Density-mediated carry-over effects explain variation in breeding output across time in a seasonal population

In seasonal environments, where density dependence can operate throughout the annual cycle, vital rates are typically considered to be a function of the number of individuals at the beginning of each season. However, variation in density in the previous season could also cause surviving individuals to be in poor physiological condition, which could carry over to influence individual success in the following season. We examine this hypothesis using replicated populations of Drosophila melanogaster, the common fruitfly, over 23 non-overlapping generations with distinct breeding and non-breeding seasons. We found that the density at the beginning of the non-breeding season negatively affected the fresh weight of individuals that survived the non-breeding season and resulted in a 25% decrease in per capita breeding output among those that survived to the next season to breed. At the population level, per capita breeding output was best explained by a model that incorporated density at the beginning of the previous non-breeding season (carry-over effect, COE) and density at the beginning of the breeding season. Our results support the idea that density-mediated COEs are critical for understanding population dynamics in seasonal environments.     

Population dynamics of a South American rodent: seasonal structure interacting with climate,density dependence and predator effects

Understanding the role of interactions between intrinsic feedback loops and external climatic forces is one of the central challenges within the field of population ecology. For rodent dynamics, the seasonal structure of the environment necessitates changes between two stages: reproductive and non-reproductive. Nevertheless, the interactions between seasonality, climate, density dependence and predators have been generally ignored. We demonstrate that direct climate effects, the nonlinear effect of predators and the nonlinear first-order feedback embedded in a seasonal structure are key elements underlying the large and irregular fluctuations in population numbers exhibited by a small rodent in a semi-arid region of central Chile. We found that factors influencing population growth rates clearly differ between breeding and non-breeding seasons. In addition, we detected nonlinear density dependencies as well as nonlinear and differential effects of generalist and specialist predators. Recent climatic changes may account for dramatic perturbations of the rodent's population dynamics. Changes in the predator guild induced by climate are likely to result, through the food web, in a large impact on small rodent demography and population dynamics. Assuming such interactions to be typical of ecological systems, we conclude that appropriate predictions of the ecological consequences of climate change will depend on having an in-depth understanding of the community-weather system.     

Why spacing behavior does not stabilize density in cyclic populations of microtine rodents

Summary There are several published hypotheses that consider spacing behavior to be a significant factor causing the multiannual density fluctuations characteristic of some microtine rodent populations. Recent modeling efforts have concluded, however, that spacing behavior should have a stabilizing rather than a destabilizing effect on population dynamics. Why doesn't spacing behavior stabilize these cyclic populations? We argue that while spacing behavior does have a stabilizing influence on population dynamics by limiting the number of breeding individuals, reproduction continues and population size is not limited in an asymptotic manner. Rather, microtine social organization produces demographic changes within a population that allow density cycles to occur under certain conditions. Using a simulation model, we demonstrate that in a strongly seasonal environment populations with low density dependence in reproduction will cycle whereas populations with high density dependence in reproduction will have relatively stable densities. Given such complicating factors as the annual species nature of microtine rodents, occasionally intense predation, and the tendency for territoriality to break down during the non-breeding season, individuals with low density dependence in reproduction will always be able to invade and eventually dominate populations with high density dependence in reproduction, regardless of the resulting destabilization of population dynamics.     

Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system

Acquired immunity is known to be a key modulator of the dynamics of many helminth parasites in domestic and human host populations, but its relative importance in natural populations is more controversial. A detailed long-term dataset on the gastrointestinal nematode Trichostrongylus retortaeformis in a wild population of European rabbits (Oryctolagus cuniculus) shows clear evidence of seasonal acquired immunity in the age-structured infection profiles. By fitting a hierarchy of demographic infection-immunity models to the observed age-structured infection patterns, we are able to quantify the importance of different components (seasonality, immunity and host age structure) of the parasite dynamics. We find strong evidence that the hosts' immunocompetence waxes and wanes with the seasons, but also contains a lifelong cohort factor, possibly acting through a maternal effect dependent on the host's month of birth. These observations have important and broad implications for the ecology of parasite infection in seasonal natural herbivore systems.     

