Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle

A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in free-living organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.     

Seasonal differences in energy expenditure,flight characteristics and spatial utilization of Dalmatian Pelicans Pelecanus crispus in Greece

Animals typically adjust their behaviour to their changing environment throughout the annual cycle, modulating key processes such as the timing of breeding and the onset of migration. Such behavioural changes are commonly manifested in the movements and the energetic balance of individuals in relation to their species‐specific physiological characteristics, habitat attributes and the environmental properties of their distribution ranges. We used GPS and acceleration data collected using transmitters on free‐ranging birds to quantify annual movement patterns and estimate energy expenditure of the Dalmatian Pelican Pelecanus crispus, a large, soaring avian species which performs short‐distance migration and spends its entire annual cycle in mid‐latitudes. To assess the representativeness of our results, the transmitter effect was also tested. We found that daily trends in the overall dynamic body acceleration (ODBA; a proxy for energy expenditure) differed among seasons, with the highest values occurring during spring and the lowest during winter. Long inter‐lake flights were very rare in winter, and the number of flights and ODBA during spring was higher than during summer, suggesting greater motivation to move in spring. Although transmitters may have affected the birds, as none of the tagged birds bred, we found seasonal differences in behaviour and activity level. The observed patterns in differences in activity levels, long‐distance flights and flight characteristics between seasons suggest an annual rhythm of energy expenditure. These findings allow a better understanding of bird phenology, specifically regarding adaptations to wintering in a cold climate by reducing movement‐driven energy expenditure. Finally, the identification of periods with high and low energy expenditure may guide future conservation efforts by adjusting conservation plans in accordance with changing needs during the annual cycle.     

Changes in ovarian morphology and hormone concentrations associated with reproductive seasonality in wild large Japanese field mice (Apodemus speciosus)

Wild large Japanese field mice (Apodemus speciosus) responses to cyclic seasonal changes are associated with physiological and behavioral changes. However, the detailed regulation of oogenesis in the ovary during the seasonal reproductive cycle in wild large Japanese field mice has not been studied. We assessed the dynamics and changes in ovarian morphology and hormone concentrations associated with reproductive seasonality throughout the year. The stages of the ovarian morphological breeding cycle of wild large Japanese field mice were classified as breeding, transition, and non-breeding periods during the annual reproductive cycle. Measurement of blood estradiol concentrations throughout the year showed that the levels in September and October were higher than those in other months. It is presumed that follicle development starts from a blood estradiol concentration of 38.4 ± 27.1 pg/mL, which marks a shift from the transitional season to the breeding season, followed by the transition to the non-breeding season at 26.1 ± 11.6 pg/mL. These results suggest that seasonal follicle development in wild rodents is correlated with estradiol regulation. We consider this species to be an alternative animal model for studying seasonal reproductive changes and the effects of environmental changes.     

Local and regional weather patterns influencing post‐breeding migration counts of soaring birds at the Strait of Gibraltar,Spain

Migration is a significant event in the annual cycle of many avian species. During migration birds face many challenges, including unfamiliar foraging and refuge habitats, resulting in a much higher rate of mortality during migration than during other seasons of the year. Weather may significantly affect a bird's decision to initiate migration, the course and pace of migration, and its survival during migration. Each of these influences may impact the counts of migrating birds at geographical convergence zones or bottlenecks. It is important to quantify the effect of short‐term weather on these counts to appropriately interpret and use such counts in other analyses. To this end, we aim to assess the effects of local and regional weather conditions on the migration counts of soaring birds at the Strait of Gibraltar during post‐breeding migration. We used information‐theoretic approaches to analyse the influence of local weather and weather in northern Spain on the migration counts of five soaring bird species from two count sites near the Strait of Gibraltar. Migration counts were higher on days with local northerly and westerly winds, often following a day of easterly winds, on days with local high pressure systems, and often following a day of lower pressure. Weather conditions in northern Spain influenced migration counts at the Strait of Gibraltar, but the effects were much weaker than local weather conditions. We confirm that short‐term weather conditions, locally and regionally, can influence migration counts and should thus be considered when these counts are used in other analyses.     

