Impact of weather conditions,seasonality and moonlight on the use of artificial canopy bridges by nocturnal arboreal mammals

Natural and artificial canopy bridges can be used to mitigate the effects of habitat fragmentation. Understanding the ecological factors that influence bridge use is imperative to the effective design and placement of this potential conservation intervention. Moonlight, seasonality and weather may influence the cost and risk of using bridges, potentially reducing their effectiveness. We installed five artificial waterline bridges and, between 2017 and 2019, monitored via camera trapping their use by Javan palm civets Paradoxurus musanga javanicus and Javan slow lorises Nycticebus javanicus. We used a weather station to record microclimate data (temperature and relative humidity) and calculated the illumination percentage of the moon. We tested the influence of moon luminosity, relative humidity, seasonality (Julian day) and temperature on the frequency of bridge use via Generalised Additive Models. Camera traps captured 938 instances of bridge use by civets, which was significantly lower than the reference value at moon luminosity?>?90%, temperatures?>?20 °C, humidity?>?90%, and during the drier period (May–July). Camera traps captured 1036 instances of bridge use by lorises, which was significantly lower than the reference value during the drier period and higher than the reference value at temperatures?>?20 °C. Lorises showed peaks in bridge use close to sunset and sunrise whereas civets showed peaks around 2 h after sunset and 2 h before sunrise. Our study illustrates the utility of simple-to-construct bridges by two sympatric nocturnal mammals facing severe habitat loss, with bridge use differing between those species according to abiotic factors. In particular, less use by both taxa during the drier season could suggest modifying placement of bridges or providing another intervention during that time. Camera traps were an excellent mechanism to record these differences and to validate the importance of the bridges, including during inclement weather and dark nights, when observations would be more difficult for human observers. By understanding the influence that abiotic factors have on the use of artificial bridges, we can improve bridge placement and construction to encourage use by a variety of species, particularly those threatened by habitat fragmentation.

     

Life in a fragment: Evolution of foraging strategies of translocated collared brown lemurs,Eulemur collaris,over an 18-year period

While the drivers of primate persistence in forest fragments have been often considered at the population level, the strategies to persist in these habitats have been little investigated at the individual or group level. Considering the rapid variation of fragment characteristics over time, longitudinal data on primates living in fragmented habitats are necessary to understand the key elements for their persistence. Since translocated animals have to cope with unfamiliar areas and face unknown fluctuations in food abundance, they offer the opportunity to study the factors contributing to successful migration between fragments. Here, we illustrated the evolution of the foraging strategies of translocated collared brown lemurs (Eulemur collaris) over an 18-year period in the Mandena Conservation Zone, south-east Madagascar. Our aim was to explore the ability of these frugivorous lemurs to adjust to recently colonized fragmented forests. Although the lemurs remained mainly frugivorous throughout the study period, over the years we identified a reduction in the consumption of leaves and exotic/pioneer plant species. These adjustments were expected in frugivorous primates living in a degraded area, but we hypothesize that they may also reflect the initial need to cope with an unfamiliar environment after the translocation. Since fragmentation is often associated with the loss of large trees and native vegetation, we suggest that the availability of exotic and/or pioneer plant species can provide an easy-to-access, nonseasonal food resource and be a key factor for persistence during the initial stage of the recolonization.     

Artificial canopy bridges improve connectivity in fragmented landscapes: The case of Javan slow lorises in an agroforest environment

Canopy bridges are increasingly used to reduce fragmentation in tropical habitats yet monitoring of their impact on the behavior of primates remains limited. The Javan slow loris (Nycticebus javanicus) is endemic to Java, Indonesia, where the species most often occurs in human-dominated, highly patchy landscapes. Slow lorises cannot leap, are highly arboreally adapted, and are vulnerable on the ground. To increase arboreal connectivity, as part of a long-term conservation project in Cipaganti, West Java, we built and monitored seven slow lorises bridges of two types—waterline or rubber—and monitored their use by seven adult individuals from 2016 to 2017. Motion triggered camera traps collected data for 195 ± standard deviation (SD) 85 days on each bridge. We collected 341.76 hr (179.67 hr before and 162.09 hr after the installation of bridges) of behavioral and home range data via instantaneous sampling every 5 min, and terrestrial behavior (distance and duration of time spent on the ground) via all occurrences sampling. We found that slow lorises used bridges on average 12.9 ± SD 9.7 days after their installment mainly for traveling. Slow lorises showed a trend toward an increase in their home range size (2.57 ha before, 4.11 ha after; p = 0.063) and reduced ground use (5.98 s/hr before, 0.43 s/hr; p = 0.063) after implementation of bridges. Although the number of feeding trees did not change, new feeding trees were included in the home range, and the proportion of data points spent traveling and exploring significantly decreased (p = 0.018). Waterline bridges serve a purpose to irrigate the crops of local farmers who thus help to maintain the bridges, and also ascribe value to the presence of slow lorises. Other endemic mammal species also used the bridges. We advocate the use and monitoring of artificial canopy bridges as an important supplement for habitat connectivity in conservation interventions.     

Habitat Degradation and Seasonality Affect Physiological Stress Levels of Eulemur collaris in Littoral Forest Fragments

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.     

