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Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: Camera trap data and preliminary behavioral observations
Abstract and Figures
Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered "strictly diurnal". We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010-April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25 % of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5 % of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53 % nighttime, 43 % daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.
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... Lemurs face significant thermal challenges, including daily temperature fluctuations (e.g., Ikeuchi et al., 2005;LaFleur et al., 2014;Rasamimanana et al., 2016), cold winters, especially in the highland rainforests (e.g., Blanco and Godfrey, 2014;Blanco et al., 2017), and extreme heat, most notably in the dry forests of south and southwestern Madagascar (e.g., Jolly et al., 2006;Rasamimanana et al., 2016). Much of the literature on lemur thermoregulation has focused on daily torpor and seasonal hibernation among Cheirogaleids (e.g., Dausmann et al., 2004Dausmann et al., , 2005Blanco et al., 2013Blanco et al., , 2018 as well as responses to low temperatures among lemurs more broadly (e.g., Donati et al., 2011;Chaplin et al., 2014;Kelley et al., 2016;Eppley et al., 2017). ...
... Much of the literature on lemur thermoregulation has focused on daily torpor and seasonal hibernation among Cheirogaleids (e.g., Dausmann et al., 2004Dausmann et al., , 2005Blanco et al., 2013Blanco et al., , 2018 as well as responses to low temperatures among lemurs more broadly (e.g., Donati et al., 2011;Chaplin et al., 2014;Kelley et al., 2016;Eppley et al., 2017). How lemurs cope with high temperatures remains understudied, though some species adopt prone body postures (Eulemur collaris: Donati et al., 2011) or shift to cathemerality (Lemur catta: LaFleur et al., 2014) when temperatures are high. ...
High temperatures pose a significant risk to mammals, especially those living in hot and dry environments such as southern Madagascar, the location of Bezà Mahafaly Special Reserve (BMSR). At BMSR, we observed sifakas (Propithecus verreauxi) hugging tree trunks while resting on the ground during the mid-day heat of the late dry season. These highly arboreal lemurs are more vulnerable to predation on the ground. To explore whether tree hugging affords a thermal advantage, we collected 615.7 hours of behavioral data on sifakas in six groups, together with the temperature of the air, ground, and tree trunks used during hugging bouts. We observed hugging only when ambient temperatures were high (above 30°C), and mean daytime temperature had a significant positive effect on whether sifakas engaged in tree hugging on a given day. The surface at the base of hugged trees were significantly cooler (by ~3-5°C) than ambient air temperatures and surface temperatures further up the trunk, likely enabling animals to dissipate body heat. These data suggest that terrestrial tree hugging behavior contributes to thermoregulation in this lemur population and, coupled with evidence from koalas (Phasocolarctos cinereus), indicate that trees may provide a widespread thermal benefit for mammals facing heat stress. The capacity of sifakas to avoid heat stress will be critical to their persistence under predicted temperature increases in southern Madagascar over coming decades, and needs to be better understood in the context of long-term conservation planning.
... Arboreal lemur species occasionally come to the ground for foraging (Eppley et al., 2016a), sleeping (Eppley et al., 2016b;Ramananjato et al., 2022), and hibernation (Blanco et al., 2013). While a few studies suggested that predation risk influences lemur terrestriality (LaFleur et al., 2014), none to our knowledge have investigated how direct predator presence influences their ground use. Fosa (Cryptoprocta ferox) are the largest native carnivore in Madagascar and prey on a variety of lemur species (Goodman et al., 1997;Hawkins, 1998;Karpanty & Wright, 2007;Lührs & Dammhahn, 2009;Schnoell & Fichtel, 2011); thus, their presence should influence lemur terrestriality. ...