Celestial moderation of tropical seabird behavior

Most animals, including birds, have cyclic life histories and numerous studies generally conducted on captive animals have shown that photoperiod is the main factor influencing this periodicity. Moon cycles can also affect periodic behavior of birds. Few studies have investigated the influence of these environmental cues in natural settings, and particularly in tropical areas where the change in photoperiod is slight and some bird species keep cyclic behaviors. Using miniaturized light sensors, we simultaneously investigated under natural conditions the influence of photoperiod and moon phases on the migration dates and at-sea activity of a tropical seabird species, the Barau's petrel, throughout its annual cycle. Firstly, we found that birds consistently started their pre- and post-breeding migrations at precise dates corresponding in both cases to a day-duration of 12.5 hours, suggesting a strong influence of the photoperiod in the regulation of migration behavior. We also found that mean population arrival dates to the colony changed from year to year and they were influenced by moon phases. Returns at their colonies occurred around the last full moon of the austral winter, suggesting that moon cycle is used by birds to synchronize their arrival. Secondly, variations of day-time activity were sinusoidal and correlated to seasonal changes of daylength. We thus hypothesize that the photoperiod could directly affect the behavior of the birds at sea. Night-time at-sea activity exhibited a clear cycle of 29.2 days, suggesting that nocturnal foraging was highly regulated by moon phase, particularly during the non-breeding season. To our knowledge, this is the first study to document a mixed regulation of the behavior of a wild bird by photoperiod and moon phases throughout its annual cycle.     

Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years

A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks?? annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost?Cbenefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.     

Anthropogenic food provisioning and immune phenotype: Association among supplemental food,body condition,and immunological parameters in urban environments

Direct or indirect supplemental feeding of free‐ranging animals occurs worldwide, resulting in significant impacts on population density or altered demographic processes. Another potential impact of increased energy intake from supplemental feeding is altered immunocompetence. As immune system maintenance is energetically costly, there may be trade‐offs between immune responses and other energy‐demanding physiological processes in individual animals. Although increased availability of food sources through supplemental feeding is expected to increase the overall immunocompetence of animals, empirical data verifying the association between supplemental feeding and different immune parameters are lacking. Understanding the potential influence of supplemental feeding on immune phenotypes is critical, as it may also impact host–pathogen dynamics in free‐ranging animals. Using urban stray cats as a study model, we tested for associations between the intensity of supplemental feeding due to cat caretaker activity (CCA); body condition; and immune phenotype (bacterial killing assay (BKA), immunoglobulin G (IgG) concentration, and leukocyte counts). Significantly higher bacterial killing ability was observed in cats from high CCA districts, whereas higher IgG concentration and eosinophil counts were observed in cats from low CCA districts. Other leukocyte counts and body condition indices showed no significant association with CCA. We observed varying patterns of different immune components in relation to supplemental feeding. Out data suggest that supplemental feeding influences immune phenotype, not only by means of energy provisioning, but also by potentially reducing exposure rates to parasite infections through stray cat behavioral changes.     

Do the high energy lifestyles of shorebirds result in high maximal metabolic rates? Basal and maximal metabolic rates in least and pectoral sandpipers during migration

Shorebirds have high resting and field metabolic rates relative to many other bird groups, and this is posited to be related to their high‐energy lifestyle. Maximum metabolic outputs for cold or exercise are also often high for bird groups with energetically demanding lifestyles. Moreover, shorebirds demonstrate flexible basal and maximal metabolic rates, which vary with changing energy demands throughout the annual cycle. Consequently, shorebirds might be expected to have high maximum metabolic rates, especially during migration periods. We captured least Calidris minutilla and pectoral C. melanotos sandpipers during spring and fall migration in southeastern South Dakota and measured maximal exercise metabolic rate (MMR; least sandpipers only), summit metabolic rate (M_sum, maximal cold‐induced metabolic rate) and basal metabolic rate (BMR, minimum maintenance metabolic rate) with open‐circuit respirometry. BMR for both least and pectoral sandpipers exceeded allometric predictions by 3–14%, similar to other shorebirds, but M_sum and MMR for both species were either similar to or lower than allometric predictions, suggesting that the elevated BMR in shorebirds does not extend to maximal metabolic capacities. Old World shorebirds show the highest BMR during the annual cycle on the Arctic breeding grounds. Similarly, least sandpiper BMR during migration was lower than on the Arctic breeding grounds, but this was not the case for pectoral sandpipers, so our data only partially support the idea of similar seasonal patterns of BMR variation in New World and Old World shorebirds. We found no correlations of BMR with either M_sum or MMR for either raw or mass‐independent data, suggesting that basal and maximum aerobic metabolic rates are modulated independently in these species.     

