Density dependence in a recovering osprey population: demographic and behavioural processes

1. Understanding how density-dependent and independent processes influence demographic parameters, and hence regulate population size, is fundamental within population ecology. We investigated density dependence in growth rate and fecundity in a recovering population of a semicolonial raptor, the osprey Pandion haliaetus [Linnaeus, 1758], using 31 years of count and demographic data in Corsica. 2. The study population increased from three pairs in 1974 to an average of 22 pairs in the late 1990s, with two distinct phases during the recovery (increase followed by stability) and contrasted trends in breeding parameters in each phase. 3. We show density dependence in population growth rate in the second phase, indicating that the stabilized population was regulated. We also show density dependence in productivity (fledging success between years and hatching success within years). 4. Using long-term data on behavioural interactions at nest sites, and on diet and fish provisioning rate, we evaluated two possible mechanisms of density dependence in productivity, food depletion and behavioural interference. 5. As density increased, both provisioning rate and the size of prey increased, contrary to predictions of a food-depletion mechanism. In the time series, a reduction in fledging success coincided with an increase in the number of non-breeders. Hatching success decreased with increasing local density and frequency of interactions with conspecifics, suggesting that behavioural interference was influencing hatching success. 6. Our study shows that, taking into account the role of non-breeders, in particular in species or populations where there are many floaters and where competition for nest sites is intense, can improve our understanding of density-dependent processes and help conservation actions.     

Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co‐occurring host species

Understanding the ecology and evolution of parasites is contingent on identifying the selection pressures they face across their infection landscape. Such a task is made challenging by the fact that these pressures will likely vary across time and space, as a result of seasonal and geographical differences in host susceptibility or transmission opportunities. Avian haemosporidian blood parasites are capable of infecting multiple co‐occurring hosts within their ranges, yet whether their distribution across time and space varies similarly in their different host species remains unclear. Here, we applied a new PCR method to detect avian haemosporidia (genera Haemoproteus, Leucocytozoon, and Plasmodium) and to determine parasite prevalence in two closely related and co‐occurring host species, blue tits (Cyanistes caeruleus, N = 529) and great tits (Parus major, N = 443). Our samples were collected between autumn and spring, along an elevational gradient in the French Pyrenees and over a three‐year period. Most parasites were found to infect both host species, and while these generalist parasites displayed similar elevational patterns of prevalence in the two host species, this was not always the case for seasonal prevalence patterns. For example, Leucocytozoon group A parasites showed inverse seasonal prevalence when comparing between the two host species, being highest in winter and spring in blue tits but higher in autumn in great tits. While Plasmodium relictum prevalence was overall lower in spring relative to winter or autumn in both species, spring prevalence was also lower in blue tits than in great tits. Together, these results reveal how generalist parasites can exhibit host‐specific epidemiology, which is likely to complicate predictions of host–parasite co‐evolution.     

The role of immigration and local adaptation on fine‐scale genotypic and phenotypic population divergence in a less mobile passerine

Dispersal and local patterns of adaptation play a major role on the ecological and evolutionary trajectory of natural populations. In this study, we employ a combination of genetic (25 microsatellite markers) and field‐based information (seven study years) to analyse the impact of immigration and local patterns of adaptation in two nearby (< 7 km) blue tit (Cyanistes caeruleus) populations. We used genetic assignment analyses to identify immigrant individuals and found that dispersal rate is female‐biased (72%). Data on lifetime reproductive success indicated that immigrant females produced fewer local recruits than their philopatric counterparts whereas immigrant males recruited more offspring than those that remained in their natal location. In spite of the considerably higher immigration rates of females, our results indicate that, in absolute terms, their demographic and genetic impact in the receiving populations is lower than that in immigrant males. Immigrants often brought novel alleles into the studied populations and a high proportion of them were transmitted to their recruits, indicating that the genetic impact of immigrants is not ephemeral. Although only a few kilometres apart, the two study populations were genetically differentiated and showed strong divergence in different phenotypic and life‐history traits. An almost absent inter‐population dispersal, together with the fact that both populations receive immigrants from different source populations, is probably the main cause of the observed pattern of genetic differentiation. However, phenotypic differentiation (P_ST) for all the studied traits greatly exceeded neutral genetic differentiation (F_ST), indicating that divergent natural selection is the prevailing factor determining the evolutionary trajectory of these populations. Our study highlights the importance of integrating individual‐ and population‐based approaches to obtain a comprehensive view about the role of dispersal and natural selection on structuring the genotypic and phenotypic characteristics of natural populations.     