It is thought arboreal species avoid foraging on the ground due to perceived predation risk, making the study of when and where arboreal species use the ground key in understanding foraging versus safety tradeoffs. We used publicly available, opportunistic, camera-trap observations from surveys across Madagascar to examine whether arboreal lemur ground use was spatially and temporally related to fosa (Cryptoprocta ferox), a native predator, and human presence. We observed 14 species of diurnal lemur (n = 287 individual observations) and six species of nocturnal lemur (n = 105 individual observations). With static two-species occupancy models and kernel density estimation, we found diurnal and nocturnal lemur ground use was spatially and temporally related to fosa presence. Diurnal lemurs used the ground less at camera locations where fosa were present compared to camera locations where they were absent, particularly if those camera locations lacked other native carnivores. Nocturnal lemurs used the ground more at camera locations fosa were observed at within the past 5 days compared with camera locations where fosa were not observed at within the past 5 days. Despite humans and diurnal lemurs being active at the same time 80% of the diel cycle (temporal overlap Δ = 0.80; 95% confidence interval [CI]: 0.75–0.85), diurnal lemur spatial or temporal use of the ground and human presence were unrelated. Diurnal lemur temporal overlap with humans at camera locations where fosa were uncommon was higher (Δ = 0.79; 95% CI: 0.71–0.86) compared with where fosa were common (Δ = 0.57; 95% CI: 0.46–0.66). Future research on how arboreal lemurs navigate ground use in a multipredator landscape should include behavioral observations to better understand animal decision-making.
... In addition, patrol teams in Lomami National Park (LNP) frequently report the lesula's pre-dawn boom calls on listening point surveys, which could suggest activity during crepuscular hours [1,14]. Other studies have used camera traps and satellite telemetry to report activity beyond daylight hours, where fluctuations in food resources, overnight temperature, thermoregulation, or predation threats play a role in activity patterns of mammals [15][16][17][18]. In this study, we assessed lesula captures over a 24 h period to determine if a divergent activity pattern exists in this species (crepuscular or cathemeral). ...
Guenons are the most diverse clade of African primates, and many species living within the core of the Congo Basin rainforest are still understudied. The recently described guenon species, Cercopithecus lomamiensis, known as lesula, is a cryptic, semi-terrestrial species endemic to the central Congo Basin in the Democratic Republic of the Congo. The recent IUCN Red List Assessment recognizes lesula’s risk of extinction in the wild as Vulnerable. The objective of our study was to use camera traps to expand knowledge on the behavioral ecology of lesula. We conducted three systematic, terrestrial camera trap (CT) surveys within Lomami National Park and buffer zone (Okulu: 2013; Losekola: 2014; E15: 2015). We accumulated 598 independent events of lesula over 5960 CT days from 92 CTs. Typical of Cercopithecus species, camera trap videos reveal that lesula has a diurnal activity pattern, birth seasonality, a group size of up to 32 individuals, and social organization with female philopatry and male dispersal. Results also suggest that lesula are highly terrestrial, distinguishing them from other Cercopithecus species, which are mostly arboreal. Our study provides new information about the behavioral ecology of this little-studied primate, generating species-specific knowledge of a threatened species for successful conservation planning.
... At Berenty Reserve, the average group size is between 12 and 16 noninfant individuals, depending on location and provisioning within the reserve; groups tend to fission between 21 and 25 individuals (Jolly et al. 2002;Pride 2005). Smaller populations, such as the ring-tailed lemurs of the Tsimanampetsotsa spiny forest, have similar ranges of nine to 14 adult individuals (LaFleur et al. 2014). Furthermore, ring-tailed lemur populations have experienced a notable decline in recent decades, which can lead to smaller, more-fragmented social groups (Gould and Sauther 2016;LaFleur et al. 2016LaFleur et al. 2018. ...
