Paternal but not maternal age influences early-life performance of offspring in a long-lived seabird

Variability in demographic traits between individuals within populations has profound implications for both evolutionary processes and population dynamics. Parental effects as a source of non-genetic inheritance are important processes to consider to understand the causes of individual variation. In iteroparous species, parental age is known to influence strongly reproductive success and offspring quality, but consequences on an offspring fitness component after independence are much less studied. Based on 37 years longitudinal monitoring of a long-lived seabird, the wandering albatross, we investigate delayed effects of parental age on offspring fitness components. We provide evidence that parental age influences offspring performance beyond the age of independence. By distinguishing maternal and paternal age effects, we demonstrate that paternal age, but not maternal age, impacts negatively post-fledging offspring performance.     

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.     

Age-specific cost of first reproduction in female southern elephant seals

When to commence breeding is a crucial life-history decision that may be the most important determinant of an individual''s lifetime reproductive output and can have major consequences on population dynamics. The age at which individuals first reproduce is an important factor influencing the intensity of potential costs (e.g. reduced survival) involved in the first breeding event. However, quantifying age-related variation in the cost of first reproduction in wild animals remains challenging because of the difficulty in reliably recording the first breeding event. Here, using a multi-event capture–recapture model that accounts for both imperfect detection and uncertainty in the breeding status on an 18-year dataset involving 6637 individuals, we estimated age and state-specific survival of female elephant seals (Mirounga leonina) in the declining Macquarie Island population. We detected a clear cost of first reproduction on survival. This cost was higher for both younger first-time breeders and older first-time breeders compared with females recruiting at age four, the overall mean age at first reproduction. Neither earlier primiparity nor delaying primiparity appear to confer any evolutionary advantage, rather the optimal strategy seems to be to start breeding at a single age, 4 years.     

Experimental evidence of long‐term reproductive costs in a colonial nesting seabird

Trade‐offs between current and future reproduction are central to the evolution of life histories. Experiments that manipulate brood size provide an effective approach to investigating future costs of current reproduction. Most manipulative studies to date, however, have addressed only the short‐term effects of brood size manipulation. Our goal was to determine whether survival or breeding costs of reproduction in a long‐lived species manifest beyond the subsequent breeding season. To this end, we investigated long‐term survival and breeding effects of a multi‐year reproductive cost experiment conducted on black‐legged kittiwakes Rissa tridactyla, a long‐lived colonial nesting seabird. We used multi‐state capture–recapture modeling to assess hypotheses regarding the role of experimentally reduced breeding effort and other factors, including climate phase and colony size and productivity, on future survival and breeding probabilities during the 16‐yr period following the experiment. We found that forced nest failures had a positive effect on breeding probability over time, but had no effect on long‐term survival. This apparent canalization of survival suggests that adult survival is the most important parameter influencing fitness in this long‐lived species, and that adults should pay reproductive costs in ways that do not compromise this critical life history parameter. When declines in adult survival rate are observed, they may indicate populations of conservation concern.     

Integrating high‐speed videos in capture‐mark‐recapture studies of insects

Capture–mark–recapture (CMR) studies have been used extensively in ecology and evolution. While it is feasible to apply CMR in some animals, it is considerably more challenging in small fast‐moving species such as insects. In these groups, low recapture rates can bias estimates of demographic parameters, thereby handicapping effective analysis and management of wild populations. Here, we use high‐speed videos (HSV) to capture two large dragonfly species, Anax junius and Rhionaeschna multicolor, that rarely land and, thus, are particularly challenging for CMR studies. We test whether HSV, compared to conventional “eye” observations, increases the “resighting” rates and, consequently, improves estimates of both survival rates and the effects of demographic covariates on survival. We show that the use of HSV increases the number of resights by 64% in A. junius and 48% in R. multicolor. HSV improved our estimates of resighting and survival probability which were either under‐ or overestimated with the conventional observations. Including HSV improved credible intervals for resighting rate and survival probability by 190% and 130% in A. junius and R. multicolor, respectively. Hence, it has the potential to open the door to a wide range of research possibilities on species that are traditionally difficult to monitor with distance sampling, including within insects and birds.     

