Feeding Ecology of Sympatric Mouse Lemur Species in Northwestern Madagascar

We performed a comparative pilot study on vertical space use and feeding ecology of 2 closely related sympatric mouse lemur species in northwestern Madagascar. We recorded feeding behavior and the use of vertical forest strata for 6 gray and 4 golden-brown mouse lemur females that we followed for 120 h. We carried out feeding experiments and analyzed fecal samples for food remains. Both species showed no significant difference in use of forest strata. They had a similar overall diet, with insect secretions and gum as main plant food resources; arthropod remains occurred in about half of all fecal samples. Both lemurs used in common >50% of the plant species that each consumed, which accounts for ≥70% of all individual plants used. However, both species used >40% of their feeding plant species exclusively and seemed to differ in their degree of specialization on certain plant species.     

Habitat Utilization of Three Sympatric Cheirogaleid Lemur Species in a Littoral Rain Forest of Southeastern Madagascar

I compared the habitat utilization in 3 sympatric species of Cheirogaleidae (Microcebus murinus [81 g], Cheirogaleus medius [183 g] and Cheirogaleus major [362 g]) in a littoral rain forest in southeastern Madagascar during 3 rainy seasons. Females of promiscuous Microcebus murinus had small home ranges and the males had large overlapping home ranges. Home ranges of family groups of monogamous Cheirogaleus medius and C. major overlapped extensively. Home ranges of all 3 species overlapped completely in the study area but home range sizes differed among species and correlate positively with body masses. Male Microcebus murinus slept in open vegetation (79%) and alone (71%), whereas female M. murinus and family group members of Cheirogaleus spp. preferred communal sleeping in tree holes. There are significant interspecific differences in the choice of sleeping sites: smaller lemurs chose smaller trees and used more sleeping sites than larger lemurs did. Species also differed significantly in the vertical dimension of forest utilization: Cheirogaleus major used the upper part of the trees, C. medius used the middle parts, and Microcebus murinus used the understory during nocturnal activities. The 3 species differed mainly in vertical habitat utilization and showed vertical stratification.     

Chemical Properties of the Diets of Two Lemur Species in Southwestern Madagascar

Seasonal dietary variations demonstrate the importance of certain plant parts during the year. A parallel analysis of their nutritional constituents provides further information on underlying patterns of consumption of the plant parts and the relative importance of key nutrients. I studied the diets of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas), for 9 mo over a 13-mo period in the highly seasonal tropical dry forest site of Beza Mahafaly in southwestern Madagascar. I tested dietary plant parts for nutrients—protein, free amino acids, and sugars—and for 2 potential deterrents, phenolics and tannins, using plant extracts prepared in the field. I compared consumption of nutrients and secondary compounds throughout the year and between seasons. Nutrients are balanced throughout the year. The 2 lemur species do not appear nutrient-starved in either season, though actual quantities of nutrients and contributing food parts differ for each species. Lemur catta consumes high levels of sugar throughout the year, whereas Propithecus takes in higher levels of protein. The effects of phenolics and tannins are quantitative, and they appear to deter consumption of plant parts only past a certain threshold. Sifakas consume them in greater quantities than those of ring-tailed lemurs, which appear more sensitive to their effects. Sifakas may have a higher tolerance for secondary plant metabolites, which is consistent with reports for other folivores. The overall stability of nutrients throughout the year indicates no lean period that coincides with the decline in food abundance during the dry season, though actual caloric intake probably decreases.     