Primate species exhibit considerable variation in behavior and outcomes during intergroup encounters (IGEs). Social group characteristics, like group size, and individual traits, such as sex, rank, and reproductive status, within those groups can influence both IGE engagement and outcomes. To better understand the impact of group heterogeneity on IGEs, we must examine individual strategies to elucidate individual costs and benefits of engaging in these interactions. Here, we present a descriptive study of the IGEs between two small social groups of ring-tailed lemurs (Lemur catta) on St. Catherines Island, GA, USA. We distinguish between dyadic and multiple-individual interactions between groups to compare collective and individual agonistic engagement. All encounters occurred when the East Road group (N = 7 individuals) traveled from the center of their home range to the boundary with Windmill group's (N = 5 individuals) home range, indicating that East Road might have been actively testing this boundary for access to food resources, sleeping trees, and mating opportunities. We also found notable individual variation in participation during IGEs. The daughters of the highest-ranking females were the most-engaged in dyadic intergroup and intragroup aggression, had high "win" rates during intergroup dyadic encounters, and engaged in intergroup multiple-individual interactions at high levels. These findings indicate that they might value their home range more as "potential alphas" compared to other group members. Dominant females were the most engaged in multiple-individual interactions, suggesting that they contribute heavily to collective action that might result in a gain or loss of access to resources. Finally, these two small groups might be equally matched despite the two-individual group size disparity due to individual free-riding strategies. Future research should focus on individual strategies during IGEs to characterize the complex decisions and trade-offs that influence participation.
... Cathemerality is considered as one of the lemurs' unusual traits compared to other primates (Wright, 1999). Among the five extant genera of the Lemuridae family, cathemeral activity patterns have been routinary observed in Hapalemur spp., Eulemur spp., Lemur catta, and Prolemur simus (Tan, 1999;Donati et al., 2009Donati et al., , 2013LaFleur et al., 2014;Eppley et al., 2015). Recent studies based on data from accelerometers also revealed that southern woolly lemur Avahi meridionalis, previously thought to be strictly nocturnal, exhibits low but consistent bouts of diurnal activity (Campera et al., 2019). ...
This study provides new findings on the flexible activity of Prolemur simus in an anthropogenically modified habitat in the rural commune of Tsaratanana, eastern Madagascar. Based on camera-trap data, we compared the temporal distribution of activity of one group of lemurs between the forest edge and the forest core. We also investigated the possible influence of nocturnal luminosity on the activity cycle. The analysis was conducted using Kernel Density estimates and the R package OVERLAP. The distribution across the 24-h cycle confirmed that Prolemur simus is cathemeral in the wild. The lemurs displayed three peaks of activity: one during the night and two coinciding with morning and evening twilights. The highest proportions of nocturnal activity occurred at the forest edge and at low moon luminosity suggesting a possible anti-predator and/or human-avoidance strategy. The flexible activity of Prolemur simus may contribute to the tolerance of this Critically Endangered species to anthropogenic disturbance.
... Arboreal camera trapping has been implemented successfully to obtain information about mammal community diversity (Bowler et al. 2017), individual behavior (Bezerra et al. 2014;LaFleur et al. 2014;Oliveira-Santos et al. 2008), as well as monitoring the effectiveness of canopy bridges or rope overpasses to restore habitat connectivity (Gregory et al. 2017;Teixeira et al. 2013). In addition, comparisons between arboreal and ground-level camera trapping, as well as between arboreal camera trapping and more traditional census transects, have revealed greater effectiveness of the former for surveying canopy wildlife, especially due to its effectiveness in recording nocturnal or cryptic arboreal mammal species (Bowler et al. 2017;Haysom et al. 2021;Moore et al. 2020;Whitworth et al. 2016). ...
Canopy camera trapping is being increasingly used to characterize assemblages of arboreal mammals. In this study we compared, for the first time, the assemblage of arboreal mammals of the Atlantic Forest, surveyed using canopy camera trapping at two protected areas of Mis-iones, Argentina: Piñalito (11 camera-trap stations) and Cruce Caballero (9 stations), with the assemblage recorded at ground-level with a camera-trapping survey conducted at another protected area, the nearby private reserve Valle del Alegría (18 stations). We calculated the number of independent photo-events for each species and site, and we built species rank abundance curves to compare the recorded species diversity among sites. We recorded six mammal species at Piñalito and Cruce Caballero, and 23 at Valle del Alegría. Canopy-survey sites showed lower diversity but a different and non-nested species composition when compared to the ground-level survey. One of the most frequently recorded species in the canopy, the brown-eared woolly opossum, Caluromys lanatus, categorized as Vulnerable in Argentina, has not been photographed in ground-level camera-trap surveys in Misiones before. Our results suggest that canopy camera trapping represents a robust method to sample arboreal species that are missed in ground-level camera-trap surveys, thus improving forest species inventories.
