Mitchell T. Irwin

Spatial and temporal arrival patterns of Madagascar's vertebrate fauna explained by distance, ocean currents, and ancestor type

How, when, and from where Madagascars vertebrates arrived on the island is poorly known, and a comprehensive explanation for the distribution of its organisms has yet to emerge. We begin to break that impasse by analyzing vertebrate arrival patterns implied by currently existing taxa. For each of 81 clades, we compiled arrival date, source, and ancestor type (obligate freshwater, terrestrial, facultative swimmer, or volant). We analyzed changes in arrival rates, with and without adjusting for clade extinction. Probability of successful transoceanic dispersal is negatively correlated with distance traveled and influenced by ocean currents and ancestor type. Obligate rafters show a decrease in probability of successful transoceanic dispersal from the Paleocene onward, reaching the lowest levels after the mid-Miocene. This finding is consistent with a paleoceanographic model [Ali JR, Huber M (2010) Nature 463:653–656] that predicts Early Cenozoic surface currents periodically conducive to rafting or swimming from Africa, followed by a reconfiguration to present-day flow 15–20 million years ago that significantly diminished the ability for transoceanic dispersal to Madagascar from the adjacent mainland.

The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS

204 Abstract The unique primates of south-eastern Madagascar face threats from growing human popula- tions. The countrys extant primates already represent only a subset of the taxonomic and ecological diversity existing a few thousand years ago. To prevent further losses remaining taxa must be subjected to effective monitoring programmes that directly inform conserva- tion efforts. We offer a necessary first step: revision of geographic ranges and quantification of habitat area and population size for diurnal and cathemeral (active during both day and night) lemurs. Recent satellite images are used to develop a forest cover geographical information system, and censuses are used to establish range boundaries and develop estimates of population density and size. These assessments are used to identify regions and taxa at risk, and will be a useful baseline for future monitoring of habitat and populations. Precise estimates are impossible for patchily-distributed taxa (especially Hapalemur aureus, H. simus and Varecia variegata variegata); these taxa require more sophisticated modelling.

Feeding Ecology of Propithecus diadema in Forest Fragments and Continuous Forest

Forest fragmentation is viewed as a serious threat to primates, yet whether or not it can disrupt food resources and cause energetic stress remains largely untested. I present the results of a 12-mo study of the feeding ecology of Propithecus diadema in fragmented and continuous forest at Tsinjoarivo, eastern Madagascar. Two continuous forest groups had higher dietary diversity and ate more fleshy fruit, but during the dry season, diversity was reduced and they relied heavily on mistletoe (Bakerella clavata). In contrast, 2 groups in fragments employed the lean season strategy of eating mistletoe year-round; the fruiting tree species that sustain continuous forest groups through the rainy season were largely absent. As expected, intersite dietary overlap was highest in the dry season. The level of specialization was high: fragment groups devoted 30–40% of feeding time to Bakerella clavata, compared to 28–30% in continuous forest. The major characteristic of Bakerella clavata enabling it to be an important fallback or staple resource, or both, is its extended phenology. The difference in resource utilization between sites may have important implications for nutritional status, as well as ranging and social behavior, largely owing to the small size and high abundance of feeding patches of Bakerella. Understanding resource shifts in fragments can shed light on socioecological questions by providing comparisons between continuous forest and fragment populations with differing diets and resource distributions. In addition, understanding dietary shifts in fragments can aid in species-specific conservation efforts, while contributing to a better understanding of the considerable interspecific variability of primates in responses to fragmentation.

Primate energy expenditure and life history

Significance Measurements of daily energy expenditure indicate that primates, including humans, expend only half of the calories expected for mammals of similar body size. As energy expenditure is central to organismal biology, these results hold important implications for life history, evolutionary biology, and foraging ecology for primates and other mammals. Specifically, we show that primates’ remarkably low metabolic rates account for their distinctively slow rates of growth, reproduction, and aging. Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates’ slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates’ slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates’ slow metabolic rates contribute to their characteristically slow life histories.

A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar

The Spiny Thicket Ecoregion (STE) of Southern and southwestern Madagascar was recently home to numerous giant lemurs and other “megafauna,” including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores. Following the arrival of humans more than 2,000 years ago, dramatic extinctions occurred. Only one‐third of the lemur species which earlier occupied the STE survive today; other taxa suffered even greater losses. We use stable isotope biogeochemistry to reconstruct past diets and habitat preferences of the recently extinct lemurs of the STE. We show that the extinct lemurs occupied a wide range of niches, often distinct from those filled by coeval non‐primates. Many of the now‐extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Most fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets. These new data suggest that the recent extinctions have likely had significant ecological ramifications for the communities and ecosystems of Southern and southwestern Madagascar. Am. J. Primatol. 73:25–37, 2011.

The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar.

There are two possible approaches to understanding natural and human-induced changes in the primate communities of Madagascar. One is to begin with present-day and recent historic interactions and work backwards. A second is to begin with paleoecological records of Malagasy primate communities before and immediately following human arrival, and the associated evidence of human and nonhuman primate interactions, and work forwards. On the basis of biological and climatic studies, as well as historic and ethnohistoric records, we are beginning to understand the abiotic and biotic characteristics of Madagascar’s habitats, the lemurs’ ecological adaptations to these unique habitats, the extent of forest loss, fragmentation and hunting, and the differential vulnerability of extant lemur species to these pressures. On the basis of integrated paleoecological, archaeological and paleontological research, we have begun to construct a detailed chronology for late prehistoric Madagascar. We are beginning to understand the complex sequence of events that led to one of the most dramatic recent megafaunal extinction/extirpation events. Combining the perspectives of the past and the present, we see a complex set of interactions affecting an initially rich but vulnerable fauna. The total evidence refutes any simple, unicausal (e.g. hunting/habitat destruction/climate change) explanation of megafaunal extinctions, yet unequivocally supports a major role – both direct and indirect – for humans as the trigger of the extinction process. It also supports a change over time in the relative importance of hunting versus habitat loss, and in the trophic characteristics of the primate communities in Madagascar.

