(Un‐)expected nocturnal activity in “Diurnal” Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation

Abstract

The ability to operate during the day and at night (i.e., cathemerality) is common among mammals but has rarely been identified in primates. Adaptive hypotheses assume that cathemerality represents a stable adaptation in primates, while nonadaptive hypotheses propose that it is the result of an evolutionary disequilibrium arising from human impacts on natural habitats. Madagascar offers a unique opportunity to study the evolution of activity patterns as there we find a monophyletic primate radiation that shows nocturnal, diurnal, and cathemeral patterns. However, when and why cathemeral activity evolved in lemurs is the subject of intense debate. Thus far, this activity pattern has been regularly observed in only three lemurid genera but the actual number of lemur species exhibiting this activity is as yet unknown. Here we show that the ring-tailed lemur, Lemur catta, a species previously considered to be diurnal, can in fact be cathemeral in the wild. In neighboring but distinct forest areas these lemurs exhibited either mainly diurnal or cathemeral activity. We found that, as in other cathemeral lemurs, activity was entrained by photoperiod and masked by nocturnal luminosity. Our results confirm the relationship between transitional eye anatomy and physiology and 24-h activity, thus supporting the adaptive scenario. Also, on the basis of the most recent strepsirrhine phylogenetic reconstruction, using parsimony criterion, our findings suggest pushing back the emergence of cathemerality to stem lemurids. Flexible activity over 24-h could thus have been one of the key adaptations of the early lemurid radiation possibly driven by Madagascar's island ecology.

Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis

“…We suggest that periods of bulky food intake by bamboo lemurs may require long periods of inactivity to digest dietary fibre. Ultimately, these data provide evidence that despite contrasting gastrointestinal morphologies and dietary adaptations among lemurid species, cathemeral activity provides Ultimate determinants of Hapalemur cathemerality 19 varying adaptive value, as different constraints appear to act simultaneously and/or in different ways depending on the habitat (Curtis and Rasmussen 2006;Donati et al 2013;Tattersall 2008). …”

“…Furthermore, our model revealed that H. meridionalis increased nocturnal activity when there was greater nocturnal luminosity (Eppley et al 2015a). This was not surprising given that moonlight has been shown to be similarly influential to most cathemeral (Charles-Dominique et al 1980;Wright 1989;Curtis et al 1999;Donati et al 2001Donati et al , 2009Donati et al , 2013Fernández- Thermoregulatory strategies appear to be common for many cathemeral non-primate mammals. High ambient temperatures have been shown to constrain diurnal activity in large herbivores, such as Przewalski horse (Equus ferus przewalskii) and eastern grey kangaroos (Macropus giganteus), thus reducing heat stress by remaining in the shade during the hot daytime and increasing nocturnal activity (Clarke et al 1995;Berger et al 1999).…”

“…We considered only full-day focal follows (N = 106) of southern bamboo lemurs, that is, we only included data limited to sessions where the focal subject was observed for ≥80% of the day (i.e., as calculated via available daylight per 24-h period), which constituted >1,206 h. We utilized a diurnal-to-nocturnal activity (DN) ratio so as to allow for comparison across taxa (Donati et al 2013). To determine which factors influenced the DN ratio, we fitted Linear Mixed-effects Models (LMM) in R statistical software (R Development Core…”

“…observ.). Assuming that the ancestral activity pattern of the family Lemuridae is likely to be cathemeral (Curtis and Rasmussen 2006;Tattersall 2008;Donati et al 2013;Eppley et al 2015a;Santini et al 2015), we hypothesize that Hapalemur dietary needs may "mask" cathemerality when heavily feeding on high fibre foods, forcing them to become more monophasic. Also, the need to maintain high foraging efficiency on leaves and grass, food categories more often associated with diurnality in primates, may further explain why bamboo lemurs concentrate activity during daylight hours.…”

“…One haplorhine species, Aotus azarae, regularly displays a cathemeral activity pattern (Fernández-Duque 2003), while the remaining cathemeral primates are limited to the strepsirrhine family Lemuridae, endemic to Madagascar (Donati and Borgognini-Tarli 2006b). While it has been hypothesized that cathemerality in lemurs is the product of a non-adaptive disequilibrium in a transition from nocturnality to diurnality Ultimate determinants of Hapalemur cathemerality 5 enabled by the recent extinction of large diurnal raptors and of competitive lemur species (Martin 1972;van Schaik andKappeler 1993, 1996;Kappeler and Erkert 2003), most evidence lends support for cathemerality likely representing a stable adaptation in lemurs (Curtis and Rasmussen 2006;Kirk 2006;Donati et al 2007aDonati et al , 2009Donati et al , 2013Eppley et al 2015a;Santini et al 2015).…”