Cathemerality in a small, folivorous primate: proximate control of diel activity in Hapalemur meridionalis

Abstract

A non-adherence to a strict diurnal or nocturnal activity cycle is prevalent among mammals, including taxa of Lemuridae, but rare among other primates. While nonmutually exclusive ecological hypotheses attempted to explain the evolution of this activity, termed cathemerality, as either an old or a recent phenomenon, the scarcity of systematic data collected over 24 h limits our potential to explore its proximate and ultimate determinants. Among strepsirrhines, systematic studies involving only two lemurid genera (Eulemur and Lemur) have recorded this activity pattern, while fewer quantitative observations are available for other taxa. If cathemerality could be shown in most members of Lemuridae despite their different ecological adaptations, this would support the hypothesis that this trait is basal and appeared early during lemurid evolution. Here, we investigated whether the folivorous southern bamboo lemur (Hapalemur meridionalis) exhibits cathemeral activity, and determined which environmental factors influence its pattern. We deployed ten archival tags across four social groups to continuously record activity data over a 15-month period. This allowed us to generate a diurnal/nocturnal (DN) ratio for each 24-h period and assess their diel activity. Our data suggest that southern bamboo lemurs are cathemeral within Mandena; while climatic factors showed no influence, nocturnal activity increased with greater nocturnal luminance. Despite contrasting dietary niches, visual morphologies, and body sizes between Hapalemur, Eulemur, and Lemur, all three exhibit cathemerality and lunarphilia. The close phylogenetic proximity of these lemurids supports this flexible activity pattern as an ancestral trait that likely dates to the origin of the Lemuridae radiation.

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

“…For the purpose of this study, however, the data are limited to collared adult individuals from January -December 2013, as this period corresponds to our behavioural observations. Capture and anaesthesia procedures have been previously described in Eppley et al (2015a). Seven of these individuals were recaptured following the same procedures and data were retrieved manually from the tags.…”

“…From these information we were able to calculate both daylength (h) and astronomical twilight (-18° below horizon; Erkert 2011; Eppley et al 2015a). We then generated a nocturnal luminosity index (NL) through indirect evaluations of moon phase and transit times using the geographic coordinates of Mandena via an ad hoc program, Moon Ultimate determinants of Hapalemur cathemerality 9 v.2.0 (Curtis et al 1999), allowing us to estimate the amount of lunar light available over the course of a specific night.…”

“…In 2013, the mean temperature in Mandena was 22.5°C (monthly mean range: 18.5 -26.7°C), displaying an absolute range between 9.5 -35.0°C (Eppley et al 2016b). Precipitation (mm) was measured daily at 6:00h using a rain gauge placed within the study site (Eppley et al 2015a). …”

“…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).…”

“…In fact, several studies of frugivorous primates, e.g., Eulemur rubriventer (Overdorff 1988), E. fulvus mayottensis (Tattersall 1979;Tarnaud 2006), and E. collaris (Donati et al 2007a(Donati et al , 2009), have linked diel activity to dietary changes and fibrous food, such as leaves (Donati et al 2016). However, recent evidence of a diel activity pattern in a folivorous primate, the southern bamboo lemur Hapalemur meridionalis (Eppley et al 2015a), adds a layer of complexity surrounding this potential ultimate determinant of lemurid cathemerality. The gastrointestinal tract of these relatively small mammals includes an enlarged, sacculated caeco-colon, which assists in their elevated ability to digest fibre (Martin 1990;Overdorff and Rasmussen 1995;Campbell et al 2004), allowing for leafy material to be fermented by symbiotic gut microbes across an average food-transit time of 18-36 h, as measured in a closely-related species (Fidgett et al 1996;Campbell et al 2000Campbell et al , 2004Perrin 2013).…”