Correction to: Population Dynamics of Nocturnal Lemurs in Littoral Forest Fragments: The Importance of Long-Term Monitoring

International Journal of Primatology -     

Estimating Encounter Rates and Densities of Three Lemur Species in Northeastern Madagascar

Primate populations, including Madagascar’s lemurs, are threatened worldwide and conservationists need accurate population estimates to develop targeted conservation plans. We sought to fill knowledge gaps for three lemur taxa —white-fronted brown lemur (Eulemur albifrons); eastern woolly lemur (Avahi laniger); and Allocebus/Microcebus, a category combining observations of hairy-eared dwarf lemurs (Allocebus trichotis) and mouse lemurs (Microcebus spp.)— in northeastern Madagascar by estimating their density, examining how their encounter rates and densities vary across three different forest types, and monitoring trends in encounter rates and densities at resurveyed sites, using data from surveys at six forest sites over a 4-year period (2010–2013). Landscape density for white-fronted brown lemur, eastern woolly lemur, and Allocebus/Microcebus was 21.5 (SE 3.67), 57.7 (SE 9.17), and 39.1 (SE 9.55) individuals/km², respectively. There was no difference in density estimates at intact and intermediately degraded forest sites; however, we encountered white-fronted brown lemurs more often in intact forest (1.64 ± SE 0.40 individuals/km) than in intermediately degraded and degraded forest (0.15 ± SE 0.06 and 0.16 ± SE 0.06 individuals/km). In addition, we encountered white-fronted brown lemurs at lower rates in 2013 (0.15 ± SE 0.06 individuals/km) compared to 2010 (0.82 ± SE 0.12 individuals/km) at a resurveyed site. Our findings emphasize that primate researchers must account for variation in how lemur encounter rates and densities differ between intact and degraded forests, and although we observed a decline in white-fronted brown lemur encounter rate at our resurveyed site, we caution that changes in lemur encounter rates may simply reflect lower detection rates rather than lower density. Future research should focus on using conventional distance sampling techniques, which are infrequently used in primate studies, to provide more robust density estimates as a way to accurately assess trends and the effects of anthropogenic pressures on lemur populations.     

Feeding Patterns and Dietary Profile of Nocturnal Southern Woolly Lemurs (Avahi meridionalis) in Southeast Madagascar

Folivory has evolved in all primate radiations but the relative importance of resource quantity and nutritional quality of food is controversial. To understand how food abundance and different nutrients affect a folivorous diet, we investigated food composition of the leaf-eating lemur Avahi meridionalis. From June to December 2004, we conducted 26 nights of focal observation (256.1 h) in Sainte Luce pluvial littoral forest (southeast Madagascar) and recorded feeding behavior of 4 radiocollared individuals. Within the subjects’ home ranges, we recorded vegetation characteristics (morphospecies, phenology, diameter at breast height) and sampled food and nonfood items for chemical analyses. A. meridionalis did not eat fruit but only leaves and flowers and did not base their choice on food abundance. Adult leaves eaten were higher in easily soluble protein than adult leaves that were not consumed. The subjects ate young leaves and flowers as soon as they became available. These young leaves contained the same concentrations of soluble protein, higher concentrations of crude protein, and lower concentrations of acid detergent fiber and sugar than mature food leaves. A. meridionalis ate leaves with condensed tannins, alkaloids, and intermediate concentrations of polyphenolics. Contrary to previous studies that considered Avahi spp. a specialist, A. meridionalis acted as leaf-eating generalists with moderate selectivity, based on nutritional quality and tolerance of a wide array of plant secondary metabolites. This illustrates the dietary flexibility within a single genus of primates that seems to be driven by environmental constraints rather than morphological or physiological adaptations.     

