Reproductive aging and age-dependent parental effects on offspring in a long-lived seabird.
Reproductive aging is a widespread process in wild populations, affecting both females and males across many species. It also plays a key role in shaping parental effects as older parents are expected to be unable to invest optimally in reproduction late in life, or such investments may be compromised by the detrimental consequences of aging. In most species, reproductive performance increases over the first breeding attempts, reaches a plateau, and then declines at older ages. Many long-lived species, however, deviate from this pattern, with older individuals maintaining high breeding performance or even improving it, often resulting in offspring of higher quality. Studies examining sex-specific patterns of reproductive aging in long-lived species from natural populations and their consequences for offspring fitness remain scarce compared to the extensive human literature. We used a long-term longitudinal dataset of reproductive data collected from a population of a long-lived seabird, the Scopoli's shearwater, to analyze (i) how a set of parental traits (i.e., reproductive success, body mass and egg size) change with maternal and paternal age, and (ii) potential age-dependent parental effects on the body mass and skeletal traits of the offspring. We found that age strongly affected reproductive success. Early-life improvement was steeper in females than in males, whereas both sexes showed the typical late-life decline expected with advancing age. Adult body mass followed a similar, though partially reversed, pattern: males gained mass more rapidly than females early in life before reaching a plateau. Age also affected female egg volume and width, with older and heavier females laying larger and wider eggs. Parental effects on offspring body mass were mainly driven by pair experience, whereas skeletal traits depended only on chick age and sex. Our study shows that reproductive aging varies across traits in long-lived species, providing support for the asynchronous theory of aging, and reveals unexpected sex-specific patterns of age-related reproductive changes in monogamous species. Moreover, it suggests that advanced parental age is not necessarily associated with negative effects on offspring fitness.
- Supplementary Content
12
- 10.1093/hropen/hoad042
- Sep 10, 2023
- Human Reproduction Open
STUDY QUESTIONWhat is the existing empirical literature on the psychosocial health and wellbeing of the parents and offspring born at an advanced parental age (APA), defined as 40 years onwards?SUMMARY ANSWERAlthough the studies show discrepancies in defining who is an APA parent and an imbalance in the empirical evidence for offspring, mothers, and fathers, there is a drive towards finding psychotic disorders and (neuro-)developmental disorders among the offspring; overall, the observed advantages and disadvantages are difficult to compare.WHAT IS KNOWN ALREADYIn many societies, children are born to parents at advanced ages and there is rising attention in the literature towards the consequences of this trend.STUDY DESIGN, SIZE, DURATIONThe systematic search was conducted in six electronic databases (PubMed including Medline, Embase, Scopus, PsycInfo, CINAHL, and SocINDEX) and was limited to papers published between 2000 and 2021 and to English-language articles. Search terms used across all six electronic databases were: (‘advanced parental age’ OR ‘advanced maternal age’ OR ‘advanced paternal age’ OR ‘advanced reproductive age’ OR ‘late parent*’ OR ‘late motherhood’ OR ‘late fatherhood’) AND (‘IVF’ OR ‘in vitro fertilization’ OR ‘in-vitro-fertilization’ OR ‘fertilization in vitro’ OR ‘ICSI’ OR ‘intracytoplasmic sperm injection’ OR ‘reproductive techn*’ OR ‘assisted reproductive technolog*’ OR ‘assisted reproduction’ OR ‘assisted conception’ OR ‘reproduction’ OR ‘conception’ OR ‘birth*’ OR ‘pregnan*’) AND (‘wellbeing’ OR ‘well-being’ OR ‘psycho-social’ OR ‘social’ OR ‘ethical’ OR ‘right to reproduce’ OR ‘justice’ OR ‘family functioning’ OR ‘parental competenc*’ OR ‘ageism’ OR ‘reproductive autonomy’ OR ‘outcome’ OR ‘risk*’ OR ‘benefit*’).PARTICIPANTS/MATERIALS, SETTING, METHODSThe included papers were empirical studies in English published between 2000 and 2021, where the study either examined the wellbeing and psychosocial health of parents and/or their children, or focused on parental competences of APA parents or on the functioning of families with APA parents. A quality assessment of the identified studies was performed with the QATSDD tool. Additionally, 20% of studies were double-checked at the data extraction and quality assessment stage to avoid bias. The variables sought were: the geographical location, the year of publication, the methodological approach, the definitions of APA used, what study group was at the centre of the research, what research topic was studied, and what advantages and disadvantages of APA were found.MAIN RESULTS AND THE ROLE OF CHANCEA total number of 5403 articles were identified, leading to 2543 articles being included for title and abstract screening after removal of duplicates. This resulted in 98 articles included for a full-text reading by four researchers. Ultimately, 69 studies were included in the final sample. The key results concerned four aspects relevant to the research goals. (i) The studies showed discrepancies in defining who is an APA parent. (ii) There was an imbalance in the empirical evidence produced for different participant groups (mothers, fathers, and offspring), with offspring being the most studied study subjects. (iii) The research topics studied underlined the increased risks of neuro-developmental and psychotic disorders among offspring. (iv) The observed advantages and disadvantages were varied and could not be compared, especially for the offspring of APA parents.LIMITATIONS, REASONS FOR CAUTIONOnly English-language studies, published between 2000 and 2021, found in the above-mentioned databases were considered for this review.WIDER IMPLICATIONS OF THE FINDINGSMore research is necessary to understand the risks and benefits of building a family at an APA for the offspring when they reach adulthood. Furthermore, studies that explore the perspective of older fathers and older parents from non-Western societies would be highly informative.STUDY FUNDING/COMPETING INTEREST(S)The writing of this manuscript was permitted by financial support provided by the Swiss National Science Foundation (Weave/Lead Agency funding program, grant number 10001AL_197415/1, project title ‘Family Building at Advanced Parental Age: An Interdisciplinary Approach’). The funder had no role in the drafting of this manuscript and the views expressed therein are those of the authors. The authors have no conflicts of interest.REGISTRATION NUMBERThis systematic review is registered in Prospero: CRD42022304564.
