An ontogenetic perspective on individual differences

Journal of Animal Ecology

1. Evolutionary theories of seasonal migration generally assume that the costs of longer migrations are balanced by benefits at the non-breeding destinations. 2. We tested, and rejected, the null hypothesis of equal survival and timing of spring migration for High Arctic breeding sanderling Calidris alba using six and eight winter destinations between 55°N and 25°S, respectively. 3. Annual apparent survival was considerably lower for adult birds wintering in tropical West Africa (Mauritania: 0.74 and Ghana: 0.75) than in three European sites (0.84, 0.84 and 0.87) and in subtropical Namibia (0.85). Moreover, compared with adults, second calendar-year sanderlings in the tropics, but not in Europe, often refrained from migrating north during the first possible breeding season. During northward migration, tropical-wintering sanderlings occurred at their final staging site in Iceland 5-15 days later than birds wintering further north or south. Namibia-wintering sanderlings tracked with solar geolocators only staged in West Africa during southward migration. 4. The low annual survival, the later age of first northward migration and the later passage through Iceland during northward migration of tropical-wintering sanderlings, in addition to the skipping of this area during northward but not southward This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Scientific Reports

Phenological variability among populations is widespread in nature. A few predictive phenological models integrate intrapopulational variability, but none has ever explored the individual strategies potentially occurring within a population. The "pace-of-life" syndrome accounts for such individual strategies, but has yet to be explored under a phenological context. Here we integrated, for the first time, the slow-fast thermal strategies stemming from the "pace-of-life" into a mechanistic predictive framework. We obtained 4619 phenological observations of an important crop pest in the Bolivian Andes by individually following 840 individuals under five rearing temperatures and across nine life stages. The model calibrated with the observed individual "pace-of-life" strategies showed a higher accuracy in phenological predictions than when accounting for intrapopulational variability alone. We further explored our framework with generated data and suggest that ectotherm species with a high number of life stages and with slow and/or fast individuals should exhibit a greater variance of populational phenology, resulting in a potentially longer time window of interaction with other species. We believe that the "pace-of-life" framework is a promising approach to improve phenological prediction across a wide array of species.

Frontiers in Ecology and Evolution

While avian migration timing is clearly influenced by both breeding and non-breeding geography, it is challenging to identify the relative and interdependent roles of endogenous programs, early-life experience, and carry-over effects in the development of adult annual schedules. Bar-tailed godwits Limosa lapponica baueri migrate northward from New Zealand toward Asian stopover sites during the boreal spring, with differences in timing between individuals known to relate to their eventual breedingground geography in Alaska. Here, we studied the timing of northward migration of individual godwits at three sites spanning 1,100 km of New Zealand's 1,400-km length. A lack of morphological or genetic structure among sites indicates that the Alaskan breeding population mixes freely across all sites, and larger birds (southern breeders) tended to migrate earlier than smaller birds (northern breeders) at all sites. However, we unexpectedly found that migration timing varied between the sites, with birds from southern New Zealand departing on average 9.4-11 days earlier than birds from more northerly sites, a difference consistent across 4 years of monitoring. There is no obvious adaptive reason for migration timing differences of this magnitude, and it is likely that geographic variation in timing within New Zealand represents a direct response to latitudinal variation in photoperiod. Using resightings of marked birds, we show that immature godwits explore widely around New Zealand before embarking on their first northward migration at age 2-4 years. Thus, the process by which individual migration dates are established appears to involve: (1) settlement by sub-adult godwits at non-breeding sites, to which they are highly faithful as adults; (2) a consequent response to environmental cues (i.e., photoperiod) that sets the local population's migration window; and (3) endogenous mechanisms, driven by breeding geography, that establish and maintain the well-documented consistent differences between individuals. This implies that behavioral decisions by young godwits have long-lasting impacts on adult annual-cycle schedules, but the factors guiding non-breeding settlement are currently unknown.

Frontiers in Ecology and Evolution

For migratory animals, events at one stage of the annual cycle can produce constraints or benefits that carry over to subsequent stages. Differing life-history strategies among individuals can influence the expression of these carry-over effects, leading to pronounced within-population variation in migration. For example, reproductive roles can drive spatiotemporal segregation during the non-breeding season and promote sex-specific carry-over effects, such as reproductive effort affecting autumn migration behavior. For an alpine breeding population of horned larks Eremophila alpestris in northern British Columbia, Canada, we addressed sex-specific variation in migration behavior and carry-over effects during both autumn and spring migration using light-level geolocators. Males spent more time farther north and arrived an average of 6 days earlier at the breeding site in spring. Females delayed autumn departure following greater reproductive effort, in turn demonstrating flexible migration behavior by increasing migration speed and decreasing stopover use. Males maintained autumn migration behavior regardless of reproductive effort or departure date. Finally, both sexes used staging areas in spring (average stopover = 41 days), with consequences for breeding success. Individuals that used staging areas during spring migration exhibited greater nest success and produced 1.8 more fledglings on average than those that migrated directly from their winter site. Consistent use of staging areas may allow individuals to monitor environmental conditions and optimize their breeding arrival date to acquire high-quality territories while avoiding the cost of arriving too early in a harsh alpine habitat. Overall, our results indicate: (1) sex-specific flexibility in migration strategies that carry-over to and from the reproductive period, and (2) spring staging areas may be a critical component of the annual life-cycle for alpine breeding larks. These behaviors may be particularly important for alpine and arctic birds because the stochastic nature of their breeding habitat likely selects for flexible responses to prevailing conditions.