Seasonal Changes in Feeding Ecology and Activity Patterns of Two Sympatric Mouse Lemur Species,the Gray Mouse Lemur (<Emphasis Type="Italic">Microcebus murinus</Emphasis>) and the Golden-brown Mouse Lemur (<Emphasis Type="Italic">M. ravelobensis</Emphasis>), in Northwestern Madagascar

Because closely related species are likely to be ecologically similar owing to common ancestry, they should show some degree of differentiation in order to coexist. We studied 2 morphologically similar congeneric species, the golden-brown mouse lemur (Microcebus ravelobensis) and the gray mouse lemur (M. murinus). These species are found in partial sympatry in the dry deciduous forest in northwestern Madagascar. We investigated whether 1) feeding niche differentiation and/or 2) a reduction in locomotor activity during periods of food shortage, which might reflect an energy saving strategy, can explain the coexistence of these 2 lemur species. To obtain feeding and behavioral data, we conducted focal observations of 11 female Microcebus murinus and 9 female M. ravelobensis during 11 months from 2007 to 2008 and collected fecal samples for 6 mo. We monitored the phenology of 272 plant specimens and trapped arthropods to determine food availability. Results revealed interspecific differences in 1) relative proportion of consumed food resources, resulting in a merely partial dietary overlap, and in 2) relative importance of seasonally varying food resources throughout the year. In addition, females of Microcebus murinus showed a reduction in locomotor activity during the early dry season, which might reflect an energy-saving strategy and might further reduce potential competition with M. ravelobensis over limited food resources. To conclude, a combination of interspecific feeding niche differentiation and differences in locomotor activity appears to facilitate the coexistence of Microcebus murinus and M. ravelobensis.     

Molecular Evidence of Reproductive Isolation in Sympatric Sibling Species of Mouse Lemurs

Recent morphological and molecular phylogenetic studies of mouse lemurs (Microcebus) living in the western and southern regions of Madagascar have shown that specific diversity had been considerably underestimated. In large part, this underestimate was due to the lack of sufficient specimens from given localities to assess properly the level of phenotypic variation within and between populations. The accurate delineation of specific boundaries has no doubt been confounded by the diminutive size, nocturnal habits, and subtle morphological variation characteristic of mouse lemurs, which can make field identification of individuals problematic. We illustrate the use of molecular phylogenetic analysis to reveal reproductive isolation in two sympatric mouse lemur species, Microcebus murinus and M. griseorufus. Their documentation in the Berenty Private Reserve in the extreme south of Madagascar verifies the historically-broad distribution of Microcebus griseorufus, a species recently resurrected from synonomy.     

Diets of Two Lemur Species in Different Microhabitats in Beza Mahafaly Special Reserve,Madagascar

Studies of primate diets usually focus on differences that distinguish species or populations. However, variation in diet can occur at a more local level of groups within a population, especially in a non-homogeneous habitat. I compared dietary variation in food composition and toughness across groups of 2 lemur species in Beza Mahafaly special reserve, Madagascar. Beza Mahafaly contains an 80-ha reserve (Parcel 1) that, while small, hosts a dense population of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas). Microhabitats in the eastern vs. western sides of the parcel are structurally and floristically distinct. Sifakas in this parcel have small, discrete home ranges and are morphological folivores. For these reasons, I expected that the 6 groups studied would eat a different menu of food plants but with similar toughness values. Ring-tailed lemurs have comparatively large, overlapping home ranges, and I expected that the 5 study groups would eat similar foods. Despite living in different microhabitats across the parcel, sifakas exhibit high dietary uniformity both in dietary plant species composition and the toughness of the foods. Food selection in sifakas operates on two distinct levels. Sifaka groups share many key food species that appear independent of local abundances, but the ranking of the foods within each group appears related to availability. Ring-tailed lemur groups are more heterogeneous in the composition of their diets relative to sifakas, though the time spent feeding on individual foods reveals a marked preference for the fruits of Tamarindus indica by all groups. Food toughness is consistent across the parcel with the exception of the most western group. Ring-tailed lemurs are highly specific feeders, but indiscriminate nibblers. Sifakas are targeted, balanced feeders. There does not appear to be a consistent microhabitat effect operating across species. Differences within sifaka and ring-tailed lemur populations in food composition and toughness, however, correspond to an east-west microhabitat gradient. Measures of dietary flexibility must take into account not only the plant species consumed and the different parts eaten but also their associated food properties and proportion of time spent feeding on them.     

