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.     

Morphometrics confirm taxonomic deflation in dwarf lemurs (Primates: Cheirogaleidae), as suggested by genetics

Detailed knowledge of the identity and distributions of extant species is essential for unravelling patterns and mechanisms of biodiversity, and it provides indispensable baseline data for conservation efforts. The taxonomy of the primates of Madagascar (Lemuriformes) has experienced drastic revisions in the last decades, with species numbers skyrocketing, especially in the genera Microcebus, Avahi, and Lepilemur. The dwarf lemurs (genus Cheirogaleus) have received less attention in terms of their taxonomy, even though they are closely related and syntopic with these diverse genera. The last revision of the genus was based on morphological data from museum specimens, and accepted seven species: Cheirogaleus medius, Cheirogaleus major, Cheirogaleus crossleyi, Cheirogaleus adipicaudatus, Cheirogaleus sibreei, Cheirogaleus ravus, and Cheirogaleus minusculus, whereas a more recent multilocus molecular study only detected three lineages: C. medius, C. major, and C. crossleyi. The goal of this study was to reassess the currently accepted taxonomy of the genus by examining six external and 32 craniodental characters of 120 museum specimens and 36 new specimens from the field. This study, in conjunction with a complementary molecular study, revealed lower diversity and a lower number of distinct morphs of dwarf lemurs than previously postulated. We conclude that in our sample there are three distinct morphs in the genus Cheirogaleus that correspond to C. medius, C. major, and C. crossleyi. We formally recognize C. adipicaudatus and C. ravus as synonyms of C. medius and C. major, respectively, and consider C. minusculus and C. sibreei to be potential synonyms of C. medius. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010.     

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.     

Biology of <Emphasis Type="Italic">Cheirogaleus major</Emphasis> in a Littoral Rain Forest in Southeast Madagascar

Greater dwarf lemurs (Cheirogaleus major) are small nocturnal primates from the rain forests of eastern Madagascar. I investigated a population of Cheirogaleus major in a littoral rain forest of Southeast Madagascar during 2 rainy seasons to supplement the sparse information available for the species. I collected data on morphology, group composition, sleeping behavior, home range, and social organization via mark/recapture, radio telemetry, and focal individual observations. I identified 2 presumed family groups, and my data from radiotracking revealed a monogamous social organization. In each group, I found an adult pair and its presumed offspring sharing home ranges and sleeping sites together. I also observed gregarious behavior of group members during their nocturnal activity. I found no difference in body measurements between sexes, but body mass and tail circumference increased significantly from November to February, indicating a fatting period before hibernating.     

Adaptive loss of color polymorphism and character displacements in sympatric <Emphasis Type="Italic">Mnais</Emphasis> damselflies

A geographical survey of two Mnais damselfly species in the Kinki area of Japan showed evidence for character displacements when the two species were found in sympatry. Mnais costalis, a species that has polymorphic male mating types of orange-winged territorial and clear-winged non-territorial morphs (hereafter abbreviated to orange and clear morphs respectively) in allopatry often shifted to having monomorphic orange morphs in sympatry. The mean body size of orange morphs was consistently larger than that of clear morph in allopatry. The mean body size of the sympatric orange morphs was even larger than that of allopatric orange morphs. By contrast, Mnais pruinosa, a species that also has two morphs of large orange and small clear morphs in allopatry, shifted to having monomorphic clear morphs in sympatry. The mean body size of the sympatric clear morphs was smaller than that of allopatric clear morphs. Divergence was also detected in the preference for habitat insolation conditions between sympatric Mnais damselflies. Both species in allopatric regions prefer half-light forest habitats, while in sympatric regions they showed diversified habitat preference: M. costalis preferred sunny habitats while M. pruinosa preferred shady habitats. Multiple character displacements in signal traits and habitat preference emerged in heterogeneous forest light environments are likely to have synergistic effects on the reproductive isolation of the two species.     