The Journal of Experimental Biology

The slow, inexorable rise in annual average global temperatures and acidification of the oceans are often advanced as consequences of global change. However, many environmental changes, especially those involving weather (as opposed to climate), are often stochastic, variable and extreme, particularly in temperate terrestrial or freshwater habitats. Moreover, few studies of animal and plant phenotypic plasticity employ realistic (i.e. short-term, stochastic) environmental change in their protocols. Here, I posit that the frequently abrupt environmental changes (days, weeks, months) accompanying much longer-term general climate change (e.g. global warming over decades or centuries) require consideration of the true nature of environmental change (as opposed to statistical means) coupled with an expansion of focus to consider developmental phenotypic plasticity. Such plasticity can be in multiple forms – obligatory/facultative, beneficial/deleterious – depending upon the degree and ra...

Ecology and Evolution, 2017

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Nature Communications, 2021

Globally, bird migration is occurring earlier in the year, consistent with climate-related changes in breeding resources. Although often attributed to phenotypic plasticity, there is no clear demonstration of long-term population advancement in avian migration through individual plasticity. Using direct observations of bar-tailed godwits (Limosa lapponica) departing New Zealand on a 16,000-km journey to Alaska, we show that migration advanced by six days during 2008–2020, and that within-individual advancement was sufficient to explain this population-level change. However, in individuals tracked for the entire migration (50 total tracks of 36 individuals), earlier departure did not lead to earlier arrival or breeding in Alaska, due to prolonged stopovers in Asia. Moreover, changes in breeding-site phenology varied across Alaska, but were not reflected in within-population differences in advancement of migratory departure. We demonstrate that plastic responses can drive population-l...

Ecology and Evolution, 2019

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Journal of Animal Ecology, 2016

African departure rather than migration speed determines variation in spring arrival in pied flycatchers.

Functional Ecology, 2017

Shifts in hatch dates do not provide pied flycatchers with a rapid ontogenetic route to adjust offspring time schedules to climate change Ouwehand, Janne; Burger, Claudia; Both, Christiaan

Journal of Avian Biology, 2018

The development of migratory behaviour is a continuous process which is not only determined by genes, but also moulded by individual differences based on life-history variations occurring at each ontogenetic stage. Assessing consistency and plasticity in migratory traits between long distance (LDM) and short distance migratory (SDM) populations within the same species that may express dissimilarities in the leeway of annual schedules is essential to understand the evolution and ontogeny of migratory strategies. We studied the migration strategies in autumn regarding flight speed and the use of stopovers (number and duration of stopovers across the whole journey) at the intraspecific level, by tracking with GPS loggers the intercontinental migration of 43 adult and juvenile ospreys Pandion haliaetus from both LDM and SDM populations. LDM ospreys travelled distances five times larger than SDM ospreys, but their total migration speed was 2.4 times slower. While daily distance travelled did not differ between populations, the reduced total migration speed by LDMs was due to higher stopover use compared to SDM birds. SDM birds used more direct routes, crossing open sea at higher flight speeds, even though both populations largely benefitted from wind assistance across their journey. Across populations, adult birds travelled longer distances per day and displayed less sinuous migratory paths than juveniles, suggesting that migratory capabilities improve with age and experience of the bird. Overall, the time constraint related to total migration distance was not the main driver of the total migration speed, and other factors such as physiological needs to rest and refuel at stopover sites may play an important role. Our study underlines the importance of investigating variability in migration strategies in partially migratory species, for a better understanding of avian migratory ecology.