Imperfect Isolation: Factors and Filters Shaping Madagascar's Extant Vertebrate Fauna

Analyses of phylogenetic topology and estimates of divergence timing have facilitated a reconstruction of Madagascar’s colonization events by vertebrate animals, but that information alone does not reveal the major factors shaping the island’s biogeographic history. Here, we examine profiles of Malagasy vertebrate clades through time within the context of the island’s paleogeographical evolution to determine how particular events influenced the arrival of the island’s extant groups. First we compare vertebrate profiles on Madagascar before and after selected events; then we compare tetrapod profiles on Madagascar to contemporary tetrapod compositions globally. We show that changes from the Mesozoic to the Cenozoic in the proportions of Madagascar’s tetrapod clades (particularly its increase in the representation of birds and mammals) are tied to changes in their relative proportions elsewhere on the globe. Differences in the representation of vertebrate classes from the Mesozoic to the Cenozoic reflect the effects of extinction (i.e., the non-random susceptibility of the different vertebrate clades to purported catastrophic global events 65 million years ago), and new evolutionary opportunities for a subset of vertebrates with the relatively high potential for transoceanic dispersal potential. In comparison, changes in vertebrate class representation during the Cenozoic are minor. Despite the fact that the island’s isolation has resulted in high vertebrate endemism and a unique and taxonomically imbalanced extant vertebrate assemblage (both hailed as testimony to its long isolation), that isolation was never complete. Indeed, Madagascar’s extant tetrapod fauna owes more to colonization during the Cenozoic than to earlier arrivals. Madagascar’s unusual vertebrate assemblage needs to be understood with reference to the basal character of clades originating prior to the K-T extinction, as well as to the differential transoceanic dispersal advantage of other, more recently arriving clades. Thus, the composition of Madagascar’s endemic vertebrate assemblage itself provides evidence of the islands paleogeographic history.

LEMUR LATRINES: OBSERVATIONS OF LATRINE BEHAVIOR IN WILD PRIMATES AND POSSIBLE ECOLOGICAL SIGNIFICANCE

Latrine behavior, or the preferential, repeated use of 1 or more specific defecation sites, is well known among mammals and believed to function in olfactory communication among individuals or groups in many circumstances. Primates have reduced their capacity for olfaction in favor of more developed visual systems; however, several prosimian primates regularly use olfactory communication for transmission of social signals, most often using scent gland secretions and urine. Latrine behaviors have been described rarely in primates and have traditionally not been included in reviews of primate olfactory communication, yet we found ample evidence that certain primate species habitually use latrine sites for defecation. Here we review the previous evidence for latrine use in primates and report new and more extensive observations of latrine use in 2 lemuriform primates (Lepilemur sp. and Hapalemur griseus). Based on these new observations, we present and evaluate 4 available hypotheses for the function of latrines (advertisement of sexual cycling, predation avoidance, intragroup spacing, and intergroup resource defense) in lemur taxa for which sufficient evidence of latrine use exists. In all cases, intergroup resource defense is the function most consistent with available observations.

The Crisis of the Critically Endangered Greater Bamboo Lemur (Prolemur simus)

Abstract: Prolemur simus (the greater bamboo lemur) is the most abundant lemur in the northern subfossil sites of Madagascar. Living populations still persist, but in low numbers within a diminished range, making it one of the most critically endangered lemurs. Over the past twenty years scientists have searched the south- and central-eastern rain forests of Madagascar. Despite surveys that encompass over 500 km2, less than 75 animals have been found, with a recent total count of 60. More encouraging is that in 2007 two new sites containing P. simus were found: Mahasoa an unprotected 150 ha fragment east of the Ranomafana/Andringitra corridor (17 P. simus), and Torotorofotsy, a RAMSAR site near Andasibe (∼16 P. simus). Prolemur simus is a bamboo specialist with a patchy geographic distribution, which may be driven by the distribution of one or two bamboo species. Home ranges are large, group size has been observed to be from four to 26 individuals, and localities may be spaced hundreds of kilometers apart. Ranomafana National Park contains the only fully habituated group, and there are a total of three groups known in the park. We make recommendations for conservation action for these populations of P. simus. If immediate action is taken, we may be able to prevent the extinction of this species within the next decades.

Variation in physiological health of diademed sifakas across intact and fragmented forest at Tsinjoarivo, Eastern Madagascar.

As undisturbed habitat becomes increasingly rare, managers charged with ensuring the survival of endangered primate species must increasingly utilize disturbed and degraded habitats in species survival plans. Yet we have an imperfect understanding of the true long‐term viability of primate populations in disturbed habitat, and census data can be misleading because density is not necessarily correlated with habitat quality and population viability in predictable ways. Here we present clinical laboratory data on hematology, serum biochemistry, fat‐soluble vitamins, minerals, iron analytes, viral serology, and parasitology of diademed sifaka (Propithecus diadema), derived from the capture of 26 individuals spanning eight groups and two habitats (undisturbed vs. disturbed and fragmented) at Tsinjoarivo, Madagascar. Blood from fragment individuals had significantly lower values for several factors: white blood cell counts, bilirubin, total protein, albumin, calcium, sodium, chloride, manganese, zinc, iron and total iron‐