Restricted dispersal reduces the strength of spatial density dependence in a tropical bird population

Spatial processes could play an important role in density-dependent population regulation because the disproportionate use of poor quality habitats as population size increases is widespread in animal populations-the so-called buffer effect. While the buffer effect patterns and their demographic consequences have been described in a number of wild populations, much less is known about how dispersal affects distribution patterns and ultimately density dependence. Here, we investigated the role of dispersal in spatial density dependence using an extraordinarily detailed dataset from a reintroduced Mauritius kestrel (Falco punctatus) population with a territorial (despotic) breeding system. We show that recruitment rates varied significantly between territories, and that territory occupancy was related to its recruitment rate, both of which are consistent with the buffer effect theory. However, we also show that restricted dispersal affects the patterns of territory occupancy with the territories close to release sites being occupied sooner and for longer as the population has grown than the territories further away. As a result of these dispersal patterns, the strength of spatial density dependence is significantly reduced. We conclude that restricted dispersal can modify spatial density dependence in the wild, which has implications for the way population dynamics are likely to be impacted by environmental change.     

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.     

Strong migratory connectivity and seasonally shifting isotopic niches in geographically separated populations of a long-distance migrating songbird

Whether migratory animals use similar resources during continental-scale movements that characterize their annual cycles is highly relevant to both individual performances and population dynamics. Direct knowledge of the locations and resources used by migrants during non-breeding is generally scarce. Our goal was to estimate migratory connectivity of a small Palaearctic long-distance migrant, the common nightingale Luscinia megarhynchos, and to compare resources used in non-breeding areas with resources used at the breeding grounds. We tracked individuals of three geographically separated populations and characterised their stable isotope niches during breeding and non-breeding over 2 years. Individuals spent the non-breeding period in population-specific clusters from west to central Africa, indicating strong migratory connectivity at the population level. Irrespective of origin, their isotopic niches were surprisingly similar within a particular period, although sites of residence were distant. However, niche characteristics differed markedly between breeding and non-breeding periods, indicating a consistent seasonal isotopic niche shift in the sampled populations. Although nightingales of distinct breeding populations migrated to different non-breeding areas, they chose similar foraging conditions within specific periods. However, nightingales clearly changed resource use between breeding and non-breeding periods, indicating adaptations to changes in food availability.     

Sex-specific costs of reproduction on survival in a long-lived seabird

Costs of reproduction on survival have captured the attention of researchers since life history theory was formulated. Adults of long-lived species may increase survival by reducing their breeding effort or even skipping reproduction. In this study, we aimed to evaluate the costs of current reproduction on survival and whether skipping reproduction increases adult survival in a long-lived seabird. We used capture–mark–recapture data (1450 encounters) from two populations of Bulwer''s petrel (Bulweria bulwerii), breeding in the Azores and Canary Islands, North Atlantic Ocean. Using a multi-event model with two different breeding statuses (breeders versus non-breeders), we calculated probabilities of survival and of transitions between breeding statuses, evaluating potential differences between sexes. Females had lower survival probabilities than males, independent of their breeding status. When considering breeding status, breeding females had lower survival probabilities than non-breeding females, suggesting costs of reproduction on survival. Breeding males had higher survival probabilities than non-breeding males, suggesting that males do not incur costs of reproduction on survival and that only the highest quality males have access to breeding. The highest and the lowest probabilities of skipping reproduction were found in breeding males from the Azores and in breeding males from the Canary Islands, respectively. Intermediate values were observed in the females from both populations. This result is probably due to differences in the external factors affecting both populations, essentially predation pressure and competition. The existence of sex-specific costs of reproduction on survival in several populations of this long-lived species may have important implications for species population dynamics.     

Experimental Examination of Intraspecific Density-Dependent Competition during the Breeding Period in Monarch Butterflies (Danaus plexippus)

A central goal of population ecology is to identify the factors that regulate population growth. Monarch butterflies (Danaus plexippus) in eastern North America re-colonize the breeding range over several generations that result in population densities that vary across space and time during the breeding season. We used laboratory experiments to measure the strength of density-dependent intraspecific competition on egg laying rate and larval survival and then applied our results to density estimates of wild monarch populations to model the strength of density dependence during the breeding season. Egg laying rates did not change with density but larvae at high densities were smaller, had lower survival, and weighed less as adults compared to lower densities. Using mean larval densities from field surveys resulted in conservative estimates of density-dependent population reduction that varied between breeding regions and different phases of the breeding season. Our results suggest the highest levels of population reduction due to density-dependent intraspecific competition occur early in the breeding season in the southern portion of the breeding range. However, we also found that the strength of density dependence could be almost five times higher depending on how many life-stages were used as part of field estimates. Our study is the first to link experimental results of a density-dependent reduction in vital rates to observed monarch densities in the wild and show that the effects of density dependent competition in monarchs varies across space and time, providing valuable information for developing robust, year-round population models in this migratory organism.     