- Research Article
75
- 10.1890/08-1475.1
- Sep 1, 2009
- Ecology
An individual's age at first reproduction and investment in successive reproductive attempts are involved in mechanisms that can impede somatic repair, resulting in a decline in reproductive abilities with age (reproductive senescence). We used long-term data from the Black-legged Kittiwake, a long-lived seabird, to address the relationship between recruitment age, age-specific breeding success (BS), and reproductive senescence, while accounting for breeding experience and temporal variation in BS. We first detected late-life improvement in BS across all recruitment groups, which we recognized as "within-generation selection" or the selective disappearance of "frail" phenotypes. When such heterogeneity was accurately accounted for, we showed that all individuals suffered reproductive senescence. We first highlighted how different combinations of pre- and post-recruitment experience across recruitment groups resulted in maximal BS at intermediate ages. BS increased in early recruits as they gained post-recruitment experience, whereas late recruits gained pre-recruitment experience that led to high BS at recruitment. Only individuals recruiting at intermediate ages balanced their pre- and post-recruitment experience. Consistent with the "cumulative reproductive cost hypothesis," we also observed a faster decline in BS in early recruits at advanced ages, whereas individuals delaying recruitment experienced the slowest decline in BS with age. Early recruits, however, reached the highest levels of BS at intermediate ages, sensus stricto (10-13 years old), whereas individuals delaying recruitment experienced the lowest at similar ages. These divergent trajectories may reflect a "delayed trade-off" balancing a maximization of midlife BS against reproductive senescence at advanced ages. Additionally, annual variation in BS had a greater effect on individuals early in life, suggesting that experienced individuals were able to buffer out the effects of temporal variation on BS, which can ultimately improve fitness in stochastic environments. Our findings stress that (1) both observed and unobserved heterogeneity are important in detecting within-individual senescence, and (2) short-term trade-offs may be rare in long-lived species; thus, cumulated reproductive costs should be invoked as an alternative mechanism underlying reproductive senescence.
- Research Article
- 10.1016/j.cbpa.2025.111963
- Feb 1, 2026
- Comparative biochemistry and physiology. Part A, Molecular & integrative physiology
Offspring innate immunity varies with parental age in a long-lived seabird.
- Research Article
- 10.1093/humrep/dead093.740
- Jun 22, 2023
- Human Reproduction
Study question What empirical evidence exists on the well-being and psycho-social health of couples who become parents at an advanced age and their children? Summary answer Empirical evidence mostly focus on the well-being and psycho-social health of offspring (psychotic disorders, (neuro-)developmental disorders) and only little knowledge exists about their parents’ well-being. What is known already In many societies, people tend to have children at an increasingly advanced age and there is increasing attention in the medical literature towards the consequences of this trend. This systematic review is the first one to critically synthesize the existing empirical literature on the psycho-social health and well-being of parents who had their children from the age 40 onwards and their offspring. Study design, size, duration We conducted a Systematic Review and registered its protocol in Prospero (CRD42022304564). The search strategy was designed based on a Population-Context-Outcome (PCO) structure, an adaptation of the traditional Population-Intervention-Comparison-Outcome (PICO) scheme to fit the specific aims of our study. The search was conducted in six electronic databases (namely Pubmed incl. MEDLINE, Embase, Scopus, PsycInfo, CINAHL and SocINDEX) and was limited to include empirical studies published between 01.01.2000 and 31.12.2021. Participants/materials, setting, methods Studies included are empirical studies – qualitative or quantitative – where subjects were children born to 40+ parents and their parents. Studies either examined the well-being and psycho-social health of parents and/or their children or focused on the social and ethical discussions surrounding risk and benefits of advanced parental age for parents and/or the offspring. Main results and the role of chance 5’403 articles were identified, leaving 2’543 after the removal of duplicates and 98 after the screening of titles and abstracts to be included for a full-text screening. Thereafter another 30 additional articles were excluded because they did not fulfil the inclusion criteria. Simultaneously, citation searching brought up 10 additional articles to include, of which 4 were in line with the defined inclusion criteria, leading to 69 total articles included in the final sample of the present systematic review. The key results concern four aspects relevant for the research question: (1) studies show discrepancies in defining who is a parent of advanced parental age (APA); (2) there is an imbalance in the empirical evidence produced for different participant groups (e.g. mothers, fathers, offspring); (3) aspects of wellbeing (e.g. psychotic disorders, (neuro-)developmental disorders, general well-being) discussed for the specific participant group studied; and (4) a narrative synthesis of the advantages and disadvantages related to psycho-social health and wellbeing for the specific participant group. Limitations, reasons for caution Only empirical studies in English, published between 01.01.2000 and 31.12.2021 were included in this review. Also, the review focuses only on empirical evidence produced in studies where parents were 40 years or older at the time of birth. Wider implications of the findings There are many aspects of the well-being of children born by older parents which remain unknown, thus requiring more research (esp. on psychosocial wellbeing of children) to understand the (non-medico-somatic) risks and benefits of becoming parents at an older age and designing evidence-informed policies. Trial registration number Not applicable
- Research Article
18
- 10.1093/humrep/dead070
- Apr 10, 2023
- Human Reproduction
Recent decades have seen a global trend towards delaying parenthood, referred to as the 'postponement transition'. Whilst there is plentiful research regarding obstetric and paediatric outcomes related to delayed parenthood, relatively little is known about the psychosocial outcomes associated with advanced parental age during early and middle childhood. This mini-review examines the current literature regarding the psychosocial functioning of families headed by older parents. First, we give an overview of the literature that examines the psychological wellbeing of older first-time parents. We then review the literature regarding the quality of the parent-child relationship in older parent families. Finally, we discuss the psychosocial adjustment and cognitive development of children of older parents. We conclude with suggestions for future research avenues.
