Sarah Burthe

Phenological sensitivity to climate across taxa and trophic levels

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5–2.9 days earlier on average), with substantial taxonomic variation (1.1–14.8 days earlier on average).

Host–pathogen time series data in wildlife support a transmission function between density and frequency dependence

A key aim in epidemiology is to understand how pathogens spread within their host populations. Central to this is an elucidation of a pathogens transmission dynamics. Mathematical models have generally assumed that either contact rate between hosts is linearly related to host density (density-dependent) or that contact rate is independent of density (frequency-dependent), but attempts to confirm either these or alternative transmission functions have been rare. Here, we fit infection equations to 6 years of data on cowpox virus infection (a zoonotic pathogen) for 4 natural populations to investigate which of these transmission functions is best supported by the data. We utilize a simple reformulation of the traditional transmission equations that greatly aids the estimation of the relationship between density and host contact rate. Our results provide support for an infection rate that is a saturating function of host density. Moreover, we find strong support for seasonality in both the transmission coefficient and the relationship between host contact rate and host density, probably reflecting seasonal variations in social behavior and/or host susceptibility to infection. We find, too, that the identification of an appropriate loss term is a key component in inferring the transmission mechanism. Our study illustrates how time series data of the host–pathogen dynamics, especially of the number of susceptible individuals, can greatly facilitate the fitting of mechanistic disease models.

Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics

Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.

Seasonal host dynamics drive the timing of recurrent epidemics in a wildlife population

The seasonality of recurrent epidemics has been largely neglected, especially where patterns are not driven by forces external to the population. Here, we use data on cowpox virus in field voles to explore the seasonal patterns in wildlife (variable abundance) populations and compare these with patterns previously found in humans. Timing in our system was associated with both the number and the rate of recruitment of susceptible hosts. A plentiful and sustained supply of susceptible hosts throughout the summer gave rise to a steady rise in infected hosts and a late peak. A meagre supply more limited in time was often insufficient to sustain an increase in infected hosts, leading to an early peak followed by a decline. These seasonal patterns differed from those found in humans, but the underlying association found between the timing and the supply of susceptible hosts was similar to that in humans. We also combine our data with a model to explore these differences between humans and wildlife. Model results emphasize the importance of the interplay between seasonal infection and recruitment and suggest that our empirical patterns have a relevance extending beyond our own system.

Tuberculosis (Mycobacterium microti) in wild field vole populations

Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5.2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10.78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13.15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.

Do early warning indicators consistently predict nonlinear change in long‐term ecological data?

1. Anthropogenic pressures, including climate change, are causing nonlinear changes in ecosystems globally. The development of reliable early warning indicators (EWIs) to predict these changes is vital for the adaptive management of ecosystems and the protection of biodiversity, natural capital and ecosystem services. Increased variance and autocorrelation are potential early warning indicators and can be readily estimated from ecological time series. Here, we undertook a comprehensive test of the consistency between early warning indicators and nonlinear abundance change across species, trophic levels and ecosystem types. 2. We tested whether long-term abundance time series of 55 taxa (126 data sets) across multiple trophic levels in marine and freshwater ecosystems showed (i) significant nonlinear change in abundance ‘turning points’ and (ii) significant increases in variance and autocorrelation (‘early warning indicators’). For each data set, we then quantified the prevalence of three cases: true positives (early warning indicators and associated turning point), false negatives (turning point but no associated early warning indicators) and false positives (early warning indicators but no turning point). 3. True positives were rare, representing only 9% (16 of 170) of cases using variance, and 13% (19 of 152) of cases using autocorrelation. False positives were more prevalent than false negatives (53% vs. 38% for variance; 47% vs. 40% for autocorrelation). False results were found in every decade and across all trophic levels and ecosystems. 4. Time series that contained true positives were uncommon (8% for variance; 6% for autocorrelation), with all but one time series also containing false classifications. Coherence between the types of early warning indicators was generally low with 43% of time series categorized differently based on variance compared to autocorrelation. 5. Synthesis and applications. Conservation management requires effective early warnings of ecosystem change using readily available data, and variance and autocorrelation in abundance data have been suggested as candidates. However, our study shows that they consistently fail to predict nonlinear change. For early warning indicators to be effective tools for preventative management of ecosystem change, we recommend that multivariate approaches of a suite of potential indicators are adopted, incorporating analyses of anthropogenic drivers and process-based understanding.

