Motion cues increase focused attention towards purely visual stimuli in a nocturnal primate and drive stimulus interaction and approach/avoidance in a context-dependent manner.

Visual information is of pivotal ecological importance to monkeys, apes, and humans, whereas its role in nocturnal primate ecology is less well understood. We explored how purely visual information modulates the behavior of a nocturnal primate. Abstract (shape), photographic (shape + detail), or video (shape + detail + motion) representations of arthropod prey (Zophobas morio; food context) or a male conspecific (social context) were systematically presented to 22 individuals of the gray mouse lemur (Microcebus murinus) using a touchscreen. We assessed stimulus-directed touch interactions, durations of focused visual attention towards the different stimuli, and durations spent in the half of the setup-chamber more distant to the touchscreen (as quantification of approach/avoidance). Focused attention towards the stimulus generally increased from abstract and photographic to videographic stimuli. For the food context, indications for a parallel increase in stimulus-directed touch interactions from abstract stimulus to video were found. Approach/avoidance was independent of the stimulus type within both contexts. A comparison between the contexts under the video condition revealed higher durations of visual attention and lower stimulus avoidance in the food context compared to the social context. The number of touch interactions with the video stimulus was not generally context-dependent, but context-dependency related to sex: In the food context, animals with high and low numbers of touch interactions were equally distributed across sexes. In the social context, females showed the highest numbers of touch interactions. Numbers in males declined compared to the food context. Our results demonstrate for the first time that purely visual information modulates mouse lemur behavior and focused attention in a content- and context-specific manner, suggesting that vision is of high importance for the ecology of these nocturnal primates. The findings emphasize the need for further vision-based experiments to gain deeper insight into the evolution of visual information processing and cognition in nocturnal primates.

Enter the Matrix: Use of Secondary Matrix by Mouse Lemurs.

Madagascar is home to many threatened and endemic primate species, yet this island has seen dramatic declines in lemur habitat due to forest loss. This forest loss has resulted in an increasingly fragmented forest landscape, with fragments isolated from each other by grasslands (i.e., matrix). The grassland matrix is not entirely homogeneous containing matrix elements such as isolated trees and shrubs and linear features such as drainage lines. Because most lemurs are predominantly arboreal, they may preferentially use matrix elements to facilitate dispersal between fragments for access to mates or reduce feeding competition, allowing gene flow between fragments of habitat. Therefore, it is important to understand to what degree they use the matrix. We investigated matrix use in two mouse lemurs, the grey mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (Microcebus ravelobensis) in a fragmented landscape in northwest Madagascar. We tested the predictions that: (1) lemurs use matrix less often than forest fragments, (2) if they use the matrix, then they will preferentially use matrix elements compared to grassland, and (3) M. murinus will disperse into the matrix further than M. ravelobensis. In 2011, we visually surveyed line transects in four areas containing matrix elements and four adjacent forest fragments during nocturnal walks. In 2017, we set up traplines in four areas of the matrix containing matrix elements, three areas that were grassland, and six traplines in adjacent fragments. We compared the relative abundance of mouse lemurs in matrix transects to fragmented forest transects, and the relative abundance of captured lemurs in matrix elements, grassland, and fragment traplines. We found that encounter rates of mouse lemurs did not significantly differ between the matrix and fragmented forest transects or traplines. Our sample size was too low to determine if the mean distance from the forest was greater for either Microcebus spp. Our study highlights that mouse lemurs do use matrix elements and there may be interspecific differences in use. Further research is needed to confirm species-specific matrix use, why mouse lemurs use matrix, and how much matrix elements facilitate movement for each species in fragmented landscapes.

The Influence of Seasonal Availability of Young Leaves on Dietary Niche Separation in Two Ecologically Similar Folivorous Lemurs.