The relevance of food peak architecture in trophic interactions

Phenological shifts and associated changes in the temporal match between trophic levels have been a major focus of the study of ecological consequences of climate change. Previously, the food peak has been thought to respond as an entity to warming temperatures. However, food peak architecture, that is, timings and abundances of prey species and the level of synchrony between them, determines the timing and shape of the food peak. We demonstrate this with a case example of three passerine prey species and their predator. We explored temporal trends in the timing, height, width, and peakedness of prey availabilities and explained their variation with food peak architecture and ambient temperatures of prebreeding and breeding seasons. We found a temporal match between the predator's breeding schedule and food availability. Temporal trends in the timing of the food peak or in the synchrony between the prey species were not found. However, the food peak has become wider and more peaked over time. With more peaked food availabilities, predator's breeding success will depend more on the temporal match between its breeding schedule and the food peak, ultimately affecting the timing of breeding in the predator population. The height and width of the food peak depended on the abundances and breeding season lengths of individual prey species and their reciprocal synchronies. Peakednesses of separate prey species' availability distributions alone explained the peakedness of the food peak. Timing and quantity of food production were associated with temperatures of various time periods with variable relevance in different prey species. Alternating abundances of early and late breeding prey species caused high annual fluctuation in the timing of the food peak. Interestingly, the food peak may become later even when prey species' schedules are advanced. Climate warming can thus produce unexpected changes in the food availabilities, intervening in trophic interactions.     

Five species of passerine bird differ in their ability to detect Batesian mimics

Multiple predators affect the evolution of aposematic signals in nature and these predators may substantially differ in terms of ecological and cognitive parameters. However, most experimental studies testing the evolution of Batesian mimics use only a single species of predator (usually the great tit or a domestic chick). Therefore, in the present study, we experimentally tested the responses of five passerine predators to an artificially made Batesian mimic (a cockroach equipped with the warning pattern of the red firebug) with respect to their dietary ecology. Half of the individuals of each species were fed on unmodified roaches before the experiment, whereas the other half were fed with mealworms and thus had no previous experience with roaches. We found that Batesian mimics were better protected than inconspicuous prey against inexperienced great tits and robins alone. The other three bird species showed high level of neophobia; therefore, the effect of warning coloration could not be assessed. We also found that experienced birds attacked a greater number of Batesian mimics compared to inexperienced individuals of all tested species, with the exception of blackcaps. In the great tits, robins, and blue tits, a significant number of experienced birds attacked the Batesian mimic, which was possibly the result of a learned search image for a roach. Our results suggest that using a limited array of predators to describe evolutionary processes forming the diversity of antipredatory strategies of the prey may be biased and need not describe the situation occurring in nature.     

Social and spatial effects on genetic variation between foraging flocks in a wild bird population

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co‐occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission–fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission–fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%–45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space‐independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.     

Intraspecific variation in the strength of density dependence in aphid populations

Abstract.  1. Experimental evidence is presented for positive, negative, and no density dependence from 32 independent density manipulations of milkweed aphids ( Aphis nerii ) in laboratory and field experiments. This substantial variation in intraspecific density dependence is associated with temperature and host-plant species.
2. It is reported that as population growth rate increases, density dependence becomes more strongly negative, suggesting that the monotonic definition of density dependence used in many common population models is appropriate for these aphids, and that population growth rate and carrying capacity are not directly proportional.
3. For populations that conform to these assumptions, population growth rate may be widely applicable as a predictor of the strength of density dependence.     