... Several primate species living in much smaller groups sometimes travel on the ground at night (Hanya et al. 2018;Tagg et al. 2018), so it is surprising that the large mandrill groups totally avoided terrestrial movement at night, although they may be active in the trees (Mochida and Nishikawa 2014). Nocturnal ground movement is also reported in wild ring-tailed lemurs (Lemur catta)-a smallersized primate living in smaller groups than mandrills (LaFleur et al. 2014). Although mandrills are known prey of leopards (Panthera pardus) and central African pythons (Python sebae) (Henschel et al. 2011;Abernethy and White 2013), it is questionable whether this avoidance of nocturnal movement can be solely explained by predator avoidance. ...
Movement is a fundamental characteristic of animals, but challenging to measure noninvasively. Noninvasive methods for measuring travel have different weaknesses, so multiple techniques need to be applied multiple techniques for reliable inferences. We used two methods, direct tracking and camera trapping, to examine the variation in time and seasonal differences in movement rates of mandrills (Mandrillus sphinx), an elusive primate that lives in large groups in central Africa. In a 400-km 2 rainforest area in Moukalaba-Doudou National Park, Gabon, we tracked unidentified groups 46 times from 2009 to 2013. We systematically placed 157 terrestrial camera traps in the same area from 2012 to 2014 and recorded groups 309 times. Generalized additive mixed models (GAMMs) of the tracking data indicated that the group travel speed varied with time and season. In the fruiting season, the movement rate fluctuated with time in a bimodal pattern, whereas in the nonfruiting season, it increased monotonously with time. The predicted day range was longer in the fruiting season (6.98 km) than in the nonfruiting season (6.06 km). These seasonal differences suggest responses to changes in food resources and temperature. Camera-trap detection rates showed similar temporal and seasonal patterns to the tracking data, allowing us to generalize our findings to the population level. Moreover, cameras never detected mandrills at night, and we observed that they slept high in trees and hardly moved until the next morning, all suggesting their strict avoidance of nighttime movement. This study demonstrated the significance of the multiple-method approach in drawing robust conclusions on temporal patterns of animal movement.
Background
This study aimed to document normal ophthalmic findings and ocular anomalies in captive ring-tailed lemurs (Lemur catta) and to establish reference intervals for the Schirmer tear test-1 (STT) and intraocular pressure (IOP).
Methods
Sixty healthy adult lemurs (22 females, 38 males) aged from 6 months to 28 years underwent ophthalmic examination. Direct illumination, STT, diffuse and slit-lamp biomicroscopy, fluorescein dye test, IOP measurement, and indirect ophthalmoscopy were performed on each eye. Reference intervals were calculated non-parametrically for STT and IOP. The eyes of three lemurs, which had died from unrelated reasons, were examined histopathologically.
Results
The median STT in the lemurs was 9 mm/min, with an estimated 95% reference interval of 2 to 15 mm/min. The median IOP was 18 mmHg, with an estimated 95% reference interval of 11 to 24 mm Hg. Ophthalmic abnormalities were noted in 21 out of 120 (17.5%) eyes, including third eyelid laceration, corneal leucoma, cataracts, chronic uveitis, and vitreous degeneration.
Conclusions and clinical relevance
Reference intervals of physiological ophthalmic parameters and the most common ophthalmic findings are defined and can be useful for clinical veterinarians during the eye examinations of ring-tailed lemurs.