Generalized Linear Dynamics of a Plant-Parasitic Nematode Population and the Economic Evaluation of Crop Rotations

In 1-year experiments, the final population density of nematodes is usually modeled as a function of initial density. Often, estimation of the parameters is precarious because nematode measurements, although laborious and expensive, are imprecise and the range in initial densities may be small. The estimation procedure can be improved by using orthogonal regression with a parameter for initial density on each experimental unit. In multi-year experiments parameters of a dynamic model can be estimated with optimization techniques like simulated annealing or Bayesian methods such as Markov chain Monte Carlo (MCMC). With these algorithms information from different experiments can be combined. In multi-year dynamic models, the stability of the steady states is an important issue. With chaotic dynamics, prediction of densities and associated economic loss will be possible only on a short timescale. In this study, a generic model was developed that describes population dynamics in crop rotations. Mathematical analysis showed stable steady states do exist for this dynamic model. Using the Metropolis algorithm, the model was fitted to data from a multi-year experiment on Pratylenchus penetrans dynamics with treatments that varied between years. For three crops, parameters for a yield loss assessment model were available and gross margin of the six possible rotations comprising these three crops and a fallow year were compared at the steady state of nematode density. Sensitivity of mean gross margin to changes in the parameter estimates was investigated. We discuss the general applicability of the dynamic rotation model and the opportunities arising from combination of the model with Bayesian calibration techniques for more efficient utilization and collection of data relevant for economic evaluation of crop rotations.     

Population density and seasonality effects on Sin Nombre virus transmission in North American deermice (Peromyscus maniculatus) in outdoor enclosures

Surveys of wildlife host-pathogen systems often document clear seasonal variation in transmission; conclusions concerning the relationship between host population density and transmission vary. In the field, effects of seasonality and population density on natural disease cycles are challenging to measure independently, but laboratory experiments may poorly reflect what happens in nature. Outdoor manipulative experiments are an alternative that controls for some variables in a relatively natural environment. Using outdoor enclosures, we tested effects of North American deermouse (Peromyscus maniculatus) population density and season on transmission dynamics of Sin Nombre hantavirus. In early summer, mid-summer, late summer, and fall 2007-2008, predetermined numbers of infected and uninfected adult wild deermice were released into enclosures and trapped weekly or bi-weekly. We documented 18 transmission events and observed significant seasonal effects on transmission, wounding frequency, and host breeding condition. Apparent differences in transmission incidence or wounding frequency between high- and low-density treatments were not statistically significant. However, high host density was associated with a lower proportion of males with scrotal testes. Seasonality may have a stronger influence on disease transmission dynamics than host population density, and density effects cannot be considered independent of seasonality.     

Breeding phenology and winter activity predict subsequent breeding success in a trans-global migratory seabird

Inter-seasonal events are believed to connect and affect reproductive performance (RP) in animals. However, much remains unknown about such carry-over effects (COEs), in particular how behaviour patterns during highly mobile life-history stages, such as migration, affect RP. To address this question, we measured at-sea behaviour in a long-lived migratory seabird, the Manx shearwater (Puffinus puffinus) and obtained data for individual migration cycles over 5 years, by tracking with geolocator/immersion loggers, along with 6 years of RP data. We found that individual breeding and non-breeding phenology correlated with subsequent RP, with birds hyperactive during winter more likely to fail to reproduce. Furthermore, parental investment during one year influenced breeding success during the next, a COE reflecting the trade-off between current and future RP. Our results suggest that different life-history stages interact to influence RP in the next breeding season, so that behaviour patterns during winter may be important determinants of variation in subsequent fitness among individuals.     

Population Dynamics of Belonolaimus longicaudatusin a Cotton Production System

Belonolaimus longicaudatus is a recognized pathogen of cotton (Gossypium hirsutum), but insufficient information is available on the population dynamics and economic thresholds of B. longicaudatus in cotton production. In this study, data collected from a field in Florida were used to develop models predicting population increases of B. longicaudatus on cotton and population declines under clean fallow. Population densities of B. longicaudatus increased on cotton, reaching a carrying capacity of 139 nematodes/130 cm³ of soil, but decreased exponentially during periods of bare fallow. The model indicated that population densities should decrease each year of monocropped cotton, if an alternate host is not present between sequential cotton crops. Economic thresholds derived from published damage functions and current prices for cotton and nematicides varied from 2 to 5 B. longicaudatus/130 cm³ of soil, depending on the nematicide used.     