- Research Article
28
- 10.1016/j.socscimed.2014.06.008
- Jun 12, 2014
- Social Science & Medicine
The association between advanced maternal and paternal ages and increased adult mortality is explained by early parental loss
- Research Article
9
- 10.1007/s11064-017-2306-9
- May 23, 2017
- Neurochemical Research
Advanced maternal or paternal age is associated with increased risks of cognitive and emotional disorders. Chronic stress is also a common experience in human life that causes psychiatric diseases. However, the synergistic effects of these two factors on offspring are rarely studied. In the present study, the offspring of both young (3-4 months) and old (12-14 months) rat parents were given CUMS for 21 days at the age of 4 weeks. The effects of advanced parental age and chronic unpredictable mild stress (CUMS) on emotional and cognitive behaviors and the related cellular mechanisms were investigated by using behavioral and electrophysiological techniques. We found that CUMS decreased sucrose consumption, increased anxiety, and impaired learning and memory in offspring from both old and young breeders. However, advanced parental age impaired fear memory and spatial memory mainly in female offspring. The serum corticosterone of female offspring was lower than males, but advanced parental age significantly elevated serum corticosterone in female offspring in response to electrical foot shocks. In addition, hippocampal LTD was severely impaired in female offspring from older parents. Our results indicated that female offspring from older breeders might be more sensitive to stress, and the hippocampal function was more vulnerable. These results might provide experimental basis for the prevention and treatment of advanced parental age related psychiatric disorders in future.
- Research Article
41
- 10.1007/s10815-022-02533-w
- Aug 4, 2022
- Journal of assisted reproduction and genetics
Fertility at advanced age has become increasingly common, but the aging of parents may adversely affect the maturation of gametes and the development of embryos, and therefore the effects of aging are likely to be transmitted to the next generation. This article reviewed the studies in this field in recent years. We searched the relevant literature in recent years with the keywords of "advanced maternal/paternal age" combined with "adverse pregnancy outcome" or "birth defect" in the PubMed database and classified the effects of parental advanced age on pregnancy outcomes and birth defects. Related studies on the effect of advanced age on birth defects were classified as chromosomal abnormalities, neurological and psychiatric disorders, and other systemic diseases. The effect of assisted reproduction technology (ART) on fertility in advanced age was also discussed. Differences in the definition of the range of advanced age and other confounding factors among studies were excluded, most studies believed that advanced parental age would affect pregnancy outcomes and birth defects in offspring. To some extent, advanced parental age caused adverse pregnancy outcomes and birth defects. The occurrence of these results was related to the molecular genetic changes caused by aging, such as gene mutations, epigenetic variations, etc. Any etiology of adverse pregnancy outcomes and birth defects related to aging might be more than one. The detrimental effect of advanced age can be corrected to some extent by ART.
- Research Article
12
- 10.1111/jeb.12561
- Dec 26, 2014
- Journal of Evolutionary Biology
In nest-building species predation of nest contents is a main cause of reproductive failure and parents have to trade off reproductive investment against antipredatory behaviours. While this trade-off is modified by lifespan (short-lived species prioritize current reproduction; long-lived species prioritize future reproduction), it may vary within a breeding season, but this idea has only been tested in short-lived species. Yet, life history theory does not make any prediction how long-lived species should trade off current against future reproductive investment within a season. Here, we investigated this trade-off through predator-exposure experiments in a long-lived bird species, the brown thornbill. We exposed breeding pairs that had no prior within-season reproductive success to the models of a nest predator and a predator of adults during their first or second breeding attempt. Overall, parents reduced their feeding rate in the presence of a predator, but parents feeding second broods were more risk sensitive and almost ceased feeding when exposed to both types of predators. However, during second breeding attempts, parents had larger clutches and a higher feeding rate in the absence of predators than during first breeding attempts and approached both types of predators closer when mobbing. Our results suggest that the trade-off between reproductive investment and risk-taking can change in a long-lived species within a breeding season depending on both prior nest predation and renesting opportunities. These patterns correspond to those in short-lived species, raising the question of whether a within-season shift in reproductive investment trade-offs is independent of lifespan.