Environmental enrichment is a management tool used to promote positive animal welfare by stimulating species-specific behaviors and providing animals with opportunities to exert choice and control over the environment. Our study aimed to evaluate the combined effect of three enrichment types and environmental/individual factors (i.e., individual age and rank position) on the behavior of six adult Lemur catta hosted at Pistoia Zoo (Italy). We collected data from June to September 2013 using a within-subject experimental design consisting of five conditions: Baseline, Food-based enrichment, Physical enrichment, Auditory enrichment and No enrichment provided. We conducted six 30-minute observation sessions per sampling day (total = 107 h). We recorded the animals’ behavior via 2-minute focal animal sampling per individual per observation period and analyzed data with Generalized Linear Models. The study group only performed normal species-specific behaviors. Enrichments decreased stress-related behavioral patterns, whereas environmental and individual factors influenced the other recorded behaviors. Our study confirmed the usefulness of employing an integrated methodological approach to enrichment assessment for enhancing captive lemur care.
Compared to other primate taxa, hand preference in strepsirrhines has been poorly investigated and the available studies have often produced conflicting results. Thanks to their remarkable plasticity in foraging and postural habits, ring-tailed lemurs (Lemur catta) represent a key model species to examine manual lateralisation. We video-recorded 23 individuals hosted at four Italian zoological gardens during three food-related trials requiring different kinds of manual actions. We found a remarkable hand preference at individual level for grasping static food presented in a bowl, both when only one kind of food was offered (“food limited-choice” task) and when a mix of less and more palatable food items were available (“food large-choice” task). Conversely, most individuals did not show any hand preference for catching highly palatable food in motion (“catching” task). Moreover, the subjects not showing any hand preference engaged more frequently in bimanual actions (concurrent and symmetric use of both hands in catching food) than the subjects displaying a manual asymmetry. No detrimental effect on the task performance was recorded, indicating a high level of hand selection plasticity in Lemur catta. In conclusion, our findings show that ring-tailed lemurs can take advantage from a flexible manual strategy and highlight how ecological factors must be carefully evaluated when assessing hand preference in extant strepsirrhines.
This chapter looks in detail at the relationship between group size and antipredator behaviors. Results indicate predator pressures affects foraging locations, with smaller groups avoiding potential predator "hot spots", e.g. terrestrial foraging, when compared to larger groups. Small groups also formed more mixed species associations with sifaka when both species' infants were more vulnerable. Larger groups exhibited fewer examples of predation sensitive foraging, and even engaged in behaviors that resulted in greater fruit feeding but also more predator encounters. Primates must balance anti-predator responses with foraging and social needs and as such, group size becomes an important variable.
Habitat characteristics represent the matrix for the evolution of morphological, physiological and behavioural adaptations and life history traits of animals. These include bottom-up factors (such as distribution and abundance of food) and top-down constraints (such as protection from predators). The role of different habitat components in the survival and reproduction of individuals is of prime interest and is relevant for evolutionary understanding as well as for primate conservation. So far, this has been studied by linking habitat characteristics with phenotypic traits of animals, assuming that these traits represent adaptation to a given habitat constraint. However, we should bear in mind that the characteristics we observe today may represent adaptations to constraints that acted in the past (the Epaminondas effect, named after the little boy who always did the right thing for the previous situation; or, in evolutionary terminology: animals are tracking fitness optima by trying to climb the sides of shifting adaptive peaks, Cody, 1974). However, testing hypotheses based on these ‘ghosts of past constraints’ has so far been impossible.
Although the behaviour and ecology of primates have been more thoroughly studied than that of any other group of mammals, there have been very few attempts to compare the communities of living primates found in different parts of the world. In Primate Communities, an international group of experts compares the composition, behaviour and ecology of primate communities in Africa, Asia, Madagascar and South America. They examine the factors underlying the similarities and differences between these communities, including their phylogenetic history, climate, rainfall, soil type, forest composition, competition with other vertebrates and human activities. As it brings together information about primate communities from around the world for the very first time, it will quickly become an important source book for researchers in anthropology, ecology and conservation, and a readable and informative text for undergraduate and graduate students studying primate ecology, primate conservation or primate behaviour.