Integrating growth and survival models for flexible estimation of size‐dependent survival in a cryptic,endangered snake

Estimates of demographic rates for animal populations and individuals have many applications for ecological and conservation research. In many animals, survival is size‐dependent, but estimating the form of the size–survival relationship presents challenges. For elusive species with low recapture rates, individuals’ size will be unknown at many points in time. Integrating growth and capture–mark–recapture models in a Bayesian framework empowers researchers to impute missing size data, with uncertainty, and include size as a covariate of survival, capture probability, and presence on‐site. If there is no theoretical expectation for the shape of the size–survival relationship, spline functions can allow for fitting flexible, data‐driven estimates. We use long‐term capture–mark–recapture data from the endangered San Francisco gartersnake (Thamnophis sirtalis tetrataenia) to fit an integrated growth–survival model. Growth models showed that females reach longer asymptotic lengths than males and that the magnitude of sexual size dimorphism differed among populations. The capture probability and availability of San Francisco gartersnakes for capture increased with snout–vent length. The survival rate of female snakes exhibits a nonlinear relationship with snout–vent length (SVL), with survival flat between 300 mm and 550 mm SVL before decreasing for females between 550 mm and 700 mm SVL. For male snakes, survival decreased for adult males >550 mm SVL. The survival rates of the smallest and largest San Francisco gartersnakes were highly uncertain because recapture rates were very low for these sizes. By integrating growth and survival models and using penalized splines, we found support for size‐dependent survival in San Francisco gartersnakes. Our results have applications for devising management activities for this endangered subspecies, and our methods could be applied broadly to the study of size‐dependent demography among animals.     

A dynamic global equilibrium in carnivoran diversification over 20 million years

The ecological and evolutionary processes leading to present-day biological diversity can be inferred by reconstructing the phylogeny of living organisms, and then modelling potential processes that could have produced this genealogy. A more direct approach is to estimate past processes from the fossil record. The Carnivora (Mammalia) has both substantial extant species richness and a rich fossil record. We compiled species-level data for over 10 000 fossil occurrences of nearly 1400 carnivoran species. Using this compilation, we estimated extinction, speciation and net diversification for carnivorans through the Neogene (22–2 Ma), while simultaneously modelling sampling probability. Our analyses show that caniforms (dogs, bears and relatives) have higher speciation and extinction rates than feliforms (cats, hyenas and relatives), but lower rates of net diversification. We also find that despite continual species turnover, net carnivoran diversification through the Neogene is surprisingly stable, suggesting a saturated adaptive zone, despite restructuring of the physical environment. This result is strikingly different from analyses of carnivoran diversification estimated from extant species alone. Two intervals show elevated diversification rates (13–12 Ma and 4–3 Ma), although the precise causal factors behind the two peaks in carnivoran diversification remain open questions.     

Multiple coping strategies maintain stability of a small mammal population in a resource‐restricted environment

In semi‐arid environments, aperiodic rainfall pulses determine plant production and resource availability for higher trophic levels, creating strong bottom‐up regulation. The influence of climatic factors on population vital rates often shapes the dynamics of small mammal populations in such resource‐restricted environments. Using a 21‐year biannual capture–recapture dataset (1993 to 2014), we examined the impacts of climatic factors on the population dynamics of the brush mouse (Peromyscus boylii) in semi‐arid oak woodland of coastal‐central California. We applied Pradel''s temporal symmetry model to estimate capture probability (p), apparent survival (φ), recruitment (f), and realized population growth rate (λ) of the brush mouse and examined the effects of temperature, rainfall, and El Niño on these demographic parameters. The population was stable during the study period with a monthly realized population growth rate of 0.993 ± SE 0.032, but growth varied over time from 0.680 ± 0.054 to 1.450 ± 0.083. Monthly survival estimates averaged 0.789 ± 0.005 and monthly recruitment estimates averaged 0.175 ± 0.038. Survival probability and realized population growth rate were positively correlated with rainfall and negatively correlated with temperature. In contrast, recruitment was negatively correlated with rainfall and positively correlated with temperature. Brush mice maintained their population through multiple coping strategies, with high recruitment during warmer and drier periods and higher survival during cooler and wetter conditions. Although climatic change in coastal‐central California will likely favor recruitment over survival, varying strategies may serve as a mechanism by which brush mice maintain resilience in the face of climate change. Our results indicate that rainfall and temperature are both important drivers of brush mouse population dynamics and will play a significant role in predicting the future viability of brush mice under a changing climate.     

Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail

Autotomy of body parts offers various prey animals immediate benefits of survival in compensation for considerable costs. I found that a land snail Satsuma caliginosa of populations coexisting with a snail-eating snake Pareas iwasakii survived the snake predation by autotomizing its foot, whereas those out of the snake range rarely survived. Regeneration of a lost foot completed in a few weeks but imposed a delay of shell growth. Imprints of autotomy were found in greater than 10 per cent of S. caliginosa in the snake range but in only less than 1 per cent out of it, simultaneously demonstrating intense predation by the snakes and high efficiency of autotomy for surviving snake predation in the wild. However, in experiments, mature S. caliginosa performed autotomy less frequently. Instead of the costly autotomy, they can use defensive denticles on the inside of their shell apertures. Owing to the constraints from the additive growth of shells, most pulmonate snails can produce these denticles only when they have fully grown up. Thus, this developmental constraint limits the availability of the modified aperture, resulting in ontogenetic switching of the alternative defences. This study illustrates how costs of adaptation operate in the evolution of life-history strategies under developmental constraints     

Effects of forest disturbance on the fitness of an endemic rodent in a biodiversity hotspot

Praomys delectorum occurs abundantly in both disturbed and intact forests in the Ukaguru Mountains within the Eastern Arc Mountains (EAM), Morogoro, Tanzania. While previous studies have reported that anthropogenic disturbances such as grazing, wood cutting, and harvesting have a positive effect on the population density of P. delectorum, the impact of habitat disturbance on its demographic traits is still unknown. We performed a capture–mark–recapture study in both disturbed and intact forests from June 2018 to February 2020 in order to investigate the effects of habitat disturbance on abundance and two demographic traits: survival and maturation of P. delectorum in the Ukaguru Mountains. We found no variation in abundance or maturation between intact and disturbed forests, but habitat type did affect survival. However, this effect was sex‐dependent since female survival was higher in disturbed forests, while male survival remained similar across the two forest types potentially due to differences in predation pressure or food availability between the two habitats. Continuous demographic monitoring of P. delectorum in EAM is necessary given that the increasing human population surrounding the landscape is leading to higher deforestation rates and expansion of the pine plantation in the forest reserve.     

A global synthesis of survival estimates for microbats

Accurate survival estimates are needed to construct robust population models, which are a powerful tool for understanding and predicting the fates of species under scenarios of environmental change. Microbats make up 17% of the global mammalian fauna, yet the processes that drive differences in demographics between species are poorly understood. We collected survival estimates for 44 microbat species from the literature and constructed a model to determine the effects of reproductive, feeding and demographic traits on survival. Our trait-based model indicated that bat species which produce more young per year exhibit lower apparent annual survival, as do males and juveniles compared with females and adults, respectively. Using 8 years of monitoring data for two Australian species, we demonstrate how knowledge about the effect of traits on survival can be incorporated into Bayesian survival analyses. This approach can be applied to any group and is not restricted to bats or even mammals. The incorporation of informative priors based on traits can allow for more timely construction of population models to support management decisions and actions.     

Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment

Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Cory's shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.     