- Research Article
- 10.1111/jne.70052
- May 28, 2025
- Journal of neuroendocrinology
In a rapidly changing world, food resources are becoming more limited, leading to unpredictable bouts and durations of nutritional stress. Many studies indicate that developmental nutritional stress can permanently alter a suite of physiological, morphological, or behavioral traits, yet the phenotypic effects of low food supply in the environment may vary depending on the mode and degree of parental care. For example, our previous work suggests that zebra finch (Taeniopygia guttata castanotis) parents can buffer offspring from food restriction, minimizing negative effects on offspring growth, at the cost of maintaining their own body mass. To evaluate the effects of whole nest food restriction on the offspring further, we investigated short- and long-term changes in physiological and morphological traits of zebra finch young exposed to either an ad libitum diet or a 40% restricted diet as nestlings and juveniles until 60 days post-hatch. Specifically, we measured furculum fat, the adrenocortical response, and glucose levels throughout development and into adulthood as well as body mass in adulthood to examine any latent or persistent effect. Young from the food-restricted nests overall had significantly higher baseline corticosterone and glucose compared to controls, suggesting that the previously observed parental buffering may not have been sufficient to mitigate the deleterious effects of food restriction. Furthermore, food-restricted birds had lower body mass compared to controls in adulthood, suggesting that there was a latent effect that manifested in adulthood, potentially due to the physiological costs observed during treatment and the later release of treatment. Furculum fat, the glucose response, and the adrenocortical response did not differ between experimental groups. There was also no difference in brood body size variance between treatment groups, and previously observed parental compensation in food-restricted nests did not correlate with offspring body mass in adulthood. Lastly, there was a significant negative relationship between body mass and baseline corticosterone in adulthood, suggesting that although growth and body mass were maintained during treatment, energy may have been redirected from growth and body mass maintenance to different processes in adulthood. This study further supports the need for measuring traits after treatment ends to determine persistent effects of stressors and highlights that parents cannot fully buffer their offspring from adverse environmental conditions.
- Research Article
77
- 10.1093/schbul/sbn109
- Aug 20, 2008
- Schizophrenia Bulletin
Evidence indicates an association between older parents at birth and increased risk for schizophrenia and autism. Patients with schizophrenia and autism and their first-degree relatives have impaired social functioning; hence, impaired social functioning is probably an intermediate phenotype of the illness. This study tested the hypothesis that advanced father's age at birth would be associated with poorer social functioning in the general population. To test this hypothesis, we examined the association between parental age at birth and the social functioning of their adolescent male offspring in a population-based study. Subjects were 403486, 16- to 17-year-old Israeli-born male adolescents assessed by the Israeli Draft Board. The effect of parental age on social functioning was assessed in analyses controlling for cognitive functioning, the other parent's age, parental socioeconomic status, birth order, and year of draft board assessment. Compared with offspring of parents aged 25-29 years, the prevalence of poor social functioning was increased both in offspring of fathers younger than 20 years (odds ratio [OR] = 1.27, 95% confidence interval [CI] = 1.08-1.49) and in offspring of fathers 45 years old (OR = 1.52, 95% CI = 1.43-1.61). Male adolescent children of mothers aged 40 years and above were 1.15 (95% CI = 1.07-1.24) times more likely to have poor social functioning. These modest associations between parental age and poor social functioning in the general population parallel the associations between parental age and risk for schizophrenia and autism and suggest that the risk pathways between advanced parental age and schizophrenia and autism might, at least partially, include mildly deleterious effects on social functioning.
- Research Article
12
- 10.1093/gerona/glz070
- Mar 15, 2019
- The Journals of Gerontology: Series A
Aging is a multifactorial trait caused by early as well as late-life circumstances. A society trend that parents deliberately delay having children is of concern to health professionals, for example as advanced parental age at conception increases disease risk profiles in offspring. We here aim to study if advanced parental age at conception affects mitochondrial DNA content, a cross-species biomarker of general health, in adult human twin offspring and in a model organism. We find no deteriorated mitochondrial DNA content at advanced parental age at conception, but human mitochondrial DNA content was higher in females than males, and the difference was twofold higher at advanced maternal age at conception. Similar parental age effects and sex-specific differences in mitochondrial DNA content were found in Drosophila melanogaster. In addition, parental longevity in humans associates with both mitochondrial DNA content and parental age at conception; thus, we carefully propose that a poorer disease risk profile from advanced parental age at conception might be surpassed by superior effects of parental successful late-life reproduction that associate with parental longevity.
- Front Matter
43
- 10.1111/1365-2656.13163
- Jan 1, 2020
- Journal of Animal Ecology
Imagine yourself, as an ecologist during field work, deep in the woods. Eerily silent was the forest, when loudly from the tree above a wren started to sing. A quick, skilful use of the binoculars showed it was the male ringed last week, but swiftly the bird disappeared again among the leaves. Similar difficulties in reliably observing the behaviour of the study species will be familiar to many ecologists and can strongly affect the choice of the study species; for example, the ethologist and zoologist Nikolaas Tinbergen mentioned ease of observation as a motivation to study seabirds instead of forest birds (Tinbergen, 1939). While certainly smart choices of the study species are key to successful research, typified by the Krogh principle: "for a large number of problems there will be some animal of choice, or a few such animals, on which it can be most conveniently studied" (Krogh, 1929), most terrestrial, aquatic and aerial species cannot be well observed in the field. Technological solutions to record the movements, behaviour and physiology of animals, and associated methodological advancements for analysing the data collected, have revolutionized research in animal ecology and beyond (Brisson-Curadeau, Patterson, Whelan, Lazarus, & Elliott, 2017; Kenward, 