Habitat Characteristics and Lemur Species Richness in Madagascar1

In the extant lemur communities of Madagascar the number of lemur species increases with increasing number of tree species. In forests with few tree species lemurs use patches with higher number of tree species than average. However, in forest plots with high number of tree species, lemurs stay in places with lower number of tree species than average. At low tree species diversity a minimum number of different tree species seems to be required within the animals' home range to assure year-round food availability. At high tree species diversity tree species essential for survival might be diluted by resources which are of no use for lemurs, thus increasing energetic expenses for traveling between suitable patches. According to the present analyses, structural diversity is of subordinate importance to the number of tree species as a correlate of lemur species richness. Within limits of disturbance intensity and on a small geographic scale, disturbances increase forest productivity. Lemurs reach higher species numbers and population densities in slightly disturbed areas compared with undisturbed sites. This peaked curve of the number of lemur species over disturbance, however, may not only be a consequence of “resource dilution” in undisturbed sites and higher food abundance in slightly disturbed areas, but also a consequence of selective extinction of lemur species which were unable to cope with the disturbance regime exaggerated by human interference over the last few hundred or thousand years.     

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.     

Quantifying Reproductive Barriers in a Sympatric Pair of Darter Species

Quantifying and comparing the strengths of different reproductive barriers between diverging lineages is especially useful for determining the evolutionary mechanisms driving speciation. Etheostoma barrenense and Etheostoma zonale are closely related sympatric species of darters that are sexually dimorphic and exhibit clear differences in male nuptial coloration. Prior studies demonstrated that these species exhibit complete behavioral isolation, and that both intraspecific and interspecific variation in male coloration play a role in female choice, all consistent with speciation by sexual selection on male nuptial color. Remaining unclear, however, is whether behavioral isolation is the strongest reproductive barrier between these species or, alternatively, whether additional reproductive barriers are equally strong, which could implicate mechanisms other than sexual selection in speciation. Here, we compare the relative strengths of multiple reproductive barriers between the two focal species, measuring: (1) ecological isolation, (2) gametic incompatibility, (3) hybrid inviability, (4) conspecific sperm precedence, and comparing these measures to a previously estimated strength of behavioral isolation. We find that behavioral isolation is the strongest reproductive barrier measured to date and suggest it may be the only barrier that has evolved to completion. This result provides additional empirical evidence for speciation driven by sexual selection and provides insight into the maintenance of sympatric species in nature.     

Group Composition, Home Range Size, and Diet of Three Sympatric Bamboo Lemur Species (Genus Hapalemur) in Ranomafana National Park, Madagascar

This is the first long-term, simultaneous, comparative study of three bamboo lemur species (Hapalemur griseus, H. aureus, and H. simus) at a site in southeastern-central Madagascar where they occur in sympatry. At Talatakely, Ranomafana National Park, the three Hapalemur spp. share overlapping home ranges. Hapalemur griseus has flexible group sizes, varying from three to nine individuals (n = 6). The home range of Hapalemur griseus averages 15 ha (n = 2). Hapalemur aureus forms family groups of 4 individuals (n = 3); they have a home range on average of 26 ha (n = 2). The single group of Hapalemur simus is composed of one or three adult males, two adult females, and their offspring; they occupy a home range of 62 ha. The three species of Hapalemur are year-round bamboo specialists: >88% of their diets consist of bamboo and grass in the Family Poaceae. Contrary to earlier findings, all three Hapalemur spp. consume the cynogenic parts—young leaf bases, young pseudopetioles, and young shoots—of the giant bamboo, Cathariostachys madagascariensis. They rely heavily on this plant, which comprises 72–95% of their diets. Hapalemur griseus and H. aureus consume similar proportions of bamboo vs. nonbamboo plants, though they differ in the species of bamboo they prefer. Hapalemur simus has the most distinct diet of the three bamboo lemurs. They exploit the young shoots of Cathariostachys madagascariensis during the austral summer rainy season, between November and April. From June to November, Hapalemur simus shifts its diet to eating the mature culm pith of Cathariostachys madagascariensis; the proportion of pith represented in their diet reaches a maximum of 89% in October. Seasonal availability of food resources, feeding competition, and factors related to body size may provide clues to the understanding of diet selection among the three sympatric Hapalemur spp.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

A National-Level Assessment of Lemur Hunting Pressure in Madagascar

International Journal of Primatology - Hunting is one of the greatest threats to nonhuman primates worldwide. Despite Madagascar’s status as a primate mega-diversity country, a critical lack...     