The strength of migratory connectivity for birds en route to breeding through the Gulf of Mexico

The strength of migratory connectivity is a measure of the cohesion of populations among phases of the annual cycle, including breeding, migration, and wintering. Many Nearctic‐Neotropical species have strong migratory connectivity between breeding and wintering phases of the annual cycle. It is less clear if this strength persists during migration when multiple endogenous and exogenous factors may decrease the cohesion of populations among routes or through time along the same routes. We sampled three bird species, American redstart Setophaga ruticilla, ovenbird Seiurus aurocapilla, and wood thrush Hylocichla mustelina, during spring migration through the Gulf of Mexico region to test if breeding populations differentiate spatially among migration routes or temporally along the same migration routes and the extent to which within‐population timing is a function of sex, age, and carry‐over from winter habitat, as measured by stable carbon isotope values in claws (δ¹³C). To make quantitative comparisons of migratory connectivity possible, we developed and used new methodology to estimate the strength of migratory connectivity (MC) from probabilistic origin assignments identified using stable hydrogen isotopes in feathers (δ²H). We found support for spatial differentiation among routes by American redstarts and ovenbirds and temporal differentiation along routes by American redstarts. After controlling for breeding origin, the timing of American redstart migration differed among ages and sexes and ovenbird migration timing was influenced by carry‐over from winter habitat. The strength of migratory connectivity did not differ among the three species, with each showing weak breeding‐to‐spring migration MC relative to prior assessments of breeding‐wintering connectivity. Our work begins to fill an essential gap in methodology and understanding of the extent to which populations remain together during migration, information critical for a full annual cycle perspective on the population dynamics and conservation of migratory animals.     

Seasonal dynamics in community structure,abundance, body size and sex ratio in two species of Neotropical annual fishes

Seven ephemeral pools on the coastal plain of southern Brazil were found to be inhabited by three annual and 22 non‐annual fish species. Two common annual species (Austrolebias minuano and Cynopoecilus fulgens) exhibited clear seasonal dynamics, with the appearance of young fishes in the austral autumn (May to June) and a decline in abundance over the seasonal cycle. The third annual species, Austrolebias wolterstorffii, was rare. No seasonal dynamics were observed in non‐annual fishes. The relative abundance of non‐annual fishes compared with annual fishes increased over the seasonal cycle, but they coexisted widely. The size structure of annual fishes suggested the presence of a single age cohort in most pools though a second age cohort was registered in one pool in August, coinciding with a large flooding. Strong sexual dimorphism in body size was found in C. fulgens throughout the seasonal cycle, while no sexual dimorphism in body size was found in A. minuano. Female‐biased sex ratios were recorded in both common annual fish species in the last three sampling dates (in spring), but not during the first two sampling dates (in winter). The natural lifespan of annual fishes was <8 months. Annual fishes disappeared before habitat desiccation in half of the pools, while non‐annual fishes were still present.     

Seasonal changes in immune response and parasite impact on hosts

Seasonal changes in the impact of parasites on hosts should result in seasonal changes in immune function. Since both ectoparasites and endoparasites time their reproduction to that of their hosts, we can predict that hosts have been selected to show an annual peak in their ability to raise an immune response during the reproductive season. We found large seasonal changes in immune function between the breeding and the nonbreeding season for a sample of temperate bird species. These changes amounted to a decrease in spleen mass from the breeding to the nonbreeding season by on average 18% across 71 species and a seasonal decrease in T-cell-mediated immunity by on average 33% across 13 species. These seasonal changes in immune function differed significantly among species. The condition dependence of immune function also differed between the breeding and the nonbreeding season, with individuals in prime condition particularly having greater immune responses during breeding. Analyses of ecological factors associated with interspecific differences in seasonal change of immune function revealed that hole-nesting species had a larger increase in immune function during the breeding season than did open nesters. Since hole nesters suffer greater reduction in breeding success because of virulent parasites than do open nesters, this seasonal change in immune function is suggested to have arisen as a response to the increased virulence of parasites attacking hole-nesting birds.     