2001; Ropert-Coudert, Beaulieu, Hanuise, & Kato, 2009; Ropert-Coudert & Wilson, 2005; Weimerskirch, 2009). The general term for this technological approach to study animals is called Biologging—'the use of miniaturized animal-attached tags for logging and/or relaying data about an animal's movements, behaviour, physiology, and/or environment' (Rutz & Hays, 2009). It is closely related to and comprises the field of Biotelemetry—the remote measurement of the physiological conditions and activity/behavioural state of animals (Cooke et al., 2004), including biomedical applications in humans. The use of electronic loggers and transmitters offers unprecedented opportunities for uncovering the 'hidden lives' of animals and achieve a more mechanistic understanding of their ecology, and indeed the first 'Virtual Issue' (an online collection of papers published on a specific topic) published by the Journal of Animal Ecology was on 'Biotelemetry and Biologging' (Hays, 2008). Progress in this broad field has been exceptional in the last decade (Baratchi, Meratnia, Havinga, Skidmore, & Toxopeus, 2013; Hussey et al., 2015; Kays, Crofoot, Jetz, & Wikelski, 2015; Wilmers et al., 2015; Brisson-Curadeau et al., 2017; Tibbetts, 2017; Harcourt et al., 2019; Lowerre-Barbieri, Kays, Thorson, & Wikelski, 2019), with exciting ongoing developments often occurring outside the field of animal ecology, including in different disciplines such as engineering, physics or computer science. As such, the Journal of Animal Ecology issued an Open Call in 2018 for a Special Feature on 'Biologging', with the aim to showcase the novel developments in the field and the range of ecological questions which can now be addressed. The call resulted in the largest number of submitted manuscripts to any Special Feature in the Journal so far, which is a further indication of the interest in the topic. In this Editorial for the Special Feature, we discuss the papers and topics covered and conclude with a brief outlook on ongoing and future developments. This Special Feature comprises 18 contributions, of which 13 present novel analyses and approaches, three are reviews, one is a meta-analysis and one is a 'How to' paper. Overall, the papers cover a broad range of biologging technologies used to address a variety of fundamental questions in animal ecology, in aquatic, terrestrial and aerial species. Three papers use light-level geolocator tags—miniature light-weight tags which measure ambient light levels to determine sunrise and sunset times, and hence estimate the approximate location of the animal (Bridge et al., 2011; Wilson, Ducamp, Rees, Culik, & Niekamp, 1992)—to investigate the ontogeny of migratory behaviour in a long-lived seabird species (Campioni, Dias, Granadeiro, & Catry, 2020), quantify effects of biologgers on the survival of tagged birds (Brlík et al., 2020) and provide a practical guide for the effective application of geolocator tags to track animals (Lisovski et al., 2020). Seven papers use GPS loggers (for a review of GPS technology, see Tomkiewicz, Fuller, Kie, & Bates, 2010) often combined with other sensor technologies such as accelerometers (see Shepard et al., 2008 for a review of the technology) and/or complementary methods including stable isotopes (see Hobson & Wassenaar, 2008 for information about the method) and behavioural observations (see Altmann, 1974 about observational methods to study animal behaviour). These GPS-based papers investigate predator–prey spatiotemporal interactions among elk Cervus canadensis and wolf Canis lupus (Cusack et al., 2020), quantify foraging niche overlap between sympatric seabird species (Dehnhard et al., 2020), or assess effects of personality on the consistency and repeatability of foraging trips in black-legged kittiwakes Rissa tridactyla (Harris et al., 2020). Other contributions present novel statistical methods to estimate individual variation in habitat selection (Muff, Signer, & Fieberg, 2020) or to identify different movement modes in movement tracks (Patin, Etienne, Lebarbier, Chamaillé-Jammes, & Benhamou, 2020), whereas other studies use fine-scale movement data to quantify the impact of wind turbines on functional habitat loss of a soaring terrestrial bird, the black kite Milvus migrans (Marques et al., 2020), or identify mating tactics of male African elephants Loxodonta africana (Taylor et al., 2020). Seven papers primarily use other biologging sensors, alone or in combination with GPS tags, including inertial measurement unit sensors (see Baratchi et al., 2013 for information on the technology) such as accelerometers (Shepard et al., 2008) and magnetometers (see Williams et al., 2017 for information on magnetometers), or wet–dry and pressure and depth sensors (for a review see Ropert-Coudert et al., 2009), to markedly enhance the quantity of information on animal behaviour, individual state and performance that can be obtained from the tagged animals. In particular, Wilson et al. (2020) critically assesses the use of metrics derived from accelerometers as a proxy for movement-related metabolic energy expenditure, with Benoit et al. (2020) using such metrics to quantify the cost of dispersal in roe deer Capreolus capreolus, and Corbeau, Prudor, Kato, and Weimerskirch (2020) to quantify and compare average energy expenditure during different flight phases (soaring and flapping flight) in juvenile and adult great frigatebirds Fregata minor during their foraging trips, to study the ontogeny of flight and foraging behaviour. Bonnot et al. (2020) use activity sensors in roe deer to disentangle the contrasting effects of predator density and human disturbance on diel activity patterns, whereas Nuijten, Gerrits, Shamoun-Baranes and Nolet (2020) present a new data compression approach for accelerometer data to overcome limitations in storage and energy capacity of loggers and aid data transmission while preserving the behavioural signal in the data. Barkley et al. (2020) develop a novel multi-sensor biologging package, combined with a new statistical modelling approach, to detect and record sub-surface interactions among aquatic animals and ensuing movement-related behavioural responses, and apply it to Greenland sharks Somniosus microcephalus. More generally, Williams et al. (2020) review a large set of biologging sensors and address the question of how to select the most appropriate type or combination of devices for different biological questions. Finally, Joo et al. (2020) review an astonishing number of 58 different R packages which have become available in the last few years for analysing movement and biologging data, to act as a road map for ecologists and software developers. We now describe in more detail the questions and topics addressed by the papers of this Special Feature. We structure this section around the diverse research questions and themes addressed by these article—ranging from topics in Behavioural Ecology, Community Ecology, Statistical Ecology and Functional Ecology, to methodological approaches, with some papers linking multiple research fields. Understanding how behaviour arises is a key question in behavioural