Nectar Production of Two Sympatric Species of Columnar Cacti

We examined the potential for exploitation competition by differential attractiveness in two sympatric species of columnar cacti on Curaçao, Netherlands Antilles. Stenocereus griseus and Subpiloccreus repandus have temporally overlapping flowering phenologies and share pollinators. We examined nectar volume, energy contents, and sugar ratios for the entire night and at two-hour intervals in both cactus species. Except for a burst in nectar volume and sugar concentration by Subpilocereus repandus during the first two hours of anthesis, nectar secretion patterns, energy contents, and sugar ratios (70% hexose) were similar for the two species. The standing crops of nectar in both species were kept very low by bat pollinators. We suggest that the potential for exploitation competition between Stenocereus griscus and Subpilocereus repandus is currently very low on Curapo.     

Transmission Patterns of Pinworms in Two Sympatric Congeneric Primate Species

Understanding pathogen transmission is essential to addressing the dynamics of infectious diseases in animal populations. Directly transmitted parasites spread in host populations via 1) contact with infected individuals and 2) contact with contaminated substrates. Although studies exist that support social or ranging effects on transmission, it is less clear how these factors interact. We test the hypothesis that a combination of social, ranging, diet, and intrinsic factors account for Trypanoxyuris minutus (pinworm) infections in sympatric howler species Alouatta palliata and A. pigra. We collected 211 howler fecal samples from 34 adults living in four groups, two of each species, in Tabasco (Mexico), and calculated pinworm prevalence and eggs per gram of feces (EPG). We followed each group for 80 h to determine ranging, diet, frequency of contact, and conspecific proximity. Prevalence of Trypanoxyuris minutus was high, with 82% of all individuals infected. Logistic modeling indicated that pinworm prevalence was positively associated with proximity and the proportion of group members contacted by focal individuals. Although EPG results should be interpreted cautiously owing to variable egg excretion, this index was also positively associated with proximity and the proportion of group members that were contacted, as well as with dietary diversity and use of non-tree foods. Neither intrinsic factors such as species and sex, nor group and population level variables, such as group and home range size, home range overlap, and intensity of range use, were significant predictors of pinworm infection. We conclude that both sociality and feeding behavior are key factors in infection dynamics of Trypanoxyuris minutus in sympatric Alouatta palliata and A. pigra, confirming that contact with infected conspecifics and contaminated substrates are important mechanisms for directly transmitted parasites.     

Metabarcoding Gastrointestinal Nematodes in Sympatric Endemic and Nonendemic Species in Ranomafana National Park,Madagascar

Sympatric species are known to host the same parasites species. Nevertheless, surveys examining parasite assemblages in sympatric species are rare. To understand how parasite assemblages in sympatric host species differ in a given locality, we used a noninvasive identification method based on high-throughput sequencing. We collected fecal samples from sympatric species in Ranomafana National Park, Madagascar, from September to December in 2010, 2011, and 2012 and identified their parasites by metabarcoding, sequencing a region of the small ribosomal subunit (18S) gene. Our survey included 11 host species, including endemic primates, rodents, frogs, gastropods, and nonendemic rats and dogs. We collected 872 samples, of which 571 contained nematodes and 249 were successfully sequenced. We identified nine putative species of parasites, although their correspondence to actual parasite species is not clear as the resolution of the marker gene differs between nematode clades. For the host species that we successfully sampled with 10 or more positive occurrences of nematodes, i.e., mouse lemurs (Microcebus rufus), black rats (Rattus rattus), and frogs (Anura), the parasite assemblage compositions differed significantly among host species, sampling sites, and sampling years. Our metabarcoding method shows promise in interrogating parasite assemblages in sympatric host species and our results emphasize the importance of choosing marker regions for parasite identification accuracy.     