Forest Age Influences In-stream Ecosystem Processes in Northeastern US

A disturbance or natural event in forested streams that alter available light can have potential consequences for nutrient dynamics and primary producers in streams. In this study, we address how functional processes (primary production and nutrient uptake) in stream ecosystems respond to changes in forest canopy structure. We focus on differences in incoming irradiance, nutrient uptake (NO₃, NH₄, and PO₄) and open-channel metabolism seasonally in 13 forested streams that drain forests with different canopy structures (10 to >300 years old) in the northeastern United States. Light irradiance was related to forest age in a U-shaped pattern, with light being the greatest in both young open forests (<50 years old) and older growth forests (>245 years old), whereas the darkest conditions were found in the secondary growth middle-aged forests (80–158 years old). Streams that had adjacent open or old-growth riparian forest had similar conditions with greater standing stock biofilm biomass (chl a), and elevated ER in October compared to streams with middle-aged riparian forests. Compared to all sites, streams with old-growth riparian forest had the greatest in-stream primary production rates (GPP) and elevated background nutrient concentrations, and to a lesser degree, increased nutrient retention and uptake (V _f). Streams draining older forests tended to be more productive and retentive than middle-aged forests, likely due to increased light availability and the age and structure of surrounding forest canopies. Middle-aged forests had the least variation in response variables compared to streams in young and old-growth riparian forests, likely a result of uniform canopy conditions. As the structure of widespread middle-aged forests in NE US is altered by loss of specific tree species, climate change, and/or human activity, it will impact in-stream production and nutrient dynamics and may ultimately alter nutrient loading in downstream catchments.     

Motivations for the Ownership of Captive Lemurs in Madagascar

The live capture of primates is occurring throughout the tropics and can be a threat to their conservation. Primates are owned as pets for a variety of reasons. Studies of the motivations for primate ownership have been conducted in several countries where they are endemic, but no study has examined this issue in Madagascar. Madagascar is home to the highest number of threatened primate taxa in any one country, and an estimated 28,000 lemurs were kept in illegal captivity from 2010 to mid-2013. We aimed to expand knowledge about the motivations of lemur ownership in Madagascar. Data were collected via a web-based survey (n = 229 respondents) and from the websites and social media pages of 25 hotels. We found that many lemurs (45%) were seen on the premises of a business or in a private home (27%). Many lemurs were perceived to be kept as personal pets (37%) or for money-making or tourism purposes (20%). When lemurs were used for money-making, owners could receive indirect (72% of the time) and direct benefits (28%). Hotels showing photographs of captive lemurs on their websites and social media sites charged USD 25.69 more per night for a standard room than hotels that did not show such photographs. We found little evidence that captive lemurs are kept as a social status symbol, for captive breeding, or as a fallback food. These findings provide evidence that the motivations for the ownership of, usually illegal, captive lemurs is typically linked with money-making or with the desire to have a lemur as a pet. These data can help target new outreach programs.     

Elevational Ranges of Lemurs in the Humid Forests of Madagascar

The geological history of Madagascar contains events that may have given rise to unusual factors that molded the primate communities of the island. In order to understand the impact of the factors we reviewed the elevational distribution of extant primate species in the humid forests. The elevational structuring of primates in the humid forests of Madagascar shows considerable differences from other tropical areas in the New World and Asia, which is correlated with the lack of large tracts of humid lowland habitat on Madagascar since it split from India.     

People,Lemurs and Utilitarian Plants of the Littoral Forests in Southeast Madagascar

International Journal of Primatology - Tropical forests support a diversity of plants. Many of them are threatened, emphasising that their shared use by people and wildlife may benefit their...     

The Effects of Habitat Disturbance on Lemurs at Ranomafana National Park, Madagascar

