Determinants of heart rate in Svalbard reindeer reveal mechanisms of seasonal energy management

Seasonal energetic challenges may constrain an animal's ability to respond to changing individual and environmental conditions. Here, we investigated variation in heart rate, a well-established proxy for metabolic rate, in Svalbard reindeer ( Rangifer tarandus platyrhynchus ), a species with strong seasonal changes in foraging and metabolic activity. In 19 adult females, we recorded heart rate, subcutaneous temperature and activity using biologgers. Mean heart rate more than doubled from winter to summer. Typical drivers of energy expenditure, such as reproduction and activity, explained a relatively limited amount of variation (2–6% in winter and 16–24% in summer) compared to seasonality, which explained 75% of annual variation in heart rate. The relationship between heart rate and subcutaneous temperature depended on individual state via body mass, age and reproductive status, and the results suggested that peripheral heterothermy is an important pathway of energy management in both winter and summer. While the seasonal plasticity in energetics makes Svalbard reindeer well-adapted to their highly seasonal environment, intraseasonal constraints on modulation of their heart rate may limit their ability to respond to severe environmental change. This study emphasizes the importance of encompassing individual state and seasonal context when studying energetics in free-living animals. This article is part of the theme issue ‘Measuring physiology in free-living animals (Part II)’.

Host phenology can select for multiple stable parasite virulence strategies

Host phenology is an important driver of parasite transmission and evolution. In a seasonal environment, monocyclic, obligate-killer parasites evolve optimal virulence strategies such that all parasite progeny are released near the end of the host season to limit parasite progeny death in the environment. It is unclear whether host seasonality imposes different constraints on polycyclic parasites such that both polycyclic and monocyclic parasites are maintained. We develop a mathematical model of a disease system with seasonal host activity to study the evolutionary consequences of host phenology on polycyclic, obligate-killer parasite virulence strategies. Seasonal host activity patterns create both monocyclic and polycyclic parasite evolutionarily stable strategies (ESS) separated by less-fit strategies (evolutionary repellors). The ESS that evolves in each system is a function of the virulence strategy of the parasite introduced into the system. The trait value for both monocyclic and polycyclic strategies is determined by two aspects of host phenology: the duration of the host activity period and the distribution in the time at which hosts first become active within each season. Longer host activity periods and more synchronous host emergence drive both the monocyclic and polycyclic strategies towards lower virulence. The results demonstrate that host phenology can, in theory, maintain diverse parasite strategies among isolated geographic locations.

Resource and seasonality drive interspecific variability in a Dynamic Energy Budget model

Animals show a vast array of phenotypic traits in time and space. These variation patterns have traditionally been described as ecogeographical rules; for example, the tendency of size and clutch size to increase with latitude (Bergman's and Lack's rules, respectively). Despite considerable research into these patterns, the processes behind trait variation remain controversial. Here, we show how food variability, which determines individual energy input and allocation trade-offs, can drive interspecific trait variation. Using a dynamic energy budget (DEB) model, we simulated different food environments as well as interspecific variability in the parameters for energy assimilation, mobilization, and allocation to soma. We found that interspecific variability is greater when the resource is non-limiting in both constant and seasonal environments. Our findings further show that individuals can reach larger biomass and greater reproductive output in a seasonal environment than in a constant environment of equal average resource due to the peaks of food surplus. Our results agree with the classical patterns of interspecific trait variation and provide a mechanistic understanding that supports recent hypotheses which explain them: the resource and the eNPP (net primary production during the growing season) rules. Due to the current alterations to ecosystems and communities, disentangling trait variation is increasingly important to understand and predict biodiversity dynamics under environmental change.

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate

The evolutionary benefits of reproductive seasonality are often measured by a single-fitness component, namely offspring survival. Yet different fitness components may be maximized by different birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons ( Papio ursinus ) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. We identify two distinct optimal birth timings in the annual cycle, located four-month apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother–offspring conflict. Maternal trade-offs over birth timing, which extend into mother–offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.

Evolutionary determinants of non-seasonal breeding in wild chacma baboons

ABSTRACTAnimal reproductive phenology varies from strongly seasonal to non-seasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of non-seasonal breeding in seasonal environments. We investigated the evolutionary determinants of non-seasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that non-seasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favouring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals, and (ii) females delay their reproductive timings (fertility periods and conceptions) according to other females in the group to stagger conceptions. These results indicate that reproductive competition generates reproductive asynchrony, weakening the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in gregarious organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Breeding seasonality generates reproductive trade-offs in a long-lived mammal

ABSTRACTThe evolutionary benefits of reproductive seasonality are usually measured by a single fitness component, namely offspring survival to nutritional independence (Bronson, 2009). Yet different fitness components may be maximised by dissimilar birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons (Papio ursinus) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. Like humans, baboons are eclectic omnivores, give birth every 1-3 years to a single offspring that develops slowly, and typically breed year-round. We identify two distinct optimal birth timings in the annual cycle, located 4-months apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother-offspring conflict (Maestripieri, 2002). Maternal trade-offs over birth timing, which extend into mother-offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Such trade-offs may substantially weaken the benefits of seasonal reproduction, and our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.SIGNIFICANCE STATEMENTWhy some species breed seasonally and others do not remain unclear. The fitness consequences of birth timing have traditionally been measured on offspring survival, ignoring other fitness components. We investigated the effects of birth timing on two fitness components in wild baboons, who breed year-round despite living in a seasonal savannah. Birth timing generates a trade-off between offspring survival and future maternal reproductive pace, meaning that mothers cannot maximize both. When birth timing favours maternal reproductive pace (instead of offspring survival), behavioural manifestations of mother-offspring conflict around weaning are intense. These results open new avenues to understand the evolution of reproductive timings in long-lived animals including humans, where such reproductive trade-offs may commonly weaken the intensity of reproductive seasonality.

Diet of Culpeo fox (Lycalopex culpaeus, Molina 1782): the role of non-native prey in a strongly seasonal environment of south-central Chile

In this study, we establish the seasonal variation of the Culpeo fox’s diet in a seasonal ecosystem of south-central Chile. By scat analyses, 21 prey taxa were identified, 16 were animal and five were plant species. Mammals (88.47%) were the main biomass contribution with small seasonal fluctuations. Plants contributed the most to the differences observed in all seasons since they showed very marked changes. We determined that the Culpeo fox inhabiting the Andes of south-central Chile feeds mainly on small non-native mammals all year round, and supplements its diet opportunistically from items whose abundance oscillates seasonally.