Global change and the distributional dynamics of migratory bird populations wintering in Central America

Understanding the susceptibility of highly mobile taxa such as migratory birds to global change requires information on geographic patterns of occurrence across the annual cycle. Neotropical migrants that breed in North America and winter in Central America occur in high concentrations on their non‐breeding grounds where they spend the majority of the year and where habitat loss has been associated with population declines. Here, we use eBird data to model weekly patterns of abundance and occurrence for 21 forest passerine species that winter in Central America. We estimate species’ distributional dynamics across the annual cycle, which we use to determine how species are currently associated with public protected areas and projected changes in climate and land‐use. The effects of global change on the non‐breeding grounds is characterized by decreasing precipitation, especially during the summer, and the conversion of forest to cropland, grassland, or peri‐urban. The effects of global change on the breeding grounds are characterized by increasing winter precipitation, higher temperatures, and the conversion of forest to peri‐urban. During spring and autumn migration, species are projected to encounter higher temperatures, forests that have been converted to peri‐urban, and increased precipitation during spring migration. Based on current distributional dynamics, susceptibility to global change is characterized by the loss of forested habitats on the non‐breeding grounds, warming temperatures during migration and on the breeding grounds, and declining summer rainfall on the non‐breeding grounds. Public protected areas with low and medium protection status are more prevalent on the non‐breeding grounds, suggesting that management opportunities currently exist to mitigate near‐term non‐breeding habitat losses. These efforts would affect more individuals of more species during a longer period of the annual cycle, which may create additional opportunities for species to respond to changes in habitat or phenology that are likely to develop under climate change.     

Is there a connection between weather at departure sites,onset of migration and timing of soaring‐bird autumn migration in Israel?

Aims Different aspects of soaring‐bird migration are influenced by weather. However, the relationship between weather and the onset of soaring‐bird migration, particularly in autumn, is not clear. Although long‐term migration counts are often unavailable near the breeding areas of many soaring birds in the western Palaearctic, soaring‐bird migration has been systematically monitored in Israel, a region where populations from large geographical areas converge. This study tests several fundamental hypotheses regarding the onset of migration and explores the connection between weather, migration onset and arrival at a distant site. Location Globally gridded meteorological data from the breeding areas in north‐eastern Europe were used as predictive variables in relation to the arrival of soaring migrants in Israel. Methods Inverse modelling was used to study the temporal and spatial influence of weather on initiation of migration based on autumn soaring‐bird migration counts in Israel. Numerous combinations of migration duration and temporal influence of meteorological variables (temperature, sea‐level pressure and precipitable water) were tested with different models for meteorological sensitivity. Results The day of arrival in Israel of white storks, honey buzzards, Levant sparrowhawks and lesser spotted eagles was significantly and strongly related to meteorological conditions in the breeding area days or even weeks before arrival in Israel. The cumulative number of days or cumulative value above or below a meteorological threshold performed significantly better than other models tested. Models provided reliable estimates of migration duration for each species. Main conclusions The meteorological triggers of migration at the breeding grounds differed between species and were related to deteriorating living conditions and deteriorating migratory flight conditions. Soaring birds are sensitive to meteorological triggers at the same period every year and their temporal response to weather appears to be constrained by their annual routine.     

Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime

Throughout the annual cycle, demands on competing physiological systems change, and animals must allocate resources to maximize fitness. Immune function is one such system and is important for survival. Yet detailed empirical data tracking immune function over the entire annual cycle are lacking for most wild animals. We measured constitutive immune indices once a month for a year on captive red knots (Calidris canutus). We also examined temperature as an environmental contributor to immune variation by manipulating ambient temperature to vary energy expenditure. To identify relationships among immune indices, we performed principal-component analysis. We found significant repeatability in immune indices over the annual cycle and covariation of immune indices within and among individuals. This covariation suggests immune strategies as individual traits among individuals and the use of different immune strategies during different annual-cycle stages within individuals. Over the annual cycle, both higher-cost phagocyte-based immunity and lower-cost lymphocyte-based immunity were high during mass change, but there was a clear shift toward lower-cost lymphocyte-based immunity during peak molt. Experimental manipulation of temperature had little effect on annual variation in immune function. This suggests that other environmental factors, such as food availability and disease, should also be examined in the future.     

