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Giuseppe Donati is a Reader in Primatology. Over the last twenty years Giuseppe has conducted research on behaviour, ecology, and conservation of lemurs and New World monkeys, and produced numerous publications in peer-reviewed journals or books. He initially focussed his research on the unique evolutionary traits of the lemur radiation, and especially their capacity to be active both during the day and at night. Through this work he made a contribution to the understanding of the cost-benefit involved in the transition from the nocturnal to the diurnal life-style during the evolution of primates. Giuseppe’s more recent research addresses a priority area in conservation research, i.e. investigating how primates tolerate habitat change. This work culminated in his involvement in the designing of the Lemur Conservation Action Plan and a leading role on lemur research and conservation in the region of Fort Dauphin (South-eastern Madagascar).
Establishing reintroduced primates in a suitable predetermined area has proven to be a challenge. Establishment is the first major step that has to be taken in the long process of reintroduction. When this first goal is not achieved, the chances of success decline drastically. Understanding the main determinants of establishment is therefore crucial for reintroduction success. This study examined the influence of three independent factors on the establishment success of reintroduced spider monkeys. We analysed data from the releases of eight groups of black-faced spider monkeys (Ateles chamek), which are part of the official reintroduction program of spider monkeys in the South Eastern Peruvian Amazon. Establishment success was measured by the proportions of individuals within groups that were found in the target area six months after release. The hours research assistants and volunteers spent with the group within the first three months after release – in the context of post-release monitoring – was shown to have a positive effect on the establishment success of the released group in the target area. The presence of an already established group in the area was found to have also a significant positive effect on establishment success. The influence of the days of post-release food provisioning had no effect Our findings emphasize the importance of long-term monitoring programs to help increase the efficiency of primate reintroductions.
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. L. 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 in food items 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.
Habitat loss and fragmentation pose a significant threat to many primate species worldwide, yet community level responses are complex and nuanced. Despite repeated calls from primatologists and the wider conservation community to increase monitoring initiatives that assess long-term population dynamics, such studies remain rare. Here we summarise results from a longitudinal study set in the littoral forests of southeast Madagascar. Littoral forests are a useful model for monitoring lemur population dynamics, as they are relatively well-studied and their highly fragmented nature enables the effect of forest size and anthropogenic impacts to be examined. This study focuses on three Endangered nocturnal lemur species – Avahi meridionalis, Cheirogaleus thomasi and Microcebus tanosi – across three forest fragments of different size and with different usage histories. Between 2011 and 2018, we walked 285km of line transect and recorded 1,968 lemur observations. Based on Distance Sampling analysis our results indicate that nocturnal lemurs respond to forest patch size and to levels of forest degradation in species-specific ways. The largest species, A. meridionalis, declined in density and encounter rate over time across the three study forests. C. thomasi populations appeared stable in all three fragments, with densities increasing in the most degraded forest. M. tanosi encounter rates were extremely low across all study fragments but were lowest in the most heavily degraded forest fragment. Our results emphasise the importance of localised pressures and species-specific responses on population dynamics. Monitoring population trends can provide an early warning signal of species loss and species-specific responses can inform crucial intervention strategies.
Whilst 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, non-seasonal food resource and be a key factor for persistence during the initial stage of the recolonization.
Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation, are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large‐bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species’ distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore‐frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive folivores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape‐level reforestation efforts.