Distribution,Population Structure and Habitat Use of Microcebus berthae Compared to Those of Other Sympatric Cheirogalids

We aimed to identify the geographical and biotic limitations of Microcebus berthae, the smallest extant primate. Furthermore we analyzed the mating system of two local populations and their habitat use in relation to microhabitat structures and to those of Microcebus murinus and Cheirogaleus medius, two potentially competing lemur species. The range of Microcebus berthae is restricted to 220 km² in the dry deciduous forest of western Madagascar. A very optimistic estimate of the total population size is ca. 7900 individuals. During a 13-mo mark-recapture study individuals were trapped from May 1995 to May 1996 at permanent trap locations 50 m apart over 2 study areas of ca. 25 ha each. The spacing of trap locations where individuals have been retrapped indicate that males have larger home ranges than those of females, which in concert with multiple intra- and intersexual range overlap indicates a promiscuous mating system. In contrast to the other 2 species, Microcebus berthae maintained specific habitat utilization patterns at 2 sites with different vegetation structures. Their habitat use in relation to vegetation characteristics differed from that of Cheirogaleus medius but not from that of Microcebus murinus. Co-occurrence patterns of Microcebus berthae and M. murinus deviated significantly from random and resembled a checkerboard distribution possibly generated by competitive exclusion. Thus, according to the niche concept, Microcebus berthae seem to be separated from Cheirogaleus medius by differences in food composition and habitat requirements, while they avoid direct competition with M. murinus by spatial separation.     

Characterizing neutral and adaptive genomic differentiation in a changing climate: The most northerly freshwater fish as a model

Arctic freshwater ecosystems have been profoundly affected by climate change. Given that the Arctic charr (Salvelinus alpinus) is often the only fish species inhabiting these ecosystems, it represents a valuable model for studying the impacts of climate change on species life‐history diversity and adaptability. Using a genotyping‐by‐sequencing approach, we identified 5,976 neutral single nucleotide polymorphisms and found evidence for reduced gene flow between allopatric morphs from two high Arctic lakes, Linne'vatn (Anadromous, Normal, and Dwarf) and Ellasjøen (Littoral and Pelagic). Within each lake, the degree of genetic differentiation ranged from low (Pelagic vs. Littoral) to moderate (Anadromous and Normal vs. Dwarf). We identified 17 highly diagnostic, putatively adaptive SNPs that differentiated the allopatric morphs. Although we found no evidence for adaptive differences between morphs within Ellasjøen, we found evidence for moderate (Anadromous vs. Normal) to high genetic differentiation (Anadromous and Normal vs. Dwarf) among morphs within Linne'vatn based on two adaptive loci. As these freshwater ecosystems become more productive, the frequency of sympatric morphs in Ellasjøen will likely shift based on foraging opportunities, whereas the propensity to migrate may decrease in Linne'vatn, increasing the frequency of the Normal morph. The Dwarf charr was the most genetically distinct group. Identifying the biological basis for small body size should elucidate the potential for increased growth and subsequent interbreeding with sympatric morphs. Overall, neutral and adaptive genomic differentiation between allopatric and some sympatric morphs suggests that the response of Arctic charr to climate change will be variable across freshwater ecosystems.     

Character displacement in style length between pollinator-sharing Clerodendrum trichotomum and C. izuinsulare (Verbenaceae)

Competition for pollination may occur between pollinator-sharing sympatric plants and this may cause character displacement of their floral traits. We examined this possibility by comparing flower morphology of the sympatric population of Clerodendrum trichotomum and its co-flowering congener, C. izuinsulare, with that of the allopatric populations. The two species were visited in common by such insects as diurnal hawkmoths, bees, swallowtails and nocturnal hawkmoths, and were pollinated nocturnally as well as diurnally. Interspecific pollen transfer can occur by sharing pollinators; however, they did not hybridize when artificially pollinated. Flower size, including stamen and style lengths, is larger in C. trichotomum with an overlap in range. The style of C. izuinsulare in the sympatric population was significantly shorter than that in the allopatric population, while there was no significant difference in style length between the allopatric and the sympatric C. trichotomum. This seems to facilitate avoidance of interspecific pollen transfer in the sympatric population.Ken Inoue was killed in an accident on July 28, 2003, during his research trip in Sakhalin.     