Exploring patterns of variation in clutch size–density reaction norms in a wild passerine bird

Negative density dependence of clutch size is a ubiquitous characteristic of avian populations and is partly due to within‐individual phenotypic plasticity. Yet, very little is known about the extent to which individuals differ in their degree of phenotypic plasticity, whether such variation has a genetic basis and whether level of plasticity can thus evolve in response to selection. Using 18 years of data of a Dutch great tit population (Parus major), we show that females reduced clutch size with increasing population density (slopes of the reaction norms), differed strongly in their average clutch size (elevations of the reaction norms) at the population‐mean density and that the latter variation was partly heritable. In contrast, we could not detect individual variation in phenotypic plasticity (‘I × E’). Level of plasticity is thus not likely to evolve in response to selection in this population. Observed clutch sizes deviated more from the estimated individual reaction norms in certain years and densities, implying that the within‐individual between‐year variance (so‐called residual variance) of clutch size was heterogeneous with respect to these factors. Given the observational nature of this study, experimental manipulation of density is now warranted to confirm the causality of the observed density effects. Our analyses demonstrate that failure to acknowledge this heterogeneity would have inflated the estimate of ‘I × E’ and led to misinterpretation of the data. This paper thereby emphasizes the fact that heterogeneity in residuals can provide biologically insightful information about the ecological processes underlying the data.     

Ultralong telomeres shorten with age in nestling great tits but are static in adults and mask attrition of short telomeres

Telomere length (TL) is increasingly being used as a biomarker of senescence, but measuring telomeres remains a challenge. Within tissue samples, TL varies between cells and chromosomes. Class I telomeres are (presumably static) interstitial telomeric sequences, while terminal telomeres have been divided in shorter (Class II) telomeres and ultralong (Class III) telomeres, and the presence of the latter varies strongly between species. Class II telomeres typically shorten with age, but little is known of Class III telomere dynamics. Using multiple experimental approaches, we show great tits to have ultralong telomeres, and we investigated age effects on Class II and III telomeres using a longitudinal approach (our method excludes Class I telomeres). In adults, TL averaged over the whole distribution did not significantly change with age. However, more detailed analyses showed that Class II TL did shorten with age, and, as in other species, the longest Class II telomeres within individuals shortened more quickly with age. In contrast, Class III TL did not shorten with age within individual adults. Surprisingly, we found the opposite pattern in nestlings: Class III TL shortened significantly with age, while the age effect on Class II TL was close to zero. Thus, Class III TL may provide information on developmental history, while Class II TL provides information on telomere dynamics in adulthood. These findings have practical implications for telomere studies and raise the interesting question of what causes variation in TL dynamics between chromosomes within individuals and how this is related to development.     

Cycles, stochasticity and density dependence in pink salmon population dynamics

Complex dynamics of animal populations often involve deterministic and stochastic components. A fascinating example is the variation in magnitude of 2-year cycles in abundances of pink salmon (Oncorhynchus gorbuscha) stocks along the North Pacific rim. Pink salmon have a 2-year anadromous and semelparous life cycle, resulting in odd- and even-year lineages that occupy the same habitats but are reproductively isolated in time. One lineage is often much more abundant than the other in a given river, and there are phase switches in dominance between odd- and even-year lines. In some regions, the weak line is absent and in others both lines are abundant. Our analysis of 33 stocks indicates that these patterns probably result from stochastic perturbations of damped oscillations owing to density-dependent mortality caused by interactions between lineages. Possible mechanisms are cannibalism, disease transmission, food depletion and habitat degradation by which one lineage affects the other, although no mechanism has been well-studied. Our results provide comprehensive empirical estimates of lagged density-dependent mortality in salmon populations and suggest that a combination of stochasticity and density dependence drives cyclical dynamics of pink salmon stocks.     

Obtaining accurate measurements of the size and volume of insects fed to nestlings from video recordings

Video recordings are commonly used to study the types, amount, and size of food items provided to nestling birds. However, the accuracy and repeatability of estimates of the size of food items from video recordings has not been examined. We assessed three aspects of the reliability of measuring prey size from video recordings of Great Tits (Parus major) provisioning nestlings. To test the accuracy of measurements of prey size (length and width) used to determine prey volume, we molded artificial plasticine caterpillars and compared their size and volume as determined using measurements of length and width on screenshots of video recordings (using the vertical diameter of nest‐box entrance holes as a size reference) to their actual size and volume. We also examined within‐ and among‐observer repeatability of measurements of the size and volume of actual prey items delivered to nestlings by adult Great Tits. We found that observers were able to accurately measure prey size and determine volume, with high agreement between the actual size and volume of plasticine caterpillars and the size and volume as determined from measurements made on screenshots from video recordings (r_ICC = 0.99). In addition, within‐ and among‐observer repeatability were also high (r_ICC = 0.98 and 0.93, respectively). Overall, our results suggest that the size of prey items delivered to nestlings by adults in video recordings can be accurately measured and those measurements, in turn, can be used to accurately determine the volume of those insect prey.     