The alarming rate of deforestation in Madagascar is driving some endemic primates to extinction. Surprisingly, anthropogenic habitat disturbance is not always deleterious. The effect of disturbance on lemur abundance may be related to diet, with frugivorous species more prone to population declines than folivores or insectivores. To test the effects of disturbance on lemur abundance and group size, we surveyed 2 sites within contiguous forest at Ranomafana National Park, 1 lightly disturbed primary forest (Vato) and 1 heavily logged forest (Tala). We quantified forest structure variables along 6 survey routes and conducted 68 diurnal and 42 nocturnal lemur surveys. Canopy closure, canopy height, and understory visibility were greater in Vato than in Tala. We encountered 2 frugivorous lemurs (Eulemur rufifrons, Varecia variegata) and 1 folivore (Avahi peyrierasi) significantly more frequently in Vato than in Tala, whereas the opposite was true for the insectivorous Microcebus rufus. Rates did not differ statistically for 1 frugivore (Eulemur rubriventer) and 2 folivores (Propithecus edwardsi, Hapalemur griseus). Comparisons across the 6 survey routes suggest that the abundance was heterogeneous within as well as between sites. Neither group size nor composition differed between sites. Encounter rates for Varecia variegata were positively related to canopy closure, and encounter rates for Avahi peyrierasi were positively related to canopy height. Encounter rates for Microcebus rufus were negatively related to canopy closure, height, and understory visibility. Similar to other studies, the results suggest that some lemurs, including folivores, may cope with anthropogenic disturbance better than others, including some frugivores. Lemur abundance is heterogeneous, though, even on small spatial scales.     

Direct and Indirect Impacts of Raptor Predation on Lemurs in Southeastern Madagascar

I calculated rates of predation by 2 species of diurnal raptors, Polyboroides radiatus and Accipiter henstii, on the lemur community of Ranomafana National Park, Madagascar from 2700 h of observation and 470 prey deliveries at 7 nests of each hawk species. The 2 hawks consumed 7 of 12 lemurs found in the park region, with a body mass of 63–3500 g and including diurnal and nocturnal species of all group sizes. Calculations of predation rates indicate that raptor predation is a significant cause of mortality for lemur populations relative to other causes. Minimum rates of predation by Polyboroides radiatus and Accipiter henstii on Microcebus rufus, Cheirogaleus major, Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata resulted in the raptors removing of 1–21% of the population per yr, similar to other rates of predation on primates documented in the literature. Modeling of lemur populations under varying levels of raptor predation pressure that I calculated found that one may attribute 3–17% of adult, juvenile, and infant mortality for nocturnal lemurs and 2–66% of adult, juvenile, and infant mortality for diurnal lemurs to diurnal raptor predation. Raptor predation may significantly depress intrinsic growth rates and carrying capacity of Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata owing to their low fecundities, long life spans, and long age to sexual maturation. Nocturnal lemurs may best avoid predation by diurnal raptors by exhibiting a solitary lifestyle and cryptic antipredator tactics, whereas, diurnal lemurs benefit less by increasing group size than by using specific antipredator tactics.     

Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar

I aimed to determine when and under which seasonal environmental conditions gray mouse lemurs (Microcebus murinus), a small nocturnal primate species endemic to Madagascar, utilize daily torpor. Using temperature-sensitive radio collars, I measured skin temperature (T _sk ) of free-ranging mouse lemurs under natural conditions. My results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a ) during the dry season, but not during the rainy season. Mouse lemurs that remained normothermic had significantly lower body masses (mean: 59.7 g) than individuals that used torpor (mean: 80.2 g). Skin temperatures dropped to 20.9°C and the mean torpor bout duration is 10.3 h. The use of torpor on a given night varied among individuals, whereas the propensity for torpor did not differ significantly between males and females. I found no evidence that T _a can be used to predict whether mouse lemurs will remain normothermic or enter torpor. It appears that the most reliable indicator for the occurrence of torpor in free-ranging Microcebus murinus is time of the year, i.e., photoperiod.     

Biogeography of Dwarf Lemurs: Genetic Evidence for Unexpected Patterns in Southeastern Madagascar