ecology. An adaptive behaviour can be informed by genetically controlled (innate) or learned components, but while some seem to be mostly programmed from birth, such as pecking in young domestic chicks (Dawkins, 1968), others, like the chaffinch song, have an innate basis but require the animal to practise and even learn from others (Thorpe, 1958). The scope for learnt behaviours may be particularly important in long-lived species, whose long lifespan increases the opportunity to practise and learn. In fact, the breeding deferral observed in many long-lived species is thought to be driven by high costs of early breeding (Lack, 1968), which could be caused by an incomplete set of skills (Daunt, Afanasyev, Adam, Croxall, & Wanless, 2007). Thanks to ever smaller loggers which can record an animal's behaviour for ever longer periods of time, biologging is now allowing researchers to study with unprecedented detail how behaviours develop in slow-maturing animals. In this Special Feature, two papers push the boundaries of this emerging field and highlight the potential of biologging to advance our understanding of the ontogeny of animal behaviour. Corbeau et al. (2020) demonstrate how juvenile great frigatebirds progressively improve their flight skills in the first few months following their first flight. Combining GPS and accelerometers to distinguish between different flight behaviours (e.g. flapping, gliding, soaring), they show that juveniles' flight skills, initially inferior, improve gradually until becoming comparable to adults'. Interestingly, juveniles outperformed adults in some aspects, likely due to their morphology, and this may explain their remarkable months-long dispersive flights (Weimerskirch, Bishop, Jeanniard-du-Dot, Prudor, & Sachs, 2016). These findings provide one of the first insights into the development of flight in long-lived birds (Rotics et al., 2016; Yoda, Kohno, & Yasuhiko, 2004), and highlight the importance of early-life learning for the acquisition of physical skills. Campioni et al. (2020) focus on another behaviour whose ontogeny is poorly understood: migration. Some animals learn their migration routes by following older conspecifics (Mueller, O'Hara, Converse, Urbanek, & Fagan, 2013), while others follow an innate migratory distance and direction (Liedvogel, Åkesson, & Bensch, 2011). Campioni et al. (2020) provide the first robust evidence for a third mechanism by which long-lived animals may acquire a migratory strategy. In an impressive long-term study tracking the migration of Cory's shearwaters Calonectris borealis across ages, from immatures to established breeders, they show that young birds follow more exploratory routes, and as they aged they gradually advance their migration timings and shorten their migration route. These findings show that learning, memory and experience can play a key role in the development of migration behaviour in long-lived species, and provide support for the exploration-refinement hypothesis (Guilford et al., 2011) as another mechanism for the development of migration behaviour in long-lived animals (Fayet, accepted). Animal movements are fundamentally characterized by facultative switches between distinct movement modes (Fryxell et al., 2008) and many methods have been developed to identify and segment movement paths into different behavioural sections (Barraquand & Benhamou, 2008; Beyer, Morales, Murray, & Fortin, 2013; Edelhoff, Signer, & Balkenhol, 2016; Gurarie et al., 2015; Leos-Barajas et al., 2017; Michelot & Blackwell, 2019; Wang, 2019), where issues of scale and the difference between stationary and non-stationary movements are of particular importance (Benhamou, 2014). Here, Patin et al. (2020) contribute to this growing literature by extending the K-segmentation approach of Lavielle (2005) to identify breakpoints in time-series of biologging data (or more generally any multivariate time-series) and potentially categorize resulting segments into common groups based on similarities in data characteristics. This provides a viable alternative to established but often statistically complicated methods (e.g. Hidden Markov models, HMMs) for identifying "behavioural states" across time-series data. Indeed, the authors contend that in some circumstances such segmentation can actually outperform these increasingly popular yet more complex methods, and through application to both fine- and broad-scale biologging data (and through simulation) they demonstrate that their approach is scale-insensitive and may be applied to many ecologically relevant questions. An alternative to using statistical segmentation methods to identify different movement modes is to observe the behaviour and state of tagged individuals, annotate the movement paths with the observed behaviour or state time-series, derive from the annotated time-series a set of criteria to distinguish different individual states or behaviour modes from the characteristics of the movement path alone, and use these rules to identify changes in state or movement mode from tagged animals which had not been also visually monitored. To do so, Taylor et al. (2020) employ a novel use of HMMs, to identify different types of sexual behaviour in male African savanna elephants Loxodonta africana as a function of their movement. The study shows that the activity and home range of elephants vary with male reproductive status and age and as such offer an exceptional opportunity to reliably estimate fitness metrics from movement itself. The authors further discuss the implications for the conservation and management of elephants, as well as the opportunities of long-term biologging of individuals for linking movement to life-history trade-offs. While an increasing body of research has shown the impact of consistent individual differences in behavioural phenotypes, called animal personalities or behavioural syndromes (Réale et al., 2010; Sih, Bell, Johnson, & Ziemba, 2004), on foraging behaviour, exploratory movements and other spatial behaviours (Bijleveld et al., 2014; Boon, Réale, & Boutin, 2008; Minderman et al., 2010; van Overveld & Matthysen, 2010; Villegas-Ríos, Réale, Freitas, Moland, & Olsen, 2018; Wilson & McLaughlin, 2007), the important relationship between animal personality and foraging site fidelity has not been studied yet. Here, in Harris et al. (2020) GPS tagged over 100 breeding kittiwakes Rissa tridactyla across four colonies in Svalbard and used a robust type of novel object tests to measure the personality (especially, boldness) of the tagged individuals, HMMs to identify the foraging sites at sea, and also quantified the repeatability of foraging trips. Their results show that individual differences in site fidelity can be driven by differences in individual personality, with bolder birds showing more repeatable foraging trips and a higher degree of site fidelity during the chick incubation stage. This has important implications for studies on individual differences in foraging behaviour and movements, indicating that in addition to age and sex or environmental drivers, also personality differences such