Slicing:A sustainable approach to structuring samples for analysis in long-term studies

The longitudinal study of populations is a core tool for understanding ecological and evolutionary processes. Long‐term studies typically collect samples repeatedly over individual lifetimes and across generations. These samples are then analysed in batches (e.g. qPCR plates) and clusters (i.e. group of batches) over time in the laboratory. However, these analyses are constrained by cross‐classified data structures introduced biologically or through experimental design. The separation of biological variation from the confounding among‐batch and among‐cluster variation is crucial, yet often ignored. The commonly used approaches to structuring samples for analysis, sequential and randomization, generate bias due to the non‐independence between time of collection and the batch and cluster they are analysed in. We propose a new sample structuring strategy, called slicing, designed to separate confounding among‐batch and among‐cluster variation from biological variation. Through simulations, we tested the statistical power and precision to detect within‐individual, between‐individual, year and cohort effects of this novel approach. Our slicing approach, whereby recently and previously collected samples are sequentially analysed in clusters together, enables the statistical separation of collection time and cluster effects by bridging clusters together, for which we provide a case study. Our simulations show, with reasonable slicing width and angle, similar precision and similar or greater statistical power to detect year, cohort, within‐ and between‐individual effects when samples are sliced across batches, compared with strategies that aggregate longitudinal samples or use randomized allocation. While the best approach to analysing long‐term datasets depends on the structure of the data and questions of interest, it is vital to account for confounding among‐cluster and batch variation. Our slicing approach is simple to apply and creates the necessary statistical independence of batch and cluster from environmental or biological variables of interest. Crucially, it allows sequential analysis of samples and flexible inclusion of current data in later analyses without completely confounding the analysis. Our approach maximizes the scientific value of every sample, as each will optimally contribute to unbiased statistical inference from the data. Slicing thereby maximizes the power of growing biobanks to address important ecological, epidemiological and evolutionary questions

Life after logging in tropical forests of Borneo: A meta-analysis

Selectively logged tropical forests retain high species richness and functional diversity, but species composition changes after logging, suggesting that some species are more vulnerable to logging than others. We did a meta-analysis to summarise the effect of logging on the abundance of individual bird and mammal species in tropical forests of Borneo, which have suffered some of the most intense selective logging in the tropics. We found that species classified by the International Union for Conservation of Nature (IUCN) as ‘vulnerable’ or ‘near-threatened’ are generally less abundant in logged tropical forests than those classified as ‘least concern’. However, the effect of logging within each IUCN category is variable, indicating that logging is not the only or main cause of decline in abundance. While our results show that closely related species responded similarly to logging, in birds there was significant variation between responses of some closely related species. Bigger species were significantly more susceptible to logging than smaller species in both birds and mammals. We also found that cavity-nesting birds suffered more from logging than did other species. Our results highlight the importance of identifying which factors lead individual species to flourish or suffer in logged tropical forests

Lego clocks: building a clock from parts

A new finding opens up speculation that the molecular mechanism of circadian clocks in Synechococcus elongatus is composed of multiple oscillator systems (Kitayama and colleagues, this issue, pp. 1513–1521), as has been described in many eukaryotic clock model systems. However, an alternative intepretation is that the pacemaker mechanism—as previously suggested—lies primarily in the rate of ATP hydrolysis by the clock protein KaiC

Temporal niche switching and reduced nest attendance in response to heat dissipation limits in lactating common voles (<i>Microtus arvalis</i>)

According to the heat dissipation limit theory, maximum metabolic turnover is limited by the capacity of the body to dissipate excess heat. Small mammals, including common voles (Microtus arvalis), face a heat dissipation limitation during lactation. Pup growth and milk production are reduced under higher ambient temperatures. Heat dissipation problems might in part be alleviated by modifying behavior, such as reducing nest attendance and being active at energetically optimal times of day. According to the circadian thermo-energetics hypothesis, animals can make use of daily ambient temperature fluctuations to alter their energetic expenditure. In this study we test whether heat challenged (housing at 30 °C compared to 21 °C) lactating common voles allocate their time differently among behaviors and whether their ultradian and circadian behavioral rhythmicity are altered. Behavior was scored every 13 min from automated picture recordings, while general locomotor activity was measured by passive infrared detectors to assess ultradian and circadian organization. The effects of ambient temperature on the ultradian organization of behavior were assessed by determining the ultradian period length and the distribution of activity within the ultradian bout. Changes in circadian organization were assessed by the distribution of activity over the light and dark phase. As a complementary measure nest temperature recordings were used to quantify nest attendance distribution between day and night. Lactating dams at 30 °C reduced the fraction of time spent on the nest while increasing the fraction of time resting without pups away from the nest. The ultradian period of locomotor activity was longer in voles housed at 30 °C during pregnancy and lactation, but not after weaning when the pups were removed. No differences in the distribution of activity within the ultradian bout could be detected. The circadian organization was also modulated by ambient temperature. Lactating voles housed at 30 °C became more day active and a loss of day–night differences in nest temperature suggests a shift of nest attendance towards the night. Reducing the time attending the nest can reduce the risk of hyperthermia, and may be the behavioral component resulting in lower milk production and hence reproductive output. Becoming more day active allows feeding and nursing of the pups during the rest phase to occur during the night at which lower ambient temperatures are expected in the field. In natural situations this strategy will increase heat dissipation and lactation capacity. Whether there are similar benefits associated with a longer ultradian period is currently unknown, but these are likely to result from decreased energy turnover at 30 °C. In conclusion, our study shows that lactating common voles facing heat dissipation problems re-organize their behavior in a way that can maximize heat dissipation capabilities and thereby optimize lactation capacity

Sanchez-Tojar_et_al_2016_JAB

This database contains the necessary data to run the all the GLMs and GLMMs presented in: Sanchez-Tojar et al. 2016 Winter territory prospecting is associated with life-history stage but not activity in a passerine, published in Journal of Avian Biology

Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis): a test of the heat dissipation limit theory

The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in livestock has increased litter size or productivity in these animals. To test the wider validity of the heat dissipation limit theory, we studied common voles (Microtus arvalis), which have small litter sizes by comparison with mice and rats, and regular addition of wild-caught individuals of this species to our laboratory colony ensures a natural genetic background. A crossover design of ambient temperatures (21 and 30°C) during pregnancy and lactation was used. High ambient temperature during lactation decreased milk production, slowing pup growth. The effect on pup growth was amplified when ambient temperature was also high during pregnancy. Shaving fur off dams at 30°C resulted in faster growth of pups; however, no significant increase in food intake and or milk production was detected. With increasing litter size (natural and enlarged), asymptotic food intake during lactation levelled off in the largest litters at both 21 and 30°C. Interestingly, the effects of lactation temperature on pup growth where also observed at smaller litter sizes. This suggests that vole dams trade-off costs associated with hyperthermia during lactation with the yield from investment in pup growth. Moreover, pup survival was higher at 30°C, despite lower growth, probably owing to thermoregulatory benefits. It remains to be seen how the balance is established between the negative effect of high ambient temperature on maternal milk production and pup growth (and/or future reproduction of the dam) and the positive effect of high temperatures on pup survival. This balance ultimately determines the effect of different ambient temperatures on reproductive success.

Sanchez-Tojar_et_al_2016_JAB

This database contains the necessary data to run the all the GLMs and GLMMs presented in: Sanchez-Tojar et al. 2016 Winter territory prospecting is associated with life-history stage but not activity in a passerine, published in Journal of Avian Biology