Implications of lemuriform extinctions for the Malagasy flora.

Madagascar's lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar's lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

The biogeographic origin of a radiation of trees in Madagascar: implications for the assembly of a tropical forest biome.

BACKGROUND: Madagascar's rain forests are characterized by extreme and uneven patterns of species richness and endemicity, the biogeographic and evolutionary origins of which are poorly understood. METHODS: Here we use a time-calibrated phylogeny of a dominant group of trees in Madagascar's eastern rain forests, Canarium, and related Burseraceae (Canarieae), to test biogeographic hypotheses regarding the origin and radiation of the flora of this unique biome. RESULTS: Our findings strongly support the monophyly of Malagasy Canarium, suggesting that this clade represents a previously undocumented in situ radiation. Contrary to expectations of dispersal from Africa during the Oligocene, concurrent with the formation of Madagascar's rain forest biome, our analyses support a late Miocene origin for Malagasy Canarium, probably by long distance dispersal from Southeast Asia. DISCUSSION: Our study illustrates the importance of considering long distance dispersal as a viable explanation for clades with pantropical distributions diversifying subsequent to the Oligocene, and it highlights the formation of the Indo-Australian Archipelago and associated fast-moving equatorial surface currents, suggesting an under-appreciated evolutionary link among tropical centers of endemism. CONCLUSIONS: We postulate that the relatively recent establishment and radiation of Canarium in Madagascar may have been facilitated by the highly stochastic climates associated with these forest ecosystems.

Demography of Verreaux's sifaka in a stochastic rainfall environment.

In this study, we use deterministic and stochastic models to analyze the demography of Verreaux's sifaka (Propithecus verreauxi verreauxi) in a fluctuating rainfall environment. The model is based on 16 years of data from Beza Mahafaly Special Reserve, southwest Madagascar. The parameters in the stage-classified life cycle were estimated using mark-recapture methods. Statistical models were evaluated using information-theoretic techniques and multi-model inference. The highest ranking model is time-invariant, but the averaged model includes rainfall-dependence of survival and breeding. We used a time-series model of rainfall to construct a stochastic demographic model. The time-invariant model and the stochastic model give a population growth rate of about 0.98. Bootstrap confidence intervals on the growth rates, both deterministic and stochastic, include 1. Growth rates are most elastic to changes in adult survival. Many demographic statistics show a nonlinear response to annual rainfall but are depressed when annual rainfall is low, or the variance in annual rainfall is high. Perturbation analyses from both the time-invariant and stochastic models indicate that recruitment and survival of older females are key determinants of population growth rate.

Female social dominance and basal metabolism in a malagasy primate, Propithecus verreauxi.

Tight energetic constraints on reproductively active females are hypothesized to be an important determinant of the phenomenon of female dominance in Propithecus verreauxi, a primate endemic to Madagascar. Five wild sifakas were captured in the Beza Mahafaly Special Reserve in southern Madagascar, and resting metabolic rates (RMR) were measured. Levels were low, as predicted, with the exception of a possibly pregnant female.; Although the data were not conclusive, they were consistent with the hypothesis.

Social relations in semi-free-ranging sifakas (Propithecus verreauxi coquereli) and the question of female dominance.

Female social dominance over males is thought to characterize most of the prosimian primates of Madagascar. It has been reported in Propithecus verreauxi coquereli in the wild but intersexual relations were not fully characterized. In this paper we examine female-male spatial and agonistic relations in semi-free-ranging P. v. coquereli in order to evaluate intersexual social dominance and related behavioral asymmetries. Two hundred hours of focal sampling were conducted on two pairs of P. v. coquereli at the Duke University Primate Center, Durham, NC. Behavioral categories including approach, departure, follow, pass, replace, and aggression were scored and recorded. Our results show strong asymmetry of aggressive encounters, suggesting female dominance over males. No submissive signals were observed. The analysis of spatial relations showed that males were more active than females in maintaining proximity and, on average, male spatial movements could be predicted by female location and activities more often than vice versa. These results indicate a spatially central role for the female of each pair. © 1992 Wiley-Liss, Inc.

Application of fecal steroid techniques to the reproductive endocrinology of female verreaux's Sifaka (Propithecus verreauxi).