Breeding systems and hybridization inPetrorhagia sect.Kohlrauschia (Caryophyllaceae)

In the diploid speciesP. prolifera, the evolution of autogamy has resulted in the presence of distinct selfing and outcrossing races. The change in breeding system toward autogamy is associated with a reduction in the size of floral features and a lower pollen production. The outbreeding populations have only been found in Greece, while the selfing populations have colonized much of Europe. The two races appear to be reproductively isolated from one another. —Petrorhagia sect.Kohlrauschia contains four species.P. glumacea is outbreeding and shows unilateral incompatibility with the small-flowered race ofP. prolifera and interfertility with the large-flowered race; althoughP. glumacea is sympatric with the large-flowered race, they do not appear to hybridize in the wild. Amongst the allopatric species, internal breeding barriers are also found. These may take the form of hybrid sterility or seed incompatibility.P. velutina is autogamous and reproductively isolated from all the other species of the section regardless of whether they are sympatric or allopatric. It is suggested that the evolution of autogamy has been an important factor in the spread ofP. velutina, the tetraploidP. nanteuilii, and the small-flowered race ofP. prolifera in Europe.     

Sympatric and allopatric combinations of hen fleas and great tits: a test of the local adaptation hypothesis

To test whether allopatric nest parasites differ from sympatric ones in their effect on various life history traits of their avian host, I designed a cross-transfer experiment in which hen fleas (Ceratophyllus gallinae) were exchanged between great tit (Parus major) nests in two geographically widely separated areas. In neither of the areas did allopatric fleas influence body mass, tarsus length, wing length, duration of nestling period or mortality in great tit nestlings more severely than did sympatric fleas. Duration of incubation was also similar among females independent of experimental treatment. This lack of difference between allopatric and sympatric fleas is hypothesized to reflect the comparative harmlessness of hen fleas for their hosts.     

Reproduction in Coquerel's dwarf lemur (Mirza coquereli)

Most nocturnal Malagasy primates, as well as many diurnal species, are highly endangered in their natural habitat. Captive breeding programs have been established for many species, but detailed information on reproduction is only available for three nocturnal taxa: the mouse lemur (Microcebus murinus), the dwarf lemur (Cheirogaleus medius), and the greater dwarf lemur (Cheirogaleus major). In this study, we present data for another nocturnal Malagasy primate, Coquerel's dwarf lemur (Mirza coquereli), which has been propagated since 1982 at the Duke University Primate Center. Unlike all other Malagasy primates bred in captivity, M. coquereli cycles throughout the year, and is clearly less seasonal in its birth distribution than is C. medius or M. murinus. Estrous intervals ranged between 19 and 30.5 days. Estrus lasted no longer than 1 day. After an average gestation length of 89.2 days, litters of one or two were born. Females cycled for the first time between 8 and 15 months of age, and gave birth for the first time between 12.8 and 33.5 months of age. The earliest mating of a male leading to conception was observed at the age of 17 months. For males and females, an increase in daylength appears to trigger pubertal development. Males had seasonal changes in testicular volume which were not explained by covariation with body weight. Maximum testis size occurred in spring, when breeding activity was highest. The occurrence of year-round reproduction in M. coquereli, and the absence of seasonal fattening and/or hibernation, along with their specialized winter diet, may be correlated. © 1995 Wiley-Liss, Inc.     

THE ROLE OF COURTSHIP SONGS IN REPRODUCTIVE ISOLATION AMONG POPULATIONS OF GREEN LACEWINGS OF THE GENUS CHRYSOPERLA (NEUROPTERA: CHRYSOPIDAE)

Male and female lacewings tremulate during courtship, establishing duets that always precede copulation. Three distinct courtship songs are found in populations of the green lacewing Chrysoperla plorabunda (P1, P2 and P3 song morphs). Analysis of five features of the songs for individuals collected from Connecticut, Idaho, Oregon and California showed few differences within song morphs, but sympatric song morphs differed significantly in temporal features of the songs and their mode of presentation. Playback experiments using recorded songs were performed on females with all possible sympatric and allopatric combinations of females and recorded songs. The results showed that females strongly prefer to duet with recordings of males of their own song type and usually showed no responses to songs of other types. Thus, song differences are effective barriers to reproduction between the sympatric morphs. Our results support the hypothesis that the three song morphs are true biological species.     

Microsatellite markers for paternity testing in fork‐marked lemurs (Phaner furcifer)

We report the development of three new microsatellites and four transferred across‐species for fork‐marked lemurs (Phaner furcifer). Two markers were isolated from Cheirogaleus medius and one from Microcebus murinus. The transferred markers also originate from Cheirogaleus medius and Microcebus murinus. The seven markers were tested on 30 individuals of Phaner furcifer and have proven to be useful for inclusion and exclusion of potential parents. The markers presented here are the first published for application on Phaner furcifer.     

Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat?

The fat-tailed dwarf lemur (Cheirogaleus medius; Cheirogaleidae) lives in the tropical forests of Madagascar. It is exceptional among primates, because this small nocturnal lemur hibernates during the dry season from the end of April until October. This field study was carried out to assess seasonal changes in body mass and behavioral traits (locomotor activity, feeding ecology) of C. medius that enable this species to accumulate large quantities of fat within weeks. Feeding observations of 36 radio-collared individuals were combined with a mark-recapture study in western Madagascar during the rainy seasons from 1995 to 1998. Pulp of fruit species not consumed, as well as fruit species eaten by C. medius was analyzed for lipid and sugar contents. Body mass changes of recaptured individuals revealed that C. medius may double its body mass within a few weeks. Most of the increase in body mass took place between March and April after infants had been weaned and directly before the onset of hibernation. Locomotor activity was significantly reduced during the period of body mass gain. During the entire study, fruits, nectar, and flowers of 34 different plant species comprised about 80% of the diet, supplemented by a seasonally varying intake of animal prey. Lipid contents of consumed fruits were comparatively low throughout the study period. No difference in lipid content was detectable between fruit species consumed and not consumed by C. medius. During prehibernation fattening, C. medius consumed mostly fruit species with a high sugar content, significantly higher than that of fruit species that were not consumed. The results suggest that a reduction in locomotor activity as well as a preference for fruit species with a high sugar content enable C. medius to deposit large quantities of fat in a few weeks. Received: 15 March 1999 / Accepted: 30 June 1999     

Character displacement in giant rhinoceros beetles

I quantitatively analyzed male morphology of two closely related rhinoceros beetles species (Chalcosoma caucasus F. and Chalcosoma atlas L.) in 12 allopatric and seven sympatric locations throughout Southeast Asia. The qualitative features and the magnitude of intraspecific variation of each species were unaltered between allopatric and sympatric locations. Across allopatric locations, body size, horn size, dimorphic dimension, and genitalia size nearly completely overlapped between C. caucasus and C. atlas. Yet, in all sympatric locations, the differences between the two species in these characters were highly significant. While the enlarged difference between the two species in body size in sympatry could be attributed to habitat differentiation, that in genitalia size far exceeded what was expected from the general body-size displacement. These results indicate that morphological character displacement in sympatry was most complete in sexual organs. This may account for the process of existing species conserving themselves as integrated units by avoiding interspecific competition and enhancing reproductive isolation.     

Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.)

We report the development of 13 new microsatellite markers for mouse lemurs (Microcebus sp.). Two markers were isolated from the fat tailed dwarf lemur (Cheirogaleus medius) and 11 from the grey mouse lemur (Microcebus murinus). A total of 561 individuals from four different species of mouse lemurs was genotyped with the newly developed markers. All markers showed Mendelian inheritance in 21 families of mouse lemurs. All markers show polymorphism in several species of mouse lemurs and seven amplified in C. medius. Among these new markers are the first 10 published for M. berthae and the first 11 for M. griseorufus.     

Character displacement in Hydrobia

Summary Fenchel's study of size variation in Hydrobiid snails in the Limfjord, Denmark, provides one of the most convincing cases of ecological character displacement available. In order to assess the generality of the phenomena within the Hydrobia genus, allopatric and sympatric Hydrobia ventrosa, H. neglecta and H. ulvae were collected from 24 coastal sites around Eastern England in July and October, 1982. Shell heights of 5,850 snails from 55 samples were recorded. These data were analysed for intraspecific allopatric-sympatric, and interspecific height differences. Such differences were not significant for H. ventrosa/H. neglecta, but the species exhibited parallel variation at sympatric sites. H. ventrosa/H. ulvae showed only significant interspecific differences, but in both allopatry and sympatry. The pattern of mean size variation for these species resembles that in the Limfjord. However the statistical analyses fail to provide support for character displacement. Differences in character states attributed to the process of character displacement may result from a number of other causes. Environmental conditions at sympatric and allopatric sites may act differentially on the heights of H. ulvae and H. ventrosa. The conditions that prevail at sympatric H. ulvae sites appear to lead to increased size in this species irrespective of the presence of H. ventrosa.     