as boldness will need to be considered. A key aim of movement ecology research is to quantify and predict habitat/resource selection by animals (Arthur, Manly, McDonald, & Garner, 1996; Christ, Hoef, & Zimmerman, 2008; Johnson, 1980; Matthiopoulos et al., 2015; Moorcroft & Barnett, 2008; Rhodes, McAlpine, Lunney, & individual movements to the of habitat selection and use at & 2008; Johnson, 1980; Moorcroft & and differences in habitat use between individuals may be caused by differences in the individual state (Bijleveld et al., or the et al., 2008). individual differences in behaviour is a key focus of ecological research et al., and for selection have as early as et al. and and occurring more for example, et al. and et al. solutions for these solutions for selection et al., or selection analyses & 2016). et al. (2020) this and present new statistical methods to estimate individual variation in habitat The approach from the between and have been as a which used in to a set of available and the more understanding that selection and are a Johnson, & Morales, The authors on this relationship between and and develop an approach based on to estimate for and habitat selection for individuals and using both and approaches, and the approach using and This methodological advance a new for and habitat selection studies and researchers to estimate individual an unprecedented opportunity to questions of differences in the spatial ecology of habitat and the habitat used by animals is also critically important for applied questions. the growing need for energy and the on will over habitat tracking movement analyses and environmental et al. (2020) showed that soaring black turbines during migration. a loss of to of habitat for these the authors highlight that the of wind turbines is and to that soaring A fundamental of the movement ecology is that the interactions between individual conditions and the characteristics and of the the structure and of movement paths et al., 2008). Thanks to the in biologging technology, there has been a in the movements and behaviour or survival of multiple individuals from species. Here, et al. (2020) use a large tracking GPS and wet–dry sensors, to investigate and niche overlap in three breeding and closely related species of stable to investigate GPS data and to identify foraging in the tracking data. a high degree of and overlap in foraging in both incubation and with niche and individual of foraging location or The study provides novel evidence that foraging may be in even from and a contrasting to niche by by other seabirds et al., 2019; & et al. (2020) combined movement and data from a predator–prey and in the investigate the question how use can a set of data, combined with a the three common in the of of robust and obtained at spatiotemporal authors show an of of to Bonnot et al. (2020) also of predator on the authors use activity sensor and accelerometer data from GPS that to from the on of roe to at changes in activity in to disturbance and predator both by human and deer in by their in to human with the human and this is when with human the in roe deer activity a when to the of a how human may with predator–prey More generally, the is also an of how technological in biologging may also researchers to large through a biologging Finally, biologging provides new opportunities to interactions for and species. Barkley et al. (2020) demonstrate this by and a novel multi-sensor biologging of a combined and a with a accelerometer and a a to the at and on a the Greenland This is to an both and statistical methods to estimate the of animal interactions based on characteristics and of between tagged The authors use these sensors to assess behavioural changes in and depth during and following and they discuss how this may be and applied to many species, with exciting potential for future energy of animals are mostly by the of and obtained from & the and energy of the foraging behaviour and habitat use of animals et al., these research has the to overcome complex to data on and energy in animals et al., 2016). of the in the is the observations to estimate energy Here, Wilson et al. (2020) this by critically the use of metrics derived from accelerometers as a proxy for movement-related metabolic energy biologging Benoit et al. (2020) to quantify energy expenditure, body and distance as a proxy for applied to the costs of To that or to that is a fundamental question in how we animal movement with implications for and mating & 2009). roe Benoit et al. (2020) that the of dispersal is markedly more that these energy costs become more in by and that these costs are primarily at so many behavioural are between energy and energy biologging quantify and these Corbeau et al. (2020) GPS with of and to identify different flight behaviours (e.g. in great frigatebirds and quantify energy expenditure during This to compare the flapping and of soaring or between age and to the hypothesis that juvenile birds have flight skills but that they learn how to improve their skills over (see also above in the Behavioural Ecology is a general that biologging has our understanding of and species & Wilson, 2005; Wilmers et al., It is also that the of biologgers to animals & Wilson, Wilson & for including the location of the devices on the body and their (e.g. and few studies the behavioural to (e.g. & 2019; et al., 2017; et al., Williams et al. (2020) discuss how many of these have not been addressed yet. In particular, the authors highlight the need for more information on physical (e.g. to the and long-term effects for animals. potential this a from et al. (2020) that meta-analysis to review the literature to effects of geolocator on bird species. Their findings that the may to a potential on the survival of tagged Overall, both are consistent with their on the of and to to the application of biologging technologies to ecological research is the management of the devices and of the of data they It is not for a to not of observations on a et al., which storage both the during data collection and in data These are by to animal such that do not affect the animal the of resulting data. are such issues covered in great detail in the ecological and a of this Special Feature is in and for Here, et al. (2020) provide a practical on the effective use of and how resulting data be and for This multiple online in an the complex of linking to the authors also provide data and to of geolocator studies and common data to data and between which may this body of data strongly common data for such to the data storage and transmission of biologgers methods to and the data and the data et al., 2018; & 2019), or the use of to the sensors to record data when the animals the behaviour of interest et al., Here, et al. (2020) present a new data compression approach for accelerometer data to storage capacity and for the data while the data from tagged the authors compare the information from of accelerometer data and from in a in data and energy use while the in behaviour and The in use and storage can hence be used to or to the and a more of the of tagged the use of