Factors affecting population regulation of a colonial vulture

Two hypotheses have been proposed to link population regulation to density‐dependent changes in demographical parameters: the habitat heterogeneity hypothesis (HHH) states that, as population density rises, an increasing proportion of individuals are forced to occupy low‐quality territories, which provokes a decline in average per‐capita survival and/or productivity although some individuals show no decline in fecundity; and the individual adjustment hypothesis (IAH), which suggests that increased densities lead to reductions in survival and/or fecundity by enhancing agonistic interactions, which affect all individuals to a similar extent. However, density‐dependent effects can be affected by density‐independent factors (DIF), such as weather. We test the effects of density dependence on annual reproductive success in Griffon Vultures Gyps fulvus at four spatial scales, nest‐site, cliff, colony and metacolony, in northern Spain from 2008 to 2015. Our results showed most support for the HHH at all scales. At the colony and cliff scale, IAH and DIF had similar importance, whereas there was little evidence of IAH at the metacolony and the nest scale. The best protected eyries (caves, potholes and sheltered ledges) produced the most fledglings and were used preferentially, whereas low‐quality eyries (exposed ledges or open crevices) were used only when the number of breeders increased. The significant interaction between breeding failure and density found for the more exposed eyries suggests that at higher densities, breeding pairs are forced to use poorer nesting areas, and the negative effect of density at the cliff scale could be due to the combined effect of a higher proportion of pairs using low‐quality eyries and the negative effect of rainfall.     

Warming at the population level: Effects on age structure,density, and generation cycles

The impact of climate change on strongly age‐structured populations is poorly understood, despite the central role of temperature in determining developmental rates in ectotherms. Here we examine the effect of warming and its interactions with resource availability on the population dynamics of the pyralid moth Plodia interpunctella, populations of which normally show generation cycles, a consequence of strong and asymmetric age‐related competition. Warming by 3°C above the standard culture temperature led to substantial changes in population density, age structure, and population dynamics. Adult populations were some 50% larger in warmed populations, probably because the reduced fecundity associated with warming leads to reduced larval competition, allowing more larvae to develop to adulthood. Warming also interacted with resource availability to alter population dynamics, with the generation cycles typical of this species breaking down in the 30° populations when standard laboratory diet was provided but not when a reduced nutrient poor diet was used. Warming by 6° led to either rapid extinction or the persistence of populations at low densities for the duration of the experiment. We conclude that even moderate warming can have considerable effects on population structure and dynamics, potentially leading to complete changes in dynamics in some cases. These results are particularly relevant given the large number of economically important species that exhibit generation cycling, in many cases arising from similar mechanisms to those operating in P. interpunctella.     

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird

Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality‐related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density‐dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.     

Predicting fluctuations of reintroduced ibex populations: the importance of density dependence, environmental stochasticity and uncertain population estimates

1. Development of population projections requires estimates of observation error, parameters characterizing expected dynamics such as the specific population growth rate and the form of density regulation, the influence of stochastic factors on population dynamics, and quantification of the uncertainty in the parameter estimates. 2. Here we construct a Population Prediction Interval (PPI) based on Bayesian state space modelling of future population growth of 28 reintroduced ibex populations in Switzerland that have been censused for up to 68 years. Our aim is to examine whether the interpopulation variation in the precision of the population projections is related to differences in the parameters characterizing the expected dynamics, in the effects of environmental stochasticity, in the magnitude of uncertainty in the population parameters, or in the observation error. 3. The error in the population censuses was small. The median coefficient of variation in the estimates across populations was 5.1%. 4. Significant density regulation was present in 53.6% of the populations, but was in general weak. 5. The width of the PPI calculated for a period of 5 years showed large variation among populations, and was explained by differences in the impact of environmental stochasticity on population dynamics. 6. In spite of the high accuracy in population estimates, the uncertainty in the parameter estimates was still large. This uncertainty affected the precision in the population predictions, but it decreased with increasing length of study period, mainly due to higher precision in the estimates of the environmental variance in the longer time-series. 7. These analyses reveal that predictions of future population fluctuations of weakly density-regulated populations such as the ibex often become uncertain. Credible population predictions require that this uncertainty is properly quantified.     