Predator sensitive foraging represents the strategies that animals employ to balance the need to eat against the need to avoid being eaten. Ecologists working with a wide range of taxa have developed sophisticated theoretical models of these strategies, and have produced elegant data to test them. However, only recently have primatologists begun to turn their attention to this area of research. This volume brings together primary data from a variety of primate species living in both natural habitats and experimental settings, and explores the variables that may play a role in primates' behavioural strategies. Taken together, these studies demonstrate that predator sensitive foraging is relevant to many primates, of various body sizes and group sizes and living in different environments. Eat or be Eaten encourages further discussion and investigation of the subject. It will make fascinating reading for researchers and students in primatology, ecology and animal behaviour.
The last decade's lemur research includes successes in discovering new living and extinct species and learning about the distribution, biogeography, physiology, behavior, and ecology of previously little-studied species. In addition, in both the dry forest and rain forest, long-term studies of lemur demography, life history and reproduction, have been completed in conjunction with data on tree productivity, phenology, and climate. Lemurs contrast with anthropoids in several behavioral features, including female dominance, targeted female-female aggression, lack of sexual dimorphism regardless of mating system, sperm competition coupled with male-male aggression, high infant mortality, cathemerality, and strict seasonal breeding. Hypotheses to explain these traits include the "energy conservation hypothesis" (ECH) suggesting that harsh and unpredictable climate factors on the island of Madagascar have affected the evolution of female dominance, and the "evolutionary disequilibrium hypotheses" (EVDH) suggesting that the recent megafauna extinctions have influenced lemurs to become diurnal. These hypotheses are compared and contrasted in light of recent empirical data on climate, subfossils, and lemur behavior. New data on life histories of the rain forest lemurs at Ranomafana National Park give further support to the ECH. Birth seasons are synchronized within each species, but there is a 6-month distribution of births among species. Gestation and lactation lengths vary among sympatric lemurs, but all lemur species in the rain forest wean in synchrony at the season most likely to have abundant resources. Across-species weaning synchrony seen in Ranomafana corroborates data from the dry forest that late lactation and weaning is the life history event that is the primary focus of the annual schedule. Lemur adaptations may assure maximum offspring survival in this environment with an unpredictable food supply and heavy predation. In conclusion, a more comprehensive energy frugality hypothesis (EFH) is proposed, which postulates that the majority of lemur traits are either adaptations to conserve energy (e.g., low basal metabolic rate (BMR), torpor, sperm competition, small group size, seasonal breeding) or to maximize use of scarce resources (e.g., cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony). Among primates, the isolated adaptive radiation of lemurs on Madagascar may have been uniquely characterized by selection toward efficiency to cope with the harsh and unpredictable island environment. (C) 1999 Wiley-Liss, Inc.
For Lemur catta at Berenty Reserve in southern Madagascar, birth corresponds to the early wet season, lactation to the wet season, estrus to the early dry season, and gestation to the dry season, with marked differences in food available to females in each physiological state. Feeding behavior, food availability and palatability were compared in two L. catta troops living in different parts of the reserve over a 20-month period. Troop H’s territory included many introduced tree species and access to tounsts’ bananas. Troop F lived in natural gallery forest far from the tourist circuit. Troop H ate more food items, from more species, was predominantly folivorous throughout the year and showed less change in diet and activity from season to season. Troop F ate less, from fewer plant species, reduced both activity and dietary diversity markedly in the dry season and was seasonally more fntgivorous than folivorous. Activity, dietary selectivity, and “snacking” during the birth season may function to maximize energy gain. There are indications of need to balance dietary components, but quantity of foodstuffs may be more important to this adaptable species. Troop F’s more limited natural diet did not translate into lower reproductive success because it increased by 50%, while Troop H increased by 17% in size.