Time is considered a resource in limited supply, and temporal niche separation is one of the most common strategies that allow ecologically similar species to live in sympatry. Mechanisms of temporal niche separation are understudied especially in cryptic animals due to logistical problems in gathering adequate data. Using high-frequency accelerometers attached to radio-collars, we investigated whether the ecologically similar lemurs Avahi meridionalis and Lepilemur fleuretae in the lowland rainforest of Tsitongambarika, south-eastern Madagascar, show temporal niche separation. Accelerometers stored data with a frequency of 1 Hz for a total of 71 days on three individuals of A. meridionalis and three individuals of L. fleuretae. We extrapolated motor activity patterns via the unsupervised learning algorithm expectation maximisation and validated the results with systematic behavioural observations. Avahi meridionalis showed peaks of activity at twilights with low but consistent activity during the day, while L. fleuretae exhibited more activity in the central hours of the night. Both lemur species had their activity pattern entrained by photoperiodic variations. The pair-living A. meridionalis was found to be lunarphilic while the solitary-living L. fleuretae was lunarphobic. We suggest that these activity differences were advantageous to minimise feeding competition, as an anti-predator strategy, and/or for dietary-related benefits. These findings demonstrate a fine-tuned temporal partitioning in sympatric, ecologically similar lemur species and support the idea that an activity spread over the 24-h, defined here as cathemerality sensu lato, is more common than previously thought in lemurs.
Ecologically similar species may exhibit temporal niche partitioning and separate their peaks of activity when co-occurring in an area. We show for the first time that the mainly nocturnal genus Avahi can exhibit high crepuscular activity with low but consistent bouts of activity (up to 44.6% of daily activity) during the day. We defined this activity as cathemerality sensu lato as opposed to the cathemerality sensu stricto observed in Eulemur sp. We suggest that this flexible activity may be advantageous for the species to minimise feeding competition and predatory pressure, and/or to provide dietary-related benefits. This finding in the secondary nocturnal genus Avahi supports the idea that activity patterns in lemurs are graded and traditional categorisations are inadequate.
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.
Facets of habitat quality which allow species persistence in forest fragments are an important aspect for primate conservation. Mantled howler monkeys (A. palliata) seem to be tolerant of habitat fragmentation, though the limits of this flexibility are not yet clear. In some areas, howler monkey densities in small, primary forest fragments are among the highest ever recorded for the species. We hypothesize that if high density is also determined by habitat carrying capacity; primaryvegetation should provide higher quality resources. Alternatively, if density is just the consequence of crowding, this would decrease the quality of the diet compared to that of monkeys living in non-crowded forests. To test these hypotheses, we studiedfour howler monkey groups at La Suerte Biological Field Station, North-eastern Costa Rica. Two groups occurred in a small primary forest with high howler density, while two groups lived in a large secondary forest with lower density. We collected behavioural data via a 5-min Focal Animal Sampling to estimate activity, habitat use and diet. Food samples were also collected and then analyzed to evaluate their nutritional contents. Moreover, we registered GPS coordinates and estimated home-ranges and mean inter-location distances. Our results show that primary forest food samples contained a significantly lower amount of fiber and a higher protein/fiber ratio than samples from the secondary habitat. Also, primary forest groups used larger feeding trees and moved substantially less than secondary forest groups. Our results support the hypothesis that the primary forest provides higher quality resources than the secondary habitat and, as a possible consequence, howler monkeys living in the latter have to move more to meet their energy requirements.
Primates deal with fluctuations of the thermal environment by both physiological and behavioral mechanisms of thermoregulation. In this article we focus on nonhibernating lemurs, which are hypometabolic and have to cope with a seasonal environment. Behavioral thermoregulation has received little attention compared with specific physiological adaptations to seasonality, i.e., hibernation and torpor, which characterize a number of lemurs. We investigated the role of seasonality and dietary-related factors in determining frequencies of resting, social and postural thermoregulation, and microhabitat selection in collared lemurs, Eulemur collaris. We observed two groups of collared lemurs over a 14-month period in the littoral forest of Sainte Luce, Southern Madagascar. Frequencies of total resting and time spent in huddling, prone, and curled postures were collected via 5-min instantaneous sampling. Microhabitat selection was evaluated as the proportion of time spent in the upper canopy as compared with other layers. Climatic variables were recorded by automatic data loggers, while dietary variables were derived from phenological data and nutritional analyses of the ingested food items. We weighted the combined effects of climatic and dietary variables on the different types of behavioral thermoregulation by means of canonical correlation analysis. The model with the strongest canonical correlation included a first root representing mainly feeding time, day length, and ambient temperature and a second root representing diet quality and height of feeding trees. The output indicated that collared lemurs adapt to thermal and dietary-related metabolic stress by adjusting resting time, social, and postural thermoregulation.
Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H. meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.
Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce.
Methodology/Principal Findings Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees. Conclusions/Significance Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.
Trade in primates is seen as a significant impediment to their conservation. Primates are traded both domestically and internationally, in order to supply, amongst others, biomedical industries and pharmaceutical markets, the entertainment business, or pet markets. Primate meat is consumed globally, whereas body parts are used as ingredients in traditional medicine or sold as curios. All international trade in primates is regulated through the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES), to which all but 2 primate range countries are signatory. The last 15 years has seen a linear increase in the export of live primates (each year 3500 more individuals are exported), with China being, numerically, the largest exporter. While the trade in live primates worldwide involves tens, if not hundreds, of thousands of individuals a year, the trade in dead primates involves millions of animals a year. We introduce here a series of studies dealing with various aspects of the primate trade. We hope that these studies will urge others to quantify the extent of trade in primates alive and dead in both domestic and international contexts, allowing us to find ways to mitigate the consequences of this trade to the conservation of primates.
Research Highlights.The papers included in this special issue examine interspecific responses to habitat fragmentation by primate populations
We identify intra and interspecific variables that can help predict primate population viability and potential persistence in fragmented landscapes
The Mahavavy-Kinkony Wetland Complex (MKWC), North-Western Madagascar gained protected status in January 2007. Remaining forests are highly fragmented yet the complex covers most of the range of two highly threatened lemur species, Propithecus coronatus and Eulemur mongoz. The IUCN Lemur Specialist Group suggested E. mongoz be updated from Vulnerable to Critically Endangered based on rapid habitat loss. Thus, new data from MKWC are crucial for conservation action planning in this area. Lemur surveys were conducted in MKWC between May-June 2008 using nocturnal/diurnal strip transects in five fragments and presence/absence data from an additional three fragments using rapid diurnal surveys. Propithecus coronatus, Propithecus deckenii, Eulemur rufifrons, Eulemur mongoz, Microcebus sp and Lepilemur sp were encountered. Compilation with previous research produced updated distribution maps for MKWC and Eulemur mongoz densities were compared over time. Eulemur mongoz densities in Anjamena decreased at a rate of 85% over 13 years. Although not significant (p=.65), nested analysis (T=0.02) suggested E. mongoz as the most vulnerable to fragmentation of the diurnal/cathemeral lemur species surveyed. During the surveys, the species was not found in any fragments less than 250ha although representatives of all other species were still present. This research supports the IUCN Lemur Specialist Group’s suggestion to update the status of the E. mongoz and highlights the urgent need for conservation planning in the MKWC.
Forest fragmentation alters both the quality and area of habitat available to primate species. Determining whether there are vegetation traits associated with primate population density and structure may help to manage fragmented habitats better. In this study, we investigated whether significant demographic changes had occurred in populations of Neotropical primates over the last decade at La Suerte Biological Station, Costa Rica. Those changes were then related to forest structureand diversity. We sampled tree height, density, diversity, crown volume and canopy cover in a small fragment of old-growth vegetation (20 ha) and in a fragment of mature, second-growth forest (250 ha). We also carried out censuses of mantled howlers (Alouatta palliata) , white-faced capuchins (Cebus capucinus) and black-handed spider monkeys (Ateles geoffroyi). Overall, both forests had similar vegetation structure, but the primary site had trees with larger crown volume and higher diversity. Forest agecorrelated positively with howler density and the size of howler foraging groups. Primate populations in the primary fragment seem to have reached carrying capacity, while populations of all three species in the secondary fragment had grown significantly. Our findings support other studies that have identified the importance of tree diversity and large trees for primate habitat.