Journal of Animal Ecology, 2017

1. Migration is a widespread phenomenon in the animal kingdom. On the basis of the considerable variation that exists between and within species, and even within populations, we may be able to infer the (age-and sex-specific) ecological trade-offs and constraints moulding migration systems from assessments of fitness associated with migration and wintering in different areas. 2. During three consecutive breeding seasons, we compared the reproductive performance (timing of breeding, breeding success, chick body condition and post-fledging survival) of Eurasian spoonbills Platalea leucorodia that breed at a single breeding site in The Netherlands, but migrate different distances (c. 4,500 vs. 2,000 km, either or not crossing the Sahara) to and from wintering areas in southern Europe and West Africa. Using mark-recapture analysis, we further investigated whether survival until adulthood (recruitment probability) of chicks hatched between 2006 and 2010 was related to their hatch date and body condition. 3. Long-distance migrants bred later, particularly the males, and raised chicks of poorer body condition than short-distance migrants. Hatch dates strongly advanced with increasing age in short-distance migrants, but hardly advanced in longdistance migrants, causing the difference in timing of breeding between long-and short-distance migrants to be more pronounced among older birds. 4. Breeding success and chick body condition decreased over the season, and chicks that fledged late in the season or in poor condition were less likely to survive until adulthood. As a result, long-distance migrants-particularly the males and older birds-likely recruit fewer offspring into the breeding population than short-distance migrants. This inference is important for predicting the population-level consequences of changes in winter habitat suitability throughout the wintering range. 5. Assuming that the long-distance migrants-being the birds that occupy the traditional wintering areas-are not the poorer quality birds, and that the observed agedependent patterns in timing of breeding are driven by within-individual effects and not by selective disappearance, our results suggest that the strategy of long-distance This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

The Auk, 2022

The Pacific Basin, by virtue of its vastness and its complex aeroscape, provides unique opportunities to address questions about the behavioral and physiological capabilities and mechanisms through which birds can complete spectacular flights. No longer is the Pacific seen just as a formidable barrier between terrestrial habitats in the north and the south, but rather as a gateway for specialized species, such as shorebirds, to make a living on hemispherically distributed seasonal resources. This recent change in perspective is dramatic, and the research that underpins it has presented new opportunities to learn about phenomena that often challenge a sense of normal. Ancient Polynesians were aware of the seasonal passage of shorebirds and other landbirds over the Pacific Ocean, incorporating these observations into their navigational "tool kit" as they explored and colonized the Pacific. Some ten centuries later, systematic visual observations and tracking technology have revealed much about movement of these shorebirds, especially the enormity of their individual nonstop flights. This invites a broad suite of questions, often requiring comparative studies with bird migration across other ocean basins, or across continents. For example, how do birds manage many days of nonstop exercise apparently without sleep? What mechanisms explain birds acting as if they possess a Global Positioning System? How do such extreme migrations evolve? Through advances in both theory and tracking technology, biologists are poised to greatly expand the horizons of movement ecology as we know it. In this integrative review, we present a series of intriguing questions about trans-Pacific migrant shorebirds and summarize recent advances in knowledge about migratory behavior operating at temporal scales ranging from immediate decisions during a single flight, to adaptive learning throughout a lifetime, to evolutionary development of migratory pathways. Recent advances in this realm should stimulate future research across the globe and across a broad array of disciplines.

The Journal of Experimental Biology, 2020

The perception, processing and response to environmental challenges involves the activation of the immuno-neuroendocrine (INE) interplay. Concerted environmental challenges might induce trade-off when resource allocation to one trait occurs at the expense of another, also producing potential transgenerational effects in the offspring. We evaluated whether concerted challenges, in the form of an immune inoculum against inactivated Salmonella Enteritidis (immune challenge, ICH) and a chronic heat stress (CHS) exposure on adult Japanese quail, modulates the INE responses of the parental generation and their offspring. Adults were inoculated and later exposed to a CHS along 9 consecutive days. The last 5 days of CHS, eggs were collected for incubation. Chicks were identified according to their parental treatments and remained undisturbed. Induced inflammatory response, Heterophil/Lymphocyte (H/L) ratio and specific humoral response against sheep red blood cells (SRBC) were evaluated in both generations. Regardless of the ICH, stressed adults showed a reduced inflammatory response (p<0.001) and an elevated H/L ratio (p=0.02) compared to controls. In offspring, the inflammatory response was elevated (p=0.03) and the specific SRBC antibody titers were diminished (p=0.02) in those chicks prenatally exposed to CHS, regardless of the ICH. No differences were found in the H/L ratio of the offspring. Together, our results suggest that CHS exposure influences the INE interplay of adult quail, establishing trade-offs within their immune system. Moreover, CHS not only affected parental INE responses but also modulated their offspring, probably affecting their potential to respond to future challenges. The adaptability of offspring's programming would depend on the environment encountered.