Traditional socio-ecological models consider that folivorous primates experience limited feeding competition due to the low quality, high abundance, and even distribution of leaves. Evidence from several folivorous species that experience similar constraints to frugivores does not support this hypothesis. The sympatric lemur genera Avahi (Indriidae) and Lepilemur (Lepilemuridae) are good models to understand how food availability constrains folivores since they are both nocturnal, folivorous, and have a comparable body mass. Here we investigate how two nocturnal folivorous primates, Avahi meridionalis and Lepilemur fleuretae, living in the lowland rain forest of Tsitongambarika, South-East Madagascar, partition their dietary niche and are influenced by seasonality of young leaves. To account for food availability, we collected annual phenological data on 769 trees from 200 species. We also collected behavioural data on 5 individuals per lemur species from August 2015 to July 2016 via continuous focal sampling. We found the phenological profile to be seasonal with peaks of leaf flushing, flowering, and fruiting occurring in the austral summer. The two species showed limited dietary overlap (37% rich period, 6% lean period), and A. meridionalis showed higher feeding time and longer daily distances travelled during the rich period. Lepilemur fleuretae showed a dietary shift during the lean period, relying more on mature leaves (73.3% during the lean period, 13.5% during the rich period) but maintaining similar activity levels between seasons. The time spent feeding on food items by A. meridionalis was positively correlated with the nitrogen content and negatively correlated with polyphenols during the rich period. We highlighted a clear effect of the seasonality of young leaves on the diet, nutritional content, activity patterns, and daily distances travelled by two folivorous species, which can be linked to nutrient balancing and time-minimising versus energy-maximising strategies.

Sahamalaza Sportive Lemur, Lepilemur sahamalaza, Vocal Communication: Call Use, Context and Gradation.

Stereotypical vocalisations can facilitate long-distance communication in dense and, thus, sound-degrading forest habitats. Despite this, primate vocal repertoires often also include gradations between different call types that are used in social interactions. Because many nocturnal primates show a solitary social structure, it has been difficult to assess the role vocalisations play in mediating their social encounters. Here we aim to expand on the call types of Sahamalaza sportive lemurs, Lepilemur sahamalaza, as well as investigate their variability and use in social contexts. Through long-term behavioural observations with concurrent recording of vocalisations of known and unknown individuals between 2015 and 2016, we described three previously unrecorded calls and expanded the vocal repertoire to 12 different call types that were used in both targeted social and broadcast solitary contexts. Linear discriminant function and cluster analysis supported initial observations that vocalisations within call types were variable and that at least two call types can be classified as "graded," contrary to expectations. Despite variations in call-context connections, no clear patterns of call use could be established. However, measurable differences in vocal behaviour between the seasons and the sexes indicate that calling is used in a reproductive context, similar to other nocturnal and diurnal primates.

Vocal Repertoire and Intraspecific Variation within Two Loud Calls of the Small-Eared Greater Galago (Otolemur garnettii) in Tanzania and Kenya.

Vocal repertoires and call structure can provide insights into the behaviour and evolution of species, as well as aid in taxonomic classification. Nocturnal primates have large vocal repertoires. This suggests that acoustic communication plays an important role in their life histories. Little is known about the behavioural context or the intraspecific variation of their vocalisations. We used autonomous recording units and manual recorders to investigate the vocal behaviour and structure of loud calls of the small-eared greater galago (Otolemur garnettii)in Kenya and Tanzania. We describe the vocal repertoire, temporal calling patterns and structure of 2 loud calls of 2 subspecies: O. g. panganiensis and O. g. kikuyuensis. We found considerable intraspecific structural differences in both loud calls. These are congruent with the current subspecies classification. Differences in vocalisations among populations are not consistent with the "acoustic adaptation hypothesis," rather they are likely a result of geographic variation due to isolation caused by vegetational barriers in southern Kenya.

Allogrooming in Male-Female Pairs of Captive Owl Monkeys (Aotus nancymaae).