biologging sensors, a of the characteristics of the many different sensors Interestingly, in the to the on and & the the need to researchers from contrasting development of ever more is among between at some of is this more between and and yet with a it can be years the importance of is as important as ever to of the opportunities by the biologging as Williams et al. (2020) highlight in a review of the field in this Special Feature. the authors identify four sensors, data and and it into an biologging to aid for ecologists to the use of biologging technologies for ecological questions. on the the authors also address in detail the yet question of how to biological questions with the most appropriate type and combination of biologging sensors, as well as how to the and how to and complex biologging data, and conclude with an outlook of the most future developments for the use of Finally, as the and of movement and environmental data has so has the number of statistical and methods to movement data, as well as the number of software packages for movement researchers are not of the number and of software packages available for movement often the to select the most appropriate and software for the question addressed. Here, Joo et al. (2020) provide the first of the field and review a 58 different packages available for analysing movement and biologging data in the R the authors first set a for the of tracking data, identifying three key which they use to the software packages by the package, including the of the available the authors use to assess the between the and development of the and provide a road map for ecologists and software to the most appropriate for a research question and improve the of software the the movements and behaviour of most animal species cannot be studied using or not over technological smaller sensors, smaller novel and methods and their to their be to advance research in animal ecology and will be through These could to insights into a range of research for of in (e.g. et al., 2011; et al., et al., of the and of species & a understanding of the terrestrial and aquatic species in and their (Cooke et al., and the effects of and environmental in habitat foraging behaviour and acquisition in individuals and their et al., ongoing developments the of GPS but also the development of alternative that smaller tracking devices et al., 2009; & 2019; & and biologgers with sensors to measure the impact of devices on tagged animals, and novel for and remote transmission of data et al., 2020). a of the and of movement ecology, combined with methods, will be to of the and complex types and of data now by biologging will be key to achieve future ecologists will also need to to the and to and the and in data and and and and statistical The papers in this Special Feature an exciting set of the and methodological which can be and an of how more may yet be with biologging We hence that by the conservation and management has the capacity to ecology as as and GPS years It is our that this Special Feature the many insights by the application of biologging to animal ecology and the of to for their
- Research Article
- 10.1111/andr.70196
- Mar 3, 2026
- Andrology
To evaluate the associations between advanced parental age and perinatal risks in twins. We analyzed 7514 twin pairs conceived through in vitro fertilization. The exposure was advanced parental age (≥35years), analyzed separately for mothers and fathers. Primary outcomes included birth weight discordance, small for gestational age, large for gestational age, macrosomia, low birth weight, very low birth weight, preterm birth, very preterm birth, and extremely preterm birth. Odds ratios (ORs) with 95% confidence intervals (CIs) were calculated using logistic regression. Additionally, parental age was analyzed both as a categorical variable and with a restricted cubic spline. The combined effect of advanced age in both parents was further evaluated. Advanced paternal age (≥35years) was associated with increased odds of birth weight discordance (adjusted OR, 1.20; 95% CI, 1.01-1.42). A graded dose-response association was evident (p for trend=0.026), with adjusted ORs for birth weight discordance progressively increasing across paternal age categories: 1.02 (95% CI, 0.83-1.25) for ages 30-34, 1.18 (95% CI, 0.91-1.52) for ages 35-39, and 1.41 (95% CI, 1.02-1.96) for ages ≥40years, all compared to the <30years reference group. Restricted cubic spline analysis identified 37years as a threshold beyond which paternal age significantly elevated birth weight discordance risk. Similarly, advanced maternal age (≥35years) was significantly associated with increased small for gestational age odds (adjusted OR, 1.21; 95% CI, 1.04-1.41), with a significant trend (p for trend=0.012) and a restricted cubic spline-derived threshold at 30years. When both parents were over 35, the odds of birth weight discordance (adjusted OR, 1.37; 95% CI, 1.15-1.63) and small for gestational age (adjusted OR, 1.30; 95% CI, 1.13-1.50) were significantly elevated compared to both being under 35. Advanced parental age was associated with elevated risks of birth weight discordance and small for gestational age in twins, suggesting it as a contributing factor to perinatal risk.
- Research Article
3
- 10.1086/724686
- Apr 13, 2023
- Physiological and biochemical zoology : PBZ
In vertebrates, developmental conditions can have long-term effects on individual performance. It is increasingly recognized that oxidative stress could be one physiological mechanism connecting early-life experience to adult phenotype. Accordingly, markers of oxidative status could be useful for assessing the developmental constraints encountered by offspring. Although some studies have demonstrated that developmental constraints are associated with high levels of oxidative stress in offspring, it remains unclear how growth, parental behavior, and brood competition may altogether affect oxidative stress in long-lived species in the wild. Here, we investigated this question in a long-lived Antarctic bird species by testing the impact of brood competition (e.g., brood size and hatching order) on body mass and on two markers of oxidative damage in Adélie penguin chicks. We also examined the influence of parental effort (i.e., foraging trip duration) and parental body condition on chick body mass and oxidative damage. First, we found that brood competition and parental traits had significant impacts on chick body mass. Second, we found that chick age and, to a lesser extent, chick body mass were two strong determinants of the levels of oxidative damage in Adélie penguin chicks. Finally, and importantly, we also found that brood competition significantly increased the levels of one marker of oxidative damage and was associated with a lower survival probability. However, parental effort and parental condition were not significantly linked to chick levels of oxidative damage. Overall, our study demonstrates that sibling competition can generate an oxidative cost even for this long-lived Antarctic species with a limited brood size (maximum of two chicks).