An integrated population model sheds light on the complex population dynamics of a unique colonial breeder

Climate models forecast increasing climatic variation and more extreme events, which could increase the variability in animal demographic rates. More variable demographic rates generally lead to lower population growth and can be detrimental to wild populations, especially if the particular demographic rates affected are those to which population growth is most sensitive. We investigated the population dynamics of a metapopulation of 25 colonies of a semi-arid bird species, the sociable weaver Philetairus socius, and how it was influenced by seasonal weather during 1993–2014. We constructed an integrated population model which estimated population sizes similar to observed population counts, and allowed us to estimate annual fecundity and recruitment. Variance in fecundity contributed most to variance in population growth, which showed no trend over time. No weather variables explained overall demographic variation at the population level. However, a separate analysis of the largest colony showed a clear decline with a high extinction probability (0.05 to 0.33) within 5 years after the study period. In this colony, juvenile survival was lower when summers were hot, and adult survival was lower when winters were cold. Rainfall was also negatively correlated with adult survival. These weather effects could be due to increased physiological demands of thermoregulation and rainfall-induced breeding activity. Our results suggest that the dynamics of the population on the whole are buffered against current weather variation, as individual colonies apparently react in different ways. However, if more and increasingly extreme weather events synchronize colony dynamics, they are likely to have negative effects.     

The trans‐equatorial loop migration system of Eleonora’s falcon: differences in migration patterns between age classes,regions and seasons

Internal factors such as experience (e.g. age) and motivation for breeding, and external ones such as environmental conditions (e.g. meteorology and landscape characteristics) can promote differences in migratory behaviour and routes among seasons, regions and populations. Using satellite telemetry we investigated whether such differences occur and which factors promote them among migrating Eleonora’s falcons breeding in the Mediterranean area (Spain and Croatia) and wintering in Madagascar. We found that during autumn migration no age differences occur when crossing the Sahara desert, but in the remaining African regions, juveniles were more prone than adults to fly at a slower and more tortuous rate, as well as exhibiting longer stop‐overs, particularly in the Sahel region. Such differences might be promoted by a lower foraging and pre‐migratory fattening efficiency in juveniles. During spring, routes were significantly more eastern than during autumn, resulting in a loop migration occurring in all studied populations. This could be accounted by seasonal variation in the distribution of trophic resources. Our results show that Eleonora’s falcons integrate spatially seasonal changing resources on a continental scale throughout their annual cycle, changing their movement patterns in response to internal (age) and external (habitat) factors. This loop migration pattern may prove to be widespread among other Palearctic trans‐continental migratory bird species.     

Local and cross‐seasonal associations of climate and land use with abundance of monarch butterflies Danaus plexippus

Quantifying how climate and land use factors drive population dynamics at regional scales is complex because it depends on the extent of spatial and temporal synchrony among local populations, and the integration of population processes throughout a species’ annual cycle. We modeled weekly, site‐specific summer abundance (1994–2013) of monarch butterflies Danaus plexippus at sites across Illinois, USA to assess relative associations of monarch abundance with climate and land use variables during the winter, spring, and summer stages of their annual cycle. We developed negative binomial regression models to estimate monarch abundance during recruitment in Illinois as a function of local climate, site‐specific crop cover, and county‐level herbicide (glyphosate) application. We also incorporated cross‐seasonal covariates, including annual abundance of wintering monarchs in Mexico and climate conditions during spring migration and breeding in Texas, USA. We provide the first empirical evidence of a negative association between county‐level glyphosate application and local abundance of adult monarchs, particularly in areas of concentrated agriculture. However, this association was only evident during the initial years of the adoption of herbicide‐resistant crops (1994–2003). We also found that wetter and, to a lesser degree, cooler springs in Texas were associated with higher summer abundances in Illinois, as were relatively cool local summer temperatures in Illinois. Site‐specific abundance of monarchs averaged approximately one fewer per site from 2004–2013 than during the previous decade, suggesting a recent decline in local abundance of monarch butterflies on their summer breeding grounds in Illinois. Our results demonstrate that seasonal climate and land use are associated with trends in adult monarch abundance, and our approach highlights the value of considering fine‐resolution temporal fluctuations in population‐level responses to environmental conditions when inferring the dynamics of migratory species.