Owl monkeys (Aotus spp.) are socially monogamous, yet allogrooming is reported to be rare. Because Aotus are nocturnal and arboreal, allogrooming is difficult to observe in natural settings. We observed 21 male-female pairs of captive Aotus nancymaae during 2 nonconsecutive study periods in order to describe the details of allogrooming between mates (partner grooming). We found that grooming bouts are brief and consist of tugging the hair or skin with flexed fingers and/or the mouth. Males groomed females most often, and their rates of partner grooming were negatively related to age. Partner grooming occurred regardless of mating behavior. Camera trap data revealed that the rate of partner grooming (1.50 bouts/h) is greater than that recorded from our direct observations in the early evenings (0.51 bouts/h, in 2013; 0.37 bouts/h in 2003) given that most bouts occurred later in the night. A positive relationship between the rates of the parents' partner grooming and those of their offspring later in life suggests intergenerational transmission. This relationship is influenced by the fathers' rates of partner grooming. We conclude that allogrooming in Aotus is a normal part of their behavioral repertoire that likely serves social functions similar to those in other pair-bonded primates.

Niche partitioning and environmental factors affecting abundance of strepsirrhines in Angola.

The African nocturnal primates (galagos, pottos, and angwantibos: suborder Strepsirrhini) are the result of the first major primate radiation event in Africa, and are found in different primate communities spread across the entire sub-Saharan Africa. Thus, they represent an interesting group of taxa to investigate community strategies to avoid interspecific competition. Here, we present the result of the first study on nocturnal primate communities in western Angola. We aimed to identify habitat factors influencing strepsirrhine abundance, collect evidence of spatial niche segregation, and discuss possible indications of competitive exclusion in this region. We conducted nocturnal surveys at four study sites: Kumbira, Bimbe, Northern Scarp, and Calandula. At each encounter we recorded species, group size, height of animals above ground, and GPS location. We sampled vegetation using the point-centered quarter method and collected data on canopy cover, disturbance, and undergrowth density. We observed a total of five strepsirrhine species with varying community structures. We did not encounter Galagoides thomasi but we recorded a new species Galagoides sp. nov. 4. Levels of disturbance, canopy cover and undergrowth density were the habitat factors that most influenced variation in abundance of Galagoides demidovii and Perodicticus edwardsi, the latter also preferring the habitat with higher tree density. Vertical separation between sympatric strepsirrhines was strongest in Northern Scarp, where overall relative abundance was also highest. Competitive exclusion between G. thomasi and G. sp. nov. 4 may explain why the former was not present within the Angolan Escarpment sites. We observed coexistence between mainly allopatric Otolemur crassicaudatus and P. edwardsi in Kumbira, and of Galago moholi and G. demidovii in Calandula. Both unusual combinations showed some levels of spatial segregation. Habitat characteristics of the Escarpment region are likely to allow for unique nocturnal primate species assemblages. We urge immediate conservation interventions in the Angolan Escarpment.

From masks to muscles: Mapping facial structure of Nycticebus.

Facial musculature in mammals underlies mastication and nonverbal communicative facial displays. Our understanding of primate facial expression comes primarily from haplorrhines (monkeys and apes), while our understanding of strepsirrhine (lemurs and lorises) facial expression remains incomplete. We examined the facial muscles of six specimens from three Nycticebus species (Nycticebus coucang, Nycticebus javanicus, and Nycticebus menagensis) using traditional dissection methodology and novel three-dimensional facial scanning to produce a detailed facial muscle map, and compared these results to another nocturnal strepsirrhine genus, the greater bushbaby (Otolemur spp.). We observed 19 muscles with no differences among Nycticebus specimens. A total of 17 muscles were observed in both Nycticebus and Otolemur, with little difference in attachment and function but some difference in directionality of movement. In the oral region, we note the presence of the depressor anguli oris, which has been reported in other primate species but is absent in Otolemur. The remaining muscle is a previously undescribed constrictor nasalis muscle located on the lateral nasal alar region, likely responsible for constriction of the nares. We propose this newly described muscle may relate to vomeronasal organ functioning and the importance of the use of nasal musculature in olfactory communication. We discuss how this combined methodology enabled imaging of small complex muscles. We further discuss how the facial anatomy of Nycticebus spp. relates to their unique physiology and behavioral ecology.

