Drivers of Infectious Disease Seasonality: Potential Implications for COVID-19.

Not 1 year has passed since the emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19). Since its emergence, great uncertainty has surrounded the potential for COVID-19 to establish as a seasonally recurrent disease. Many infectious diseases, including endemic human coronaviruses, vary across the year. They show a wide range of seasonal waveforms, timing (phase), and amplitudes, which differ depending on the geographical region. Drivers of such patterns are predominantly studied from an epidemiological perspective with a focus on weather and behavior, but complementary insights emerge from physiological studies of seasonality in animals, including humans. Thus, we take a multidisciplinary approach to integrate knowledge from usually distinct fields. First, we review epidemiological evidence of environmental and behavioral drivers of infectious disease seasonality. Subsequently, we take a chronobiological perspective and discuss within-host changes that may affect susceptibility, morbidity, and mortality from infectious diseases. Based on photoperiodic, circannual, and comparative human data, we not only identify promising future avenues but also highlight the need for further studies in animal models. Our preliminary assessment is that host immune seasonality warrants evaluation alongside weather and human behavior as factors that may contribute to COVID-19 seasonality, and that the relative importance of these drivers requires further investigation. A major challenge to predicting seasonality of infectious diseases are rapid, human-induced changes in the hitherto predictable seasonality of our planet, whose influence we review in a final outlook section. We conclude that a proactive multidisciplinary approach is warranted to predict, mitigate, and prevent seasonal infectious diseases in our complex, changing human-earth system.

Temporal partitioning among diurnally and nocturnally active desert spiny mice: energy and water turnover costs.

Nocturnal Acomys cahirinus and diurnally active A. russatus coexist in hot rocky deserts. Diurnal and nocturnal activity exposes them to different climatic challenges. A doubly-labelled water field study revealed no significant differences in water turnover between the species at all seasons, reflecting the adaptations of A. russatus to water conservation. In summers the energy expenditure of A. russatus tended to be higher than that of A. cahirinus. Energy requirements of A. cahirinus in winter are double than that of A. russatus, and may reflect the cost of thermoregulating during cold nights.

Convergence in morphological patterns and community organization between Old and New World rodent guilds.

We studied morphological relationships within three guilds of gerbillid rodents in Israel. We found a nonrandom pattern of overdispersed means (community-wide character displacement) for upper incisor widths among the species in these three guilds. Upper tooth-row lengths, condylo-basal skull lengths, and tooth-row surfaces displayed similar patterns. We also studied seed-size selection by two well-studied gerbil species, which have previously been found to compete, in order to test whether specializing on husking seeds of different sizes as a mechanism of coexistence may underlie the morphological patterns. The seed-size selection experiments took place in two large aviaries with artificial lighting simulating full-moon nights, which is when predation risk is perceived as high. Seeds of different sizes (commercial seeds in one experiment and husked wheat particles in the other) mixed with sand were offered in trays. The larger Gerbillus pyramidum took significantly larger commercial seeds and marginally larger wheat particles than the smaller Gerbillus allenbyi. The patterns attest to ecomorphological convergence at the guild level; we previously demonstrated size structuring in several North American heteromyid rodent guilds, and we now report similar size structuring among Israeli gerbillid guilds. The occurrence of convergent community structure strongly indicates general rules governing ecological communities or guilds.

Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice.

Diurnally active golden spiny mice (Acomys russatus) and nocturnal common spiny mice (Acomys cahirinus) coexist in hot rocky deserts of Israel. Diurnal and nocturnal activities expose these species to different climatic conditions. Nonshivering thermogenesis (NST) capacity of individuals of both species immediately upon removal from the field exhibited seasonal changes, with no significant interspecific difference. Colony-reared mice of either species transferred in the laboratory from long to short photoperiod increased NST capacity, though to a lesser extent than observed in the seasonal acclimatization. The underlying biochemical mechanisms of short photoperiod acclimation differed between the species. In both Cytochrome-c oxidase (Cox) activity was higher in short as compared to long photoperiod. In short-photoperiod-acclimated A. cahirinus uncoupling protein (UCP) content in brown adipose tissue (BAT) was significantly higher than in long photoperiod, while in A. russatus there was no significant change. In A. russatus there was a significant increase in lipoprotein lipase (LPL) activity in BAT in short-photoperiod-acclimated individuals, while in A. cahirinus LPL activity was high under both acclimations. The low LPL activity in brown adipose tissue of desert-adapted A. russatus may facilitate lipid uptake in white adipose tissue, an advantage in desert conditions where food is scarce and irregularly distributed in space and time.