Solid phase extraction, high performance liquid chromatography, and radioimmunoassay were used to test the validity of fecal steroid analysis for assessing ovarian function in sifaka (Propithecus verreauxi). Daily fecal samples were collected over a 4 month period from two cycling female sifaka, and single samples were collected from females during normal gestation and males while housed at the Duke University Primate Center. Tests of radioimmunoassay validity indicated that solid phase extraction and microradioimmunoassay techniques were reliable and accurate methods for quantifying ovarian steroids in sifaka feces. The progesterone (P4 ) antibody specifically quantitated only P4 , while several estrogen metabolites made small contributions to immunoreactive measures of estradiol (E2 ). A 1:10 dilution reduced these contributions to 3-15% of the estimated E2 concentration. Although the spectral data suggested that E2 was not the major metabolite present, it accounted for the majority of the immunoreactivity at normal assay dilutions. Fecal profiles of immunoreactive E2 and P4 in the conceptive female resembled serum profiles of other strepsirhines. E2 and P4 were elevated at the end of the conceptive cycle and were more markedly increased in late pregnancy in the two pregnant females. Mating behavior and indices of sexual interest were observed in conjunction with E2 peaks, although not all peaks were accompanied by observations of sexual behavior. © 1995 Wiley-Liss, Inc.

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar.

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.

Evolution in the hypervariable environment of Madagascar.

We show that the diverse ecoregions of Madagascar share one distinctive climatic feature: unpredictable intra- or interannual precipitation compared with other regions with comparable rainfall. Climatic unpredictability is associated with unpredictable patterns of fruiting and flowering. It is argued that these features have shaped the evolution of distinctive characteristics in the mammalian fauna of the island. Endemic Herpestidae and Tenrecidae and members of five endemic primate families differ from closely related species elsewhere, exhibiting extremes of "fastness" and "slowness" in their life histories. Climatic features may also account for the dearth of frugivorous birds and mammals in Madagascar, and for the evolutionary prevalence of species with large body mass.

Intrasexual selection in Verreaux's sifaka (Propithecus verreauxi verreauxi).

Studies of sexual selection show that both female choice and male-male competition can influence the evolution and expression of male phenotypes. In this regard, it is important to determine the functional basis through which male traits influence variation in male reproductive success. In this study, we estimate the strength and type of sexual selection acting on adult males in a population of wild lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). The data used in this study were collected at Beza Mahafaly Special Reserve, southwest Madagascar. We conducted paternity analyses on 70 males in order to estimate the distribution of reproductive success in this population. Paternity data were combined with morphometric data in order to determine which morphological traits covary with male fitness. Five morphological traits were defined in this analysis: body size, canine size, torso shape, arm shape, and leg shape. We utilized phenotypic selection models in order to determine the strength and type of selection acting directly on each trait. Our results show that directional selection acts on leg shape (a trait that is functionally related to locomotor performance), stabilizing selection acts on body mass and torso shape, and negative correlational selection acts on body mass and leg shape. We draw from biomechanical and kinematic studies of sifaka locomotion to provide a functional context for how these traits influence male mating competition within an arboreal environment. Verreaux's sifaka and many other gregarious lemurs are sexually monomorphic in body mass and canine size, despite a high frequency and intensity of male-male aggressive competition. Our results provide some insight into this paradox: in our population, there is no directional selection acting on body mass or canine size in males. The total pattern of selection implicates that behaviors relating to locomotor performance are more important than behaviors relating to fighting ability during intrasexual contests.

Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar (1992-2001).

Gene flow within and between social groups is contingent on behaviourally mediated patterns of mating and dispersal. To understand how these patterns affect the genetic structure of primate populations, long-term data are required. In this study, we analyse 10 years of demographic and genetic data from a wild lemur population (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar. Our goal is to specify how patterns of mating and dispersal determine kinship and genetic diversity among animals in the population. Specifically, we use microsatellite, parentage, and census data to obtain estimates of genetic subdivision (FST), within group homozygosity (FIS), and relatedness (r) within and among social groups in the population. We analyse different classes of individuals (i.e. adults, offspring, males, females) separately in order to discern which classes most strongly influence aspects of population structure. Microsatellite data reveal that, across years, offspring are consistently more heterozygous than expected within social groups (FIS mean = -0.068) while adults show both positive and negative deviations from expected genotypic frequencies within groups (FIS mean = 0.003). Offspring cohorts are more genetically subdivided than adults (FST mean = 0.108 vs. 0.052) and adult females are more genetically subdivided than adult males (FST mean = 0.098 vs. 0.046). As the proportion of females in social groups increases, the proportion of offspring sired by resident males decreases. Offspring are characterized by a heterozygote excess as resident males (vs. nonresident males) sire the majority of offspring within groups. We link these genetic data to patterns of female philopatry, male dispersal, exogamy, and offspring sex-ratio. Overall, these data reveal how mating and dispersal tactics influence the genetic population structure in this species.