Oikos, 2018

Oikos, 2018

Individuals are rarely equal. When differences among individuals are associated with traits that underlie fitness components, they provide the variation required for natural selection to take place. To address unanswered questions related to the fundamental process of individual heterogeneity, we held a workshop entitled 'Ontogeny, adaptation, and chance in life-history trajectories: do individual differences matter?' at UiT The Arctic University of Norway in October 2015. The analyses performed, the major findings obtained, and the discussions held during this workshop form the foundations of this special issue. It is worth mentioning from the start that variation in traits within and among individuals has been addressed using different metrics and many different terms in the literature, which includes among-individual variance (Peck et al. 2015), between-individual process (van de Pol and Verhulst 2006), individual quality (Wilson and Nussey 2010), individual frailty (Vaupel et al. 1979), individual stochasticity (Caswell 2009), individual heterogeneity (Vindenes and Langangen 2015), individual differences (Bérubé et al. 1999), individual variability (Pettorelli et al. 2015), carry-over effects (Harrison et al. 2011), reversible state effects (Senner et al. 2015), and silver spoon effects (Grafen 1988). In the following, we will use 'individual heterogeneity' to refer to any observed or unobserved source of variation in a given trait among individuals, irrespective of its influence on fitness. Early in life, individual heterogeneity results from genetic differences, environmental variation, and differences in parental condition or allocation (Mousseau and Fox 1998, Lindström 1999, Nussey et al. 2005, Senner et al. 2015). When initial individual heterogeneity persists-throughout life (e.g. carry-over or silver spoon effects), it is referred to as static or fixed heterogeneity (Tuljapurkar et al. 2009, Vindenes and Langangen 2015; but see Cam et al. (2016) for a discussion on this terminology). Variation in environmental conditions experienced by individuals during adulthood can also influence their life-history traits, which results in dynamic heterogeneity (Tuljapurkar et al. 2009, Vindenes and Langangen 2015). A substantial part of this dynamic heterogeneity can be driven by stochastic events and be neutral (Tuljapurkar et al. 2009, Steiner and Tuljapurkar 2012, Hernandez-Pacheco and Steiner 2017), which is also referred as individual stochasticity (Caswell 2009, Caswell and Vindenes 2018). Individual heterogeneity can have strong impacts at several scales of biological organization, from individuals to ecosystems (

Functional Ecology, 2017

Parenting is costly and because the relationship between the mother and embryos is not mutualistic, mother-offspring conflicts may exist whenever resource are scarce. However, intergenerational trade-offs and conflicts resulting from limited access to water, a vital and depreciable resource, remain largely overlooked. 2. In this study, we examined the physiological, reproductive and life history responses to water restriction in the European Common Lizard (Zootoca vivipara). We hypothesised that, under water-limited conditions, pregnant females experience both short-term and longterm physiological impacts (dehydration and stress) underlying an allocation trade-off for water between mothers and offspring. 3. Water restriction led to a decrease in body mass, and an increase in plasma osmolality (dehydration) and corticosterone concentration in both males and females. The extent of the dehydration was positively correlated with fecundity in females. This suggests a trade-off between maternal water balance and allocation of water to developing embryos during reproduction. 4. Water restriction had no immediate effect on reproductive output or offspring morphology at birth. Yet, water restriction in pregnant females enhanced their reproductive effort the following year but reduced the early life growth and annual survival of their second-year offspring. 5. These delayed fitness responses to water restriction in offspring and mothers suggest that water can trigger intergenerational conflicts as demonstrated for energy. Although the mediation of this conflict remains to be clarified, we hypothesized that it represents a selective force that influences reproductive strategies.

Functional Ecology, 2018

1. Senescence has been widely documented in wild vertebrate populations, yet the proximate drivers of age-related declines in breeding success, including allocation trade-offs and links with foraging performance, are poorly understood. For longlived, migratory species, the non-breeding period represents a critical time for investment in self-maintenance and restoration of body condition, which in many species is linked to fitness. However, the relationships between age, non-breeding foraging behaviour and fitness remain largely unexplored. 2. We performed a cross-sectional study, investigating age-related variation in the foraging activity, distribution and diet of an extremely long-lived seabird, the wandering albatross Diomedea exulans, during the non-breeding period. Eighty-two adults aged 8-33 years were tracked with geolocator-immersion loggers, and body feathers were sampled for stable isotope analysis. We tested for variation in metrics of foraging behaviour and linked age-related trends to subsequent reproductive performance. 3. There was an age-related decline in the number of landings (a proxy of foraging effort) during daylight hours, and a decrease in body feather δ 13 C values in older males but not females, yet this did not accompany an age-related shift in distributions. Males conducted fewer landings than females, and the sexes showed some spatial segregation, with males foraging further south, likely due to their differential utilization of winds. 4. Although younger (<20 years) birds had higher foraging effort, they all went on to breed successfully the following season. In contrast, among older (20+ years) birds, individuals that landed more often were more likely to defer breeding or fail during incubation, suggesting they have lower foraging success. 5. As far as we are aware, this is the first demonstration of an age-specific carry-over effect of foraging behaviour in the non-breeding period on subsequent reproductive performance. This link between foraging behaviour and fitness in late but not early adulthood indicates that the ability of individuals to forage efficiently outside the breeding period may be an important driver of fitness differences in old age. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.