An analysis of chewed food particle size and its relationship to molar structure in the primatesCheirogaleus medius andGalago senegalensis and the insectivoranTupaia glis

The chewed food particle size and shearing capacity of the lower molars of two primate species, the fat-tailed dwarf lemur,Cheirogaleus medius and the bushbabyGalago senegalensis, and an insectivoran, the tree shrew,Tupaia glis, were compared. Differences in the shearing design of the lower molars correlate strongly with the chewed food particle size in these species: the greater the shearing capacity, the smaller the chewed food particles. These three species are of comparable size but differ greatly in diet in the wild.C. medius primarily eats fruit and nectar, whileG. senegalensis andT. glis are largely insect-eaters. The lower molars ofG. senegalensis andT. glis show a much greater shearing capacity than do those ofC. medius. The average length of chewed food particles ofC. medius is significantly larger than that ofG. senegalensis, while that ofT. glis is intermediate between the two primates but is closer to that ofG. senegalensis. Our findings that insect-eating species grind their food more finely than do fruit- and resin-eating species can be correlated with digestibility of foods: finely chewing foods such as fruits which are low in relatively undigestible cell wall components would not greatly improve their digestibility, so a highly efficient food processing apparatus would be less important to the animal's survival. Insect-eaters much more finely chew their foods, implying that there is some constituent of insect bodies difficult to digest, and that grinding increases its digestibility. We suggest that this constituent is chitin.     

Does sympatry predict life history and morphological diversification in the Mexican livebearing fish Poeciliopsis baenschi?

Understanding why some species coexist and others do not remains one of the fundamental challenges of ecology. Although there is evidence to suggest that closely‐related species are unlikely to occupy the same habitat because of competitive exclusion, there are many cases where closely‐related species do co‐occur. Research comparing sympatric and allopatric populations of co‐occurring species provides a framework for understanding the role of phenotypic diversification in species coexistence. In the present study, we compare phenotypic divergence between sympatric and allopatric populations of the livebearing fish, Poeciliopsis baenschi. We focus on life‐history traits and body shape, comprising two sets of integrated traits likely to diverge in response to varying selective pressures. Given that males and females can express different phenotypic traits, we also test for patterns of divergence among sexes by comparing size at maturity and sexual dimorphism in body shape between males and females in each population type. We take advantage of a natural experiment in western Mexico where, in some locations, P. baenschi co‐occur with a closely‐related species, Poeciliopsis turneri (sympatric populations) and, in other locations, they occur in isolation (allopatric populations). The results obtained in the present study show that sympatric populations of P. baenschi differed significantly in life‐history traits and in body shape compared to their allopatric counterparts. Additionally, males and females showed different responses for size at maturity in sympatric conditions versus allopatric conditions. However, the amount of sexual dimorphism did not differ between sympatric and allopatric populations of P. baenschi. Hence, we conclude that not all traits show similar levels of phenotypic divergence in response to sympatric conditions. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 608–618.     

Xanthogranuloma of the choroid plexus in the fat-tailed dwarf lemur (Cheirogaleus medius)

This report documents the death of two fat-tailed dwarf lemurs (Cheirogaleus medius) maintained over 6 years each in our laboratory. Postmortem studies revealed xanthogranuloma of the choroid plexus, a mass replete with stored lipids, including cholesterol crystals. Six months prior to their deaths, both animals developed a peculiar head tilt and signs suggestive of neurological dysfunction. At autopsy, each had masses projecting into the lateral and IVth ventricles and an associated obstructive hydrocephalus. Cryostat sections of the brains of both lemurs showed histological features consistent with xanthogranuloma of the choroid plexus, a histologically benign and usually asymptomatic lesion found in up to 7% of human autopsies. This case is of special interest because of the unique feeding strategies in the fat-tailed dwarf lemur. Since C. medius remains in torpor for 6 months out of the year during the time of food scarcity in the forests of Madagascar, the animal must accumulate large reserves of fat during its active period. In the laboratory, however, dwarf lemurs do not normally go into torpor, and the accumulated fat is not used. The finding of this tumor, therefore, suggests that the combination of a captive high-fat diet and the unusual fat-storage mechanisms utilized by C. medius contributed to the buildup of lipids and might be etiologically related to the development of those lesions. © 1996 Wiley-Liss, Inc.