of yellowhammers emberiza citrinella as a model.  yellowhammers infected by haemoproteus spp. showed both a reduced heterophil to lymphocyte ratio, and an elevated standardised white blood cell count compared to uninfected birds, indicating an immunological response to infection. infected birds had shorter wings during the first winter of sampling but not during the second, colder, winter; survival analysis of birds sampled across four winters indicated that increased wing length conferred a survival advantage.  we suggest that the potential impacts of blood parasite infections on over-wintering birds may have been underestimated. further research should consider the potential impacts of sub-clinical parasite infections on the dynamics of vulnerable populations, and we suggest using declining populations as model systems within which to investigate these relationships as well as examining interactions between sub-clinical disease and other environmental stressors. jel code q5 sub-clinical diseaseparasite ecologyfarmland birdsdeclining populationsemberiza citrinellayellowhammerhaemoproteus 