Ecological Flexibility as Measured by the Use of Pioneer and Exotic Plants by Two Lemurids: <Emphasis Type="BoldItalic">Eulemur collaris</Emphasis> and <Emphasis Type="BoldItalic">Hapalemur meridionalis</Emphasis>

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal southeastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioral observations between 2011 and 2013 on frugivorous collared brown lemurs (Eulemur collaris) and folivorous southern bamboo lemurs (Hapalemur meridionalis). To estimate the ability of lemurs to use pioneer species, we categorized all plants used for feeding and resting as fast growing, mid-growing, or slow growing. We fitted general linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species (E. collaris and H. meridionalis), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to use secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with that for other primate folivores.     

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments

Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments.     

Ecological and Anthropogenic Correlates of Activity Patterns in <Emphasis Type="Italic">Eulemur</Emphasis>

The ultimate determinants of cathemerality, i.e., activity spread over the 24-h cycle, in primates have been linked to various ecological factors. Owing to the fast rate of habitat modification, it is imperative to know whether and how this behavioral flexibility responds to anthropogenic disturbance. The true lemurs (Eulemur clade) constitute a valuable case to study these potential effects, as all species studied so far exhibit cathemerality. Here we explored the effects of anthropogenic disturbance on activity patterns of Eulemur while controlling for ecological factors proposed as determinants of activity shifts. We first performed a meta-analysis using 13 long-term studies conducted over the last three decades on various populations of Eulemur. We fitted a beta regression using the proportion of diurnality (the activity taking place between sunrise and sunset) as the response variable and seven climatic, ecological, and anthropogenic disturbance variables at each site as predictors. We also present a validation with original data using year-round, 24-h activity of collared brown lemurs (Eulemur collaris) in forest fragments with different levels of disturbance in southeastern Madagascar. Diurnality was prevalent at most sites. Seasonality, proportions of leaves in the diet, and group size were all found to be significant predictors of the proportion of diurnal activity. After controlling for socioecological factors in the model, overall anthropogenic disturbance emerged as a negative predictor of diurnality. Our validation suggests that the lemurs in the more disturbed area exhibited more nocturnal activity than those in the less disturbed area. It is unclear whether the plasticity observed might allow populations of Eulemur to persist in disturbed areas longer than lemurs with less flexible activity patterns.     

Aposematic signaling and seasonal variation in dorsal pelage in a venomous mammal

In mammals, colouration patterns are often related to concealment, intraspecific communication, including aposematic signals, and physiological adaptations. Slow lorises (Nycticebus spp.) are arboreal primates native to Southeast Asia that display stark colour contrast, are highly territorial, regularly enter torpor, and are notably one of only seven mammal taxa that possess venom. All slow loris species display a contrasting stripe that runs cranial‐caudally along the median sagittal plane of the dorsum. We examine whether these dorsal markings facilitate background matching, seasonal adaptations, and intraspecific signaling. We analyzed 195 images of the dorsal region of 60 Javan slow loris individuals (Nycticebus javanicus) from Java, Indonesia. We extracted greyscale RGB values from dorsal pelage using ImageJ software and calculated contrast ratios between dorsal stripe and adjacent pelage in eight regions. We assessed through generalized linear mixed models if the contrast ratio varied with sex, age, and seasonality. We also examined whether higher contrast was related to more aggressive behavior or increased terrestrial movement. We found that the dorsal stripe of N. javanicus changed seasonally, being longer and more contrasting in the wet season, during which time lorises significantly increased their ground use. Stripes were most contrasting in younger individuals of dispersal age that were also the most aggressive during capture. The dorsal stripe became less contrasting as a loris aged. A longer stripe when ground use is more frequent can be related to disruptive colouration. A darker anterior region by younger lorises with less fighting experience may allow them to appear larger and fiercer. We provide evidence that the dorsum of a cryptic species can have multimodal signals related to concealment, intraspecific communication, and physiological adaptations.     

Long-term genetic monitoring of a translocated population of collared brown lemurs

Post-release monitoring is important to improve translocation success because it provides an opportunity to identify factors relevant to the survival of local populations. We studied a population of the endangered collared brown lemur (Eulemur collaris) translocated from a degraded forest fragment to a nearby littoral forest within the Mandena Conservation Area in southeast Madagascar from 2000–2011. We compared genetic surveys of mitochondrial and nuclear markers with the genetic profile of nearby populations to examine the dispersal capacity of the collared brown lemur. We also performed a landscape analysis to assess changes in connectivity between forest fragments. There was a fluctuating trend characterized by a phase of demographic and genetic stability shortly after translocation, followed by an increase in genetic diversity coinciding with a population decrease and a gradual recovery of initial conditions. These results demonstrated the ability of the collared brown lemur to disperse through unfavorable landscapes and to recover after translocation. Our study revealed the importance of monitoring translocated populations over time using a multidisciplinary approach.     

The sticky tasty: the nutritional content of the exudativorous diet of the Javan slow loris in a lowland forest

Primates - Plant exudates are an important food source for many primates. The Critically Endangered Javan slow loris (Nycticebus javanicus) was previously found to prefer Acacia decurrens exudate...