Seven species of dwarf lemurs (Cheirogaleus spp.) are currently recognized after a recent revision of the genus. During a field study in southeastern Madagascar, we observed 3 distinct morphotypes of Cheirogaleus resembling Cheirogaleus medius, C. major and C. crossleyi. In particular, for Cheirogaleus crossleyi southeastern Madagascar was far away from the known distribution range of the species when referring to the recent revision of the genus. In order to clarify the taxonomic status of the 3 morphotypes, we compared field samples from southeastern Madagascar to museum specimens from several locations in Madagascar and to field samples from Kirindy/CFPF, western Madagascar by genetic analyses using the mitochondrial cytochrome b gene. Genetic data yield strong support for 2 of the 3 morphotypes to represent Cheirogaleus medius and C. major. The third morphotype is genetically closely related to Cheirogaleus crossleyi, albeit more distantly than the other 2 morphotypes to the respective reference samples. The genetic distance is related to a considerable geographic distance between the location of our field study and the origin of the respective reference specimen, because Cheirogaleus crossleyi had been reported only from northern Madagascar. Our field observations indicate an isolated population in southeastern Madagascar. We propose to identify them as Cheirogaleus crossleyi and discuss the population genetic and biogeographic considerations supporting this conclusion.     

Taxonomic Revision of Mouse Lemurs (Microcebus) in the Western Portions of Madagascar

The genus Microcebus (mouse lemurs) are the smallest extant primates. Until recently, they were considered to comprise two different species: Microcebus murinus, confined largely to dry forests on the western portion of Madagascar, and M. rufus, occurring in humid forest formations of eastern Madagascar. Specimens and recent field observations document rufous individuals in the west. However, the current taxonomy is entangled due to a lack of comparative material to quantify intrapopulation and intraspecific morphological variation. On the basis of recently collected specimens of Microcebus from 12 localities in portions of western Madagascar, from Ankarana in the north to Beza Mahafaly in the south, we present a revision using external, cranial, and dental characters. We recognize seven species of Microcebus from western Madagascar. We name and describe 3 spp., resurrect a previously synonymized species, and amend diagnoses for Microcebus murinus (J. F. Miller, 1777), M. myoxinus Peters, 1852, and M. ravelobensis Zimmermann et al., 1998.     

Effect of Soil Type on Population Densities of Nematodes in Soybean Rotation Fields

The effect of soil type on population densities of plant parasitic nematode species in 17 field blocks of four different soil types rotated to corn, soybeans, wheat, and forage mixtures was investigated during a generally droughty 5-year period. High densities of Helicotylenchus pseudorobustus were found in dark silty clay loams. Highest densities of Tylenchorhynchus acutus were also in one of the dark-colored silty clay loams. Light-colored silt loams favored development of Paratylenchus projectus, which developed poorly in the darker soils. Comparable densities of Xiphinema americanum were found in all soils and on all crops, regardless of soil type. Tylenchorhynchus martini, although present, did not build up in any of the soils. Populations of Pratylenchus species were generally low in the rotated blocks of all soil types.     

Habitat Suitability and Population Size Estimates for the Mongoose Lemurs (Eulemur mongoz) of Madagascar and the Comoro Islands,and Implications for Their Conservation

International Journal of Primatology - Tropical forests face an alarming rate of loss driven by anthropogenic pressures, exposing forest-dwelling species such as primates to extinction risks....     

Social Relationships Among Ring-Tailed Lemurs (Lemur catta) in Two Free-Ranging Troops at Berenty Reserve, Madagascar

We observed two free-ranging troops of ring-tailed lemurs at the Berenty Reserve, Madagascar. Kinship affinities in these troops are known only for mothers and their offspring 4 years of age. We attempted to quantify social relationships. Almost all agonistic interactions were dyadic, and triadic agonistic interactions, such as alliances, were very rare. Dominance hierarchies in both sexes in the two troops were not linear. As in cercopithecine monkeys, mothers were dominant over their adult daughters. However, the daughters were not ranked immediately below their mothers. Close proximity and social grooming occurred more frequently between closely related females, such as mother–daughter and sister–sister dyads, than between unrelated females. Frequent-proximity relations also occurred between adult males that had emigrated from another troop and entered the present troop together, even though they did not rank closely to one another. Subordinates were likely to groom and to greet dominants more frequently than vice versa. During group encounters, particular females were involved in agonistic interactions with animals of other troops, regardless of dominance rank. Adult males, regardless of their dominance rank, but not adult females, constantly tried to drive solitary males away.