Diet of the Brown Mouse Lemur (Microcebus rufus) in Ranomafana National Park, Madagascar

The conventional notion is that small-bodied primates should be highly insectivorous in order to obtain protein and other nutrients from a food source that is more easily digestible than plant matter. I studied feeding behavior of Microcebus rufus for 16 months in the east coast rainforest of Ranomafana National Park. I determined the diet primarily through analysis of 334 fecal samples from live-trapped individuals. They consumed a mixed diet basically of fruit and insects year-round. I identified 24 fruits, while 40–52 remain unidentified. Bakerella, a high-lipid epiphytic semiparasitic plant, was in 58% of fecal samples that contained fruit seeds, and was consumed year-round irrespective of general resource availability. It served both as a staple and keystone resource. Fruit was less frequently totally absent from fecal samples of individual mouse lemurs than insect matter was. For Microcebus rufus, fruit may be a primary source of energy, not just complementary to insects. Fruit consumption increased in quantity and diversity during the latter part of the rainy season and the very early part of the dry season, when fruit production was relatively high. This pattern in fruit feeding is similar to that for mouse lemurs in the west coast dry forests and is related to specific nutritional needs dictated by the highly seasonal character of the life cycle. Coleoptera were present in 67% of samples examined and were consumed year-round by the subjects, but insect consumption did not increase during the rainy season when insect abundance was highest.     

Dietary Spectrum of Two Sympatric Canid Species in Ladakh,India

We have conducted a study between May and August 2013 to understand the dietary spectrum of two canid species: Tibetan wolf (Canis lupus chanco) and Red fox (Vulpes vulpes) in one of the most inhospitable landscape of the world. Ladakh is characterized by harsh environmental conditions and low primary productivity and therefore animal populations, particularly of large and medium sized herbivores are also low and sparsely distributed. This in turn poses a challenge to the survival of predators. We have attempted to investigate the ways by which the two sympatric canid species are optimizing feeding for their survival in an environment where there is scarcity of wild prey base. Scats of the two species were collected from Chiktan and Rangdum valleys and undigested food remnants were identified. The dietary spectrum of Tibetan wolf was composed of six prey species (2 wild and 4 livestock species). The share of livestock species in the diet was maximum (RO: 62.0%). The Red fox being an opportunistic feeder consumed 19 forgeable items, including small and medium sized mammals, birds, reptiles, insects, plant material, eggs, stones and debris. The livestock species contributed maximum to the diet of Red fox (RO: 22.9%). The dietary niche breadths of both species were more or less similar (0.53 and 0.58) and indicating a generalist feeding behavior. Both the species are surviving in the same environment with a dietary overlap of 0.60. The given information is expected to aid further studies in Indian Trans-Himalaya.     

Vibrational Communication in Two Sympatric Species of Mantophasmatodea (Heelwalkers)

The communication via percussion of the abdomen on the substrate for species recognition and mate location of males and females of two sympatric species of the recently described insect order Mantophasmatodea (Heelwalkers) was investigated. Each sex produced a single and distinctive call. The female call consisted of repeated single pulses, whereas the more complex male call comprised repeated pulse trains. The calls of males and females of the two species were of similar general structure, but differed in most temporal characters such as pulse and pulse train repetition time. In behavioral playback experiments females reacted to the call of conspecific males by calling and decreasing locomotion. When stimulated with the call of the heterospecific, sympatric male, females showed no reaction. Males exhibited abdominal rubbing, high tapping rates, increased activity (both movement and active searching) as well as characteristic searching behavior at branch nodes, when presented with the conspecific female call. Being stimulated with the playback of the heterospecific female call and the conspecific male call respectively, males responded with less intense locomotor and searching behavior. The drumming behavior in the control situation (no playback) suggests that males sometimes call in the absence of other individuals.