Seasonal climate effects on the survival of a hibernating mammal

Global climate change and associated regional climate variability is impacting the phenology of many species, ultimately altering individual fitness and population dynamics. Yet, few studies have considered the effects of pertinent seasonal climate variability on phenology and fitness. Hibernators may be particularly susceptible to changes in seasonal climate since they have a relatively short active season in which to reproduce and gain enough mass to survive the following winter. To understand whether and how seasonal climate variability may be affecting hibernator fitness, we estimated survival from historical (1964–1968) and contemporary (2014–2017) mark–recapture data collected from the same population of Uinta ground squirrels (UGS, Urocitellus armatus), a hibernator endemic to the western United States. Despite a locally warming climate, the phenology of UGS did not change over time, yet season‐specific climate variables were important in regulating survival rates. Specifically, older age classes experienced lower survival when winters or the following springs were warm, while juveniles benefited from warmer winter temperatures. Although metabolic costs decrease with decreasing temperature in the hibernacula, arousal costs increase with decreasing temperature. Our results suggest that this trade‐off is experienced differently by immature and mature individuals. We also observed an increase in population density during that time period, suggesting resources are less limited today than they used to be. Cheatgrass is now dominating the study site and may provide a better food source to UGS than native plants did historically.     

Effects of tail autotomy on survival,growth and territory occupation in free‐ranging juvenile geckos (Oedura lesueurii)

Abstract Many animals autotomize their tails to facilitate escape from predators. Although tail autotomy can increase the likelihood of surviving a predatory encounter, it may entail subsequent costs, including reduced growth, loss of energy stores, a reduction in reproductive output, loss of social status and a decreased probability of survival during subsequent encounters with predators. To date, few studies have investigated the potential fitness costs of tail autotomy in natural populations. I investigated whether tail loss influenced survival, growth and territory occupation of juvenile velvet geckos Oedura lesueurii in a population where predatory snakes were common. During the 3‐year mark–recapture study, 32% of juveniles voluntarily autotomized their tails when first captured. Analysis of survival using the program mark showed that voluntary tail autotomy did not influence the subsequent survival of juvenile geckos. Survival was age‐dependent and was higher in 1‐year‐old animals (0.98) than in hatchlings (0.76), whereas recapture probabilities were time‐dependent. Growth rates of tailed and tailless juveniles were very similar, but tailless geckos had slow rates of tail regeneration (0.14 mm day⁻¹). Tail autotomy did not influence rock usage by geckos, and both tailed and tailless juveniles used few rocks as diurnal retreat sites (means of 1.64 and 1.47 rocks, respectively) and spent long time periods (85 and 82 days) under the same rocks. Site fidelity may confer survival advantages to juveniles in populations sympatric with ambush foraging snakes. My results show that two potential fitness costs of tail autotomy – decreased growth rates and a lower probability of survival – did not occur in juveniles from this population. However, compared with juveniles, significantly fewer adult geckos (17%) voluntarily autotomized their tails during capture. Because adults possess large tails that are used for lipid storage, the energetic costs of tail autotomy are likely to be much higher in adult than in juvenile O. lesueurii.     

Contrasted patterns of age-specific reproduction in long-lived seabirds

While the number of studies providing evidence of actuarial senescence is increasing, and covers a wide range of taxa, the process of reproductive senescence remains poorly understood. In fact, quite high reproductive output until the last years of life has been reported in several vertebrate species, so that whether or not reproductive senescence is widespread remains unknown. We compared age-specific changes of reproductive parameters between two closely related species of long-lived seabirds: the small-sized snow petrel Pagodroma nivea, and the medium-sized southern fulmar Fulmarus glacialoides. Both are sympatric in Antarctica. We used an exceptional dataset collected over more than 40 years to assess age-specific variations of both breeding probability and breeding success. We found contrasted age-specific reproductive patterns between the two species. Reproductive senescence clearly occurred from 21 years of age onwards in the southern fulmar, in both breeding probability and success, whereas we did not report any decline in the breeding success of the snow petrel, although a very late decrease in the proportion of breeders occurred at 34 years. Such a contrasted age-specific reproductive pattern was rather unexpected. Differences in life history including size or migratory behaviour are the most likely candidates to account for the difference we reported in reproductive senescence between these sympatric seabird species.     

Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird,the wandering albatross

Seabirds are top predators of the marine environment that accumulate contaminants over a long life-span. Chronic exposure to pollutants is thought to compromise survival rate and long-term reproductive outputs in these long-lived organisms, thus inducing population decline. However, the demographic consequences of contaminant exposure are largely theoretical because of the dearth of long-term datasets. This study aims to test whether adult survival rate, return to the colony and long-term breeding performance were related to blood mercury (Hg), cadmium (Cd) and persistent organic pollutants (POPs), by using a capture–mark–recapture dataset on the vulnerable wandering albatross Diomedea exulans. We did not find evidence for any effect of contaminants on adult survival probability. However, blood Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities. The proximate mechanisms underlying these deleterious effects are likely multifaceted, through physiological perturbations and interactions with reproductive costs. Using matrix population models, we projected a demographic decline in response to an increase in Hg or POPs concentrations. This decline in population growth rate could be exacerbated by other anthropogenic perturbations, such as climate change, disease and fishery bycatch. This study gives a new dimension to the overall picture of environmental threats to wildlife populations.     

Selection analysis on the rapid evolution of a secondary sexual trait

Evolutionary analyses of population translocations (experimental or accidental) have been important in demonstrating speed of evolution because they subject organisms to abrupt environmental changes that create an episode of selection. However, the strength of selection in such studies is rarely measured, limiting our understanding of the evolutionary process. This contrasts with long-term, mark–recapture studies of unmanipulated populations that measure selection directly, yet rarely reveal evolutionary change. Here, we present a study of experimental evolution of male colour in Trinidadian guppies where we tracked both evolutionary change and individual-based measures of selection. Guppies were translocated from a predator-rich to a low-predation environment within the same stream system. We used a combination of common garden experiments and monthly sampling of individuals to measure the phenotypic and genetic divergence of male coloration between ancestral and derived fish. Results show rapid evolutionary increases in orange coloration in both populations (1 year or three generations), replicating the results of previous studies. Unlike previous studies, we linked this evolution to an individual-based analysis of selection. By quantifying individual reproductive success and survival, we show, for the first time, that males with more orange and black pigment have higher reproductive success, but males with more black pigment also have higher risk of mortality. The net effect of selection is thus an advantage of orange but not black coloration, as reflected in the evolutionary response. This highlights the importance of considering all components of fitness when understanding the evolution of sexually selected traits in the wild.     

Population dynamics in a long-lived seabird: I. Impact of breeding activity on survival and breeding probability in unbanded king penguins

Understanding the trade-off between current reproductive effort, future survival and future breeding attempts is crucial for demographic analyses and life history studies. We investigated this trade-off in a population of king penguins (Aptenodytes patagonicus) marked individually with transponders using multistate capture-recapture models. This colonial seabird species has a low annual proportion of non-breeders (13%), despite a breeding cycle which lasts over 1 year. To draw inferences about the consequences of non-breeding, we tested for an effect of reproductive activity on survival and on the probability of subsequent breeding. We found that birds non-breeding in year t show the same survival rate as breeders (two-states analysis: breeding and non-breeding). However, breeders had a lower probability of breeding again the following year. This negative phenotypic correlation suggests the existence of reproductive costs affecting future breeding probability, but it might also be strengthened by late arrival for courtship in year t. A three-state analysis including breeding success revealed that failed breeders in year t have a lower probability to reproduce successfully in year t + 1 than non-breeders in year t, providing some evidence for the existence of reproductive costs. Moreover, successful breeders showed higher survival probability. This positive phenotypic correlation between current reproduction and subsequent survival supports the hypothesis of an heterogeneity in individual quality. Males breeding in year t had a lower probability to breed again in year t + 1 than females, suggesting higher reproductive costs for this sex. Such additional costs might be due to higher male parental investment in the final phase of chick-rearing, which also delays the arrival of males in year t + 1, and decreases their breeding probability. Our study is the first to explore the breeding biology and the demography of penguins without the disturbance of flipper-bands.