Trypanosomes, fleas and field voles : ecological dynamics of a host-vector-parasite interaction

To investigate the prevalence of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in its field vole (Microtus agrestis) host, we monitored over a 2-year period a range of intrinsic and extrinsic parameters pertaining to host demographics, infection status and vector (flea) prevalence. Generalized Linear Mixed Modelling was used to analyse patterns of both flea and trypanosome occurrence. Overall, males of all sizes and ages were more likely to be infested with fleas than their female counterparts. Flea prevalence also showed direct density dependence during the winter, but patterns of density dependence varied amongst body mass (age) classes during the summer. Trypanosome prevalence did not vary between the sexes but was positively related to past flea prevalence with a lag of 3 months, with the highest levels occurring during the autumn season. A convex age-prevalence distribution was observed, suggesting that individuals develop a degree of immunity to trypanosome infection with age and exposure. An interaction between age and whether the individual was new or recaptured suggested that infected animals are less likely to become territory holders than their uninfected counterparts.

Longitudinal bio‐logging reveals interplay between extrinsic and intrinsic carry‐over effects in a long‐lived vertebrate

Carry-over effects have major implications for individual fitness and population and evolutionary dynamics. The strength of these effects is dependent on an individuals intrinsic performance and the environmental conditions it experiences. However, understanding the relative importance of environmental and intrinsic effects underpinning seasonal interactions has proved extremely challenging, since they covary. A powerful approach is longitudinal measurement of individuals across a range of conditions, whereby each animal is effectively acting as its own control. We related time spent foraging during the nonbreeding period to subsequent breeding performance in European Shags Phalacrocorax aristotelis. By following individuals for up to six years, we could test simultaneously for extrinsic and intrinsic effects using random regression modeling. We detected significant annual and among-individual variation in daily foraging time during the late winter, and clear variation among individuals in the quadratic relationship between foraging time and date. Shorter foraging times were associated with earlier and more successful breeding, driven by differences among years and individuals, with no evidence of individual variation in the slope of these relationships. That both environmental and intrinsic variation shape carry-over effects has important implications for population responses to environmental change.

Demographic consequences of increased winter births in a large aseasonally breeding mammal (Bos taurus) in response to climate change

1. Studies examining changes in the scheduling of breeding in response to climate change have focused on species with well-defined breeding seasons. Species exhibiting year-round breeding have received little attention and the magnitudes of any responses are unknown. 2. We investigated phenological data for an enclosed feral population of cattle (Bos taurus L.) in northern England exhibiting year-round breeding. This population is relatively free of human interference. 3. We assessed whether the timing of births had changed over the last 60 years, in response to increasing winter and spring temperatures, changes in herd density, and a regime of lime fertilisation. 4. Median birth date became earlier by 1·0 days per year. Analyses of the seasonal distribution of calving dates showed that significantly fewer calves were born in summer (decline from 44% of total births to 20%) and significantly more in winter (increase from 12% to 30%) over the study period. The most pronounced changes occurred in winter, with significant increases in both the proportion and number of births. Winter births arise from conceptions in the previous spring, and we considered models that investigated climate and weather variables associated with the winter preceding and the spring of conceptions. 5. The proportion of winter births was higher when the onset of the plant growing season was earlier during the spring of conceptions. This relationship was much weaker during years when the site had been fertilised with lime, suggesting that increased forage biomass was over-riding the impacts of changing plant phenology. When the onset of the growing season was late, winter births increased with female density. 6. Recruitment estimates from a stage-structured state-space population model were significantly negatively correlated with the proportion of births in the preceding winter, suggesting that calves born in winter are less likely to survive than those born in other seasons. 7. This is one of the first studies to document changes in the phenology of a year-round breeder, suggesting that the impact of climate on the scheduling of biological events may be more extensive than previously thought and that impacts may be negative, even for species with relatively flexible breeding strategies.

Contrasting responses of male and female foraging effort to year‐round wind conditions

Summary There is growing interest in the effects of wind on wild animals, given evidence that wind speeds are increasing and becoming more variable in some regions, particularly at temperate latitudes. Wind may alter movement patterns or foraging ability, with consequences for energy budgets and, ultimately, demographic rates. These effects are expected to vary among individuals due to intrinsic factors such as sex, age or feeding proficiency. Furthermore, this variation is predicted to become more marked as wind conditions deteriorate, which may have profound consequences for population dynamics as the climate changes. However, the interaction between wind and intrinsic effects has not been comprehensively tested. In many species, in particular those showing sexual size dimorphism, males and females vary in foraging performance. Here, we undertook year‐round deployments of data loggers to test for interactions between sex and wind speed and direction on foraging effort in adult European shags Phalacrocorax aristotelis, a pursuit‐diving seabird in which males are c. 18% heavier. We found that foraging time was lower at high wind speeds but higher during easterly (onshore) winds. Furthermore, there was an interaction between sex and wind conditions on foraging effort, such that females foraged for longer than males when winds were of greater strength (9% difference at high wind speeds vs. 1% at low wind speeds) and when winds were easterly compared with westerly (7% and 4% difference, respectively). The results supported our prediction that sex‐specific differences in foraging effort would become more marked as wind conditions worsen. Since foraging time is linked to demographic rates in this species, our findings are likely to have important consequences for population dynamics by amplifying sex‐specific differences in survival rates.