Population dynamics of three songbird species in a nestbox population in Central Europe show effects of density,climate and competitive interactions

Unravelling the contributions of density‐dependent and density‐independent factors in determining species population dynamics is a challenge, especially if the two factors interact. One approach is to apply stochastic population models to long‐term data, yet few studies have included interactions between density‐dependent and density‐independent factors, or explored more than one type of stochastic population model. However, both are important because model choice critically affects inference on population dynamics and stability. Here, we used a multiple models approach and applied log‐linear and non‐linear stochastic population models to time series (spanning 29 years) on the population growth rates of Blue Tits Cyanistes caeruleus, Great Tits Parus major and Pied Flycatchers Ficedula hypoleuca breeding in two nestbox populations in southern Germany. We focused on the roles of climate conditions and intra‐ and interspecific competition in determining population growth rates. Density dependence was evident in all populations. For Blue Tits in one population and for Great Tits in both populations, addition of a density‐independent factor improved model fit. At one location, Blue Tit population growth rate increased following warmer winters, whereas Great Tit population growth rates decreased following warmer springs. Importantly, Great Tit population growth rate also decreased following years of high Blue Tit abundance, but not vice versa. This finding is consistent with asymmetric interspecific competition and implies that competition could carry over to influence population dynamics. At the other location, Great Tit population growth rate decreased following years of high Pied Flycatcher abundance but only when Great Tit population numbers were low, illustrating that the roles of density‐dependent and density‐independent factors are not necessarily mutually exclusive. The dynamics of this Great Tit population, in contrast to the other populations, were unstable and chaotic, raising the question of whether interactions between density‐dependent and density‐independent factors play a role in determining the (in) stability of the dynamics of species populations.     

Accounting for stochasticity in demographic compensation along the elevational range of an alpine plant

Demographic compensation arises when vital rates change in opposite directions across populations, buffering the variation in population growth rates, and is a mechanism often invoked to explain the stability of species geographic ranges. However, studies on demographic compensation have disregarded the effects of temporal variation in vital rates and their temporal correlations, despite theoretical evidence that stochastic dynamics can affect population persistence in temporally varying environments. We carried out a seven‐year‐long demographic study on the perennial plant Arabis alpina (L.) across six populations encompassing most of its elevational range. We discovered demographic compensation in the form of negative correlations between the means of plant vital rates, but also between their temporal coefficients of variation, correlations and elasticities. Even if their contribution to demographic compensation was small, this highlights a previously overlooked, but potentially important, role of stochastic processes in stabilising population dynamics at range margins.     

An integrated modeling approach to estimating Gunnison sage‐grouse population dynamics: combining index and demographic data

Evaluation of population dynamics for rare and declining species is often limited to data that are sparse and/or of poor quality. Frequently, the best data available for rare bird species are based on large‐scale, population count data. These data are commonly based on sampling methods that lack consistent sampling effort, do not account for detectability, and are complicated by observer bias. For some species, short‐term studies of demographic rates have been conducted as well, but the data from such studies are typically analyzed separately. To utilize the strengths and minimize the weaknesses of these two data types, we developed a novel Bayesian integrated model that links population count data and population demographic data through population growth rate (λ) for Gunnison sage‐grouse (Centrocercus minimus). The long‐term population index data available for Gunnison sage‐grouse are annual (years 1953–2012) male lek counts. An intensive demographic study was also conducted from years 2005 to 2010. We were able to reduce the variability in expected population growth rates across time, while correcting for potential small sample size bias in the demographic data. We found the population of Gunnison sage‐grouse to be variable and slightly declining over the past 16 years.