Population Abundance and Density Estimates of Poorly Documented Near-Threatened Calabar Angwantibo (Arctocebus calabarensis) in Oban Hills Region.

Population abundance and density estimates play important roles in biodiversity conservation assessment and can lead to prioritization of conservation efforts, strategies, and management. The Calabar angwantibo (Arctocebus calabarensis) is a poorly studied, Near-Threatened nocturnal, arboreal mammal species occurring only in the lowland moist tropical rainforest blocks of southeastern Nigeria and southwestern Cameroon. Like other arboreal nocturnal mammals, there are gaps in knowledge of the distribution and abundance of this species, which may be facing population declines due to habitat loss and hunting. In this study, we investigated the abundance and density of A. calabarensis in the Oban Hills Region of Nigeria. We conducted systematic distance sampling survey along 32 transects in different habitats in a 1227 km of survey efforts. A total of 41 sightings of A. calabarensis were detected, resulting in an abundance of 7345 individuals (95% CI = 1.51-4.37) with an estimated density of 2.57 animals/km2. The estimated population abundance is 6515 individuals in closed-canopy forests and 830 individuals in secondary forests, with encounter rates of 0.52 individual/km2 and 0.60 individuals/km2 in the closed canopy and secondary forest habitats. The global estimates encounter rate of A. calabarensis across the habitat types is 0.33 individuals/km2 and population abundance of 4456 individuals. Our findings indicate that the A. calabarensis populations can adapt to low changes in forest habitat modifications resulting from increasing and widespread forest disturbance by human-dominated activity, which is giving way to forest clearance for agriculture cultivation and infrastructural development. Our findings help to fill a knowledge gap regarding this species and may help establish a baseline for future management, population monitoring, and conservation of the cryptic population of A. calabarensis in Cross-Sanaga Forests.

Social Behavior of a Reproducing Pair of the Philippine Tarsier (Tarsius syrichta) in Captivity.

Social interactions of the nocturnal primates are not well studied. One of the species for which social behavior is scarcely known is the Philippine tarsier (Tarsius [= Carlito] syrichta). We observed a reproducing pair of captive individuals over two mating seasons for two consecutive years. The tarsiers spent approximately 4% of their activity budget on social interactions; ca. 20% of time in 0-1 m proximity to each other; and shared sleeping sites for half of the study time. The majority of the animals' social interactions were peaceful: affiliative and sexual (83%), and the smallest component of the behavior was agonistic (17%). We witnessed two copulation events (one per estrus day), each lasting ca. 5 min, and both occurring just after waking. We revealed temporal - nightly and hourly - fluctuations in the frequency of social interactions, in the distances the individuals spent from each other and in the number of vocalizations. The results present the first assessment of the social behavior of the Philippine tarsier, much needed to improve the captive breeding management for this highly sensitive species threatened with extinction.

Urbanisation as an important driver of nocturnal primate sociality.

Urbanisation is an important factor driving species and biodiversity decline. Although habitat alterations can be detrimental for species, studies have shown that many diurnal primates are able to adapt to novel environments. Little is known about the ability of nocturnal primates to survive within an urban environment. To increase our understanding on this topic, we present ad libitum observations on group movement and sociality from urban and rural populations of the African lesser bushbaby (Galago moholi) in South Africa from 2014-2018. Our data show considerable changes in the social dynamics within urban bushbaby populations. In contrast to rural individuals, which spent the majority of their activity period solitarily or in pairs, urban individuals displayed a larger degree of sociality throughout their active period, forming groups of up to ten individuals. Furthermore, urban individuals spent less time moving around, while increasing social (communication/pair-grooming), foraging and feeding behaviour. Urban individuals fed on a range of different anthropogenic and natural food sources (insects/tree gum/nectar) compared to their rural counterparts. In summary, urban bushbabies showed a large degree of behavioural plasticity, with changes in social dynamics and structure frequently observed. Such alterations in sociality, along with the ability to utilise different feeding resources, may explain the ability of the species to survive within a highly altered environment.