Implications of nest-site limitation on density-dependent nest predation at variable spatial scales in a cavity-nesting bird

Nest‐site limitation may have different implications in the spatial distribution of breeding pairs depending on the availability of suitable habitat and the types of nest‐sites. Distribution of cavities suitable as nest sites may allow circumstantial aggregation or active choice of colonial nesting, which may have different implications on breeding performance through effects on breeding density, with variable costs and benefits depending on the consequences of intraspecific competition, social interactions and predation. We evaluated the effects of breeding density derived from nesting site limitation on breeding performance and predation at different spatial scales and considering multiple social, population and environmental limiting factors in the red‐billed chough Pyrrhocorax pyrrhocorax. The results indicate that variable breeding density may arise within the population depending on the availability and spatial distribution of nest‐sites. Nest‐site availability and distribution may also determine social breeding systems (isolated or aggregated) at variable densities, thus resembling differences found at different spatially distant populations under contrasting environmental conditions. Breeding performance was related to density‐dependent processes of population regulation, especially density‐dependent nest predation due to predator attraction to nest clusters. Results also indicate that predation pressure depend on density patterns at large scales. This suggest that predation may have important consequences on population dynamics of spatially structured populations depending on the strength of this kind of density dependence, which in turn may depend on habitat features affecting the prey but also the spatially variable guild of predators. Because habitat and nesting site availability may vary spatially depending on multiple human influences, understanding the strength and form in which breeding density and nest predation at different spatial scales may influence the size and persistence of populations can help to manage them more adequately.     

Reconsidering the importance of the past in predator–prey models: both numerical and functional responses depend on delayed prey densities

We propose that delayed predator–prey models may provide superficially acceptable predictions for spurious reasons. Through experimentation and modelling, we offer a new approach: using a model experimental predator–prey system (the ciliates Didinium and Paramecium), we determine the influence of past-prey abundance at a fixed delay (approx. one generation) on both functional and numerical responses (i.e. the influence of present : past-prey abundance on ingestion and growth, respectively). We reveal a nonlinear influence of past-prey abundance on both responses, with the two responding differently. Including these responses in a model indicated that delay in the numerical response drives population oscillations, supporting the accepted (but untested) notion that reproduction, not feeding, is highly dependent on the past. We next indicate how delays impact short- and long-term population dynamics. Critically, we show that although superficially the standard (parsimonious) approach to modelling can reasonably fit independently obtained time-series data, it does so by relying on biologically unrealistic parameter values. By contrast, including our fully parametrized delayed density dependence provides a better fit, offering insights into underlying mechanisms. We therefore present a new approach to explore time-series data and a revised framework for further theoretical studies.     

Weak migratory connectivity,loop migration and multiple non-breeding site use in British breeding Whinchats Saxicola rubetra

Determining the links between breeding populations and the pressures, threats and conditions they experience presents a challenge for the conservation of migratory birds which can use multiple sites separated by hundreds to thousands of kilometres. Furthermore, migratory connectivity – the connections made by migrating individuals between networks of breeding and non-breeding sites – has important implications for population dynamics. The Whinchat Saxicola rubetra is declining across its range, and tracking data from a single African non-breeding site implies high migratory spread. We used geolocators to describe the migration routes and non-breeding areas of 20 Whinchats from three British breeding populations. As expected, migratory spread was high, with birds from the three populations overlapping across a wide area of West Africa. On average, in non-breeding areas, British breeding Whinchats were located 652 km apart from one another, with some likely to share non-breeding areas with individuals from breeding populations as far east as Russia. Four males made a direct non-breeding season movement to a second, more westerly, non-breeding location in January. Autumn migration was through Iberia and around the western edge of the Sahara Desert, whereas spring migration was more direct, indicating an anticlockwise loop migration. Weak migratory connectivity implies that Whinchat populations are somewhat buffered against local changes in non-breeding conditions. If non-breeding season processes have played a role in the species’ decline, then large-scale drivers are likely to be the cause, although processes operating on migration, or interactions between breeding and non-breeding processes, cannot be ruled out.     

Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird

Prior to reproduction, migratory animals are at the juxtaposition of three life history stages in which they must finish the non-breeding stage, initiate and complete migration, and prepare for the onset of breeding. However, how these stages interact with one another is not fully understood. We provide evidence that, for migratory birds that begin breeding development prior to departure from non-breeding sites, the level of breeding preparation can drive migration phenology, a critical behavioral determinant of reproductive success. Specifically, male American redstart (Setophaga ruticilla) plasma androgen levels, which increase in males during the period leading into migration, were positively correlated with energetic condition. We empirically tested the hypothesis that elevated androgen simultaneously supports migratory and breeding preparation in a hormone manipulation field experiment. Males with testosterone implants showed advanced preparation for migration and breeding, and ultimately departed on migration earlier than controls. It is assumed that early departure leads to early arrival at breeding areas, which increases breeding success. Collectively, our observational and experimental results demonstrate how overlapping life history stages can interact to influence important components of an individual's fitness. This highlights the critical need for understanding population processes across the full life cycle of an organism to better understand the ecological and evolutionary origins of complex life history events.     

Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent

Animals have to adjust their physiology to seasonal changes, in response to variation in food availability, social tactics and reproduction. I compared basal corticosterone and testosterone levels in free ranging striped mouse from a desert habitat, comparing between the sexes, breeding and philopatric non-breeding individuals, and between the breeding and the non-breeding season. I expected differences between breeders and non-breeders and between seasons with high and low food availability. Basal serum corticosterone was measured from 132 different individuals and serum testosterone from 176 different individuals of free living striped mice. Corticosterone and testosterone levels were independent of age, body weight and not influenced by carrying a transmitter. The levels of corticosterone and testosterone declined by approximately 50% from the breeding to the non-breeding season in breeding females as well as non-breeding males and females. In contrast, breeding males showed much lower corticosterone levels during the breeding season than all other classes, and were the only class that showed an increase of corticosterone from the breeding to the non-breeding season. As a result, breeding males had similar corticosterone levels as other social classes during the non-breeding season. During the breeding season, breeding males had much higher testosterone levels than other classes, which decreased significantly from the breeding to the non-breeding season. My results support the prediction that corticosterone decreases during periods of low food abundance. Variation in the pattern of hormonal secretion in striped mice might assist them to cope with seasonal changes in energy demand in a desert habitat.     

Explaining the geographical origins of seasonal influenza A (H3N2)

Most antigenically novel and evolutionarily successful strains of seasonal influenza A (H3N2) originate in East, South and Southeast Asia. To understand this pattern, we simulated the ecological and evolutionary dynamics of influenza in a host metapopulation representing the temperate north, tropics and temperate south. Although seasonality and air traffic are frequently used to explain global migratory patterns of influenza, we find that other factors may have a comparable or greater impact. Notably, a region''s basic reproductive number (R₀) strongly affects the antigenic evolution of its viral population and the probability that its strains will spread and fix globally: a 17–28% higher R₀ in one region can explain the observed patterns. Seasonality, in contrast, increases the probability that a tropical (less seasonal) population will export evolutionarily successful strains but alone does not predict that these strains will be antigenically advanced. The relative sizes of different host populations, their birth and death rates, and the region in which H3N2 first appears affect influenza''s phylogeography in different but relatively minor ways. These results suggest general principles that dictate the spatial dynamics of antigenically evolving pathogens and offer predictions for how changes in human ecology might affect influenza evolution.     

Prefledging Growth and Recruitment of Female Lesser Scaup

Annual variation in juvenile recruitment is an important component of duck population dynamics, yet little is known about the factors affecting the probability of surviving and breeding in the first year of life. Two hypothesized mechanisms to explain annual variability are indirect carry-over effects (COEs) from conditions experienced during the prefledging period and direct effects from climatic conditions during the postfledging period. We used Cormack-Jolly-Seber models to estimate apparent survival and detection rates of 643 juvenile female lesser scaup (Aythya affinis) marked just prior to fledging at Red Rock Lakes National Wildlife Refuge in southwestern Montana, USA, 2010–2018. We evaluated COEs from hatch date, a hatch date × spring phenology interaction, and conspecific duckling density in addition to a direct climatic effect of winter conditions (indexed by the El Niño Southern Oscillation [ENSO]) and spring habitat conditions on the study area. We used growth data from a subset (n = 190) of known-aged ducklings to estimate the influence of hatch date and conspecific density on prefledging growth to help identify mechanisms underlying COEs. Prefledging growth and juvenile apparent survival were negatively related to measures of conspecific duckling density. We found evidence that detection probability varied annually for juvenile (but not adult) scaup, possibly representing decisions to delay breeding and not return to or remain at the study site in their first year of life. Like with apparent survival, there was suggestive evidence that detection probability decreased with increasing duckling density in the previous year. Hatching date was weakly negatively related to detection probability, but unrelated to apparent survival, whereas neither vital rate was related to winter ENSO index. Our results are consistent with a process where density-dependent growth rates in the prefledging period carry over to influence fitness in subsequent life-cycle stages. If this pattern generalizes to other systems, this density COE may have important implications for our understanding of duck population dynamics and reaffirms the importance of maintaining abundant brood-rearing habitats in conservation and management of ducks. © 2021 The Wildlife Society.