Hydroquinone antioxidants from the Indian ocean tunicate Aplidium savignyi.

Three hydroquinone compounds have been isolated from the Indian Ocean tunicate Aplidium savignyi. Two are already known: geranylhydroquinone and the 2-(3-hydroxy-3,7-dimethyloct-6-enyl)-1,4-benzenediol as a new stereoisomer 2-(2Z)-(3-hydroxy-3, 7-dimethyloct-2,6-dienyl)-1,4-benzenediol. The structures were determined using spectroscopic data ((1)H NMR, (13)C NMR, MS, UV, and IR). These compounds are potential natural antioxidants.

Differential behavioural and hormonal responses of voles and spiny mice to owl calls.

Rodents usually respond to the presence of owls by reducing overall activity, in particular foraging. In this study, a playback of recorded tawny owl, Strix aluco, calls was sufficient to induce a marked effect in the social (Gunther's) vole, Microtus socialis. Some of the voles exposed to owl calls reduced their activity ('freeze' pattern) unlike control voles exposed to a human voice. Other voles, however, dashed around the cage ('flee' pattern). Owl calls also increased corticosterone levels in the voles, showing that the calls induced stress. We suggest that the behavioural dichotomy to freeze or flee in voles is a result of differences in individual normal behaviour and/or in stimulus interpretation. In the common spiny mouse, Acomys cahirinus, no behavioural changes were detected after exposure to owl calls, despite increased cortisol levels which are indicative of stress. Differences in the habitats of voles and spiny mice may explain the apparent lack of behavioural response in the latter. They are rock-dwelling rodents preferentially foraging between boulders and in rock crevices, where they are relatively protected from aerial predation, whereas voles forage in relatively open spaces. Copyright 1999 The Association for the Study of Animal Behaviour.

Telemetric field studies of body temperature and activity rhythms of Acomys russatus and A. cahirinus in the Judean Desert of Israel.

Two species of the genus Acomys coexist in arid zones of southern Israel. Acomys russatus is distributed in extremely arid areas, while A. cahirinus is common in both Mediterranean and arid regions. Individuals of both species from a rodent community in the Ein Gedi Nature Reserve were implanted with temperature-sensitive transmitters. Body temperature (T b) rhythms were recorded in free-ranging mice at four different seasons of the year. A. cahirinus (30-45 g) showed a nocturnal rhythm of T b throughout the year. In the activity phase during the night T b increased to 38.2°C. During the day T b decreased to 34°C. This species displayed this pattern in summer also when ambient temperatures rose above T b. The T b of A. russatus (45-65 g) varied between 34.8 and 41°C during the hot season, showing a bimodal temperature rhythm with maximal values in the morning and in the evening. Measurements of activity in this species showed inactivity during the hottest period of a summer day. In winter A. russatus showed no clearly detectable diurnal or ultradian rhythm in T b, which remained constant between narrow limits of 35.2 and 36.8°C.

Several new isoprenoids from the soft coral sinularia erecta

Eight compounds were isolated from the Indo-Pacific soft coral Sinularia erecta (Tixier-Durivault, 1945) collected from the lagoon of Mayotte, Comoros Islands, northwest of Madagascar. Four of the compounds, namely the sesquiterpene germacrene D, the diterpenoids nephthenol and decaryiol, and norcembrene, are known. The other four are the new secondary metabolites germacrene E (1), epi-norcembrene (3), and two bis-pukalide diterpenes, mayotolides A and B (4 and 5). The structure of each of the compounds was determined by means of 1D and 2D NMR and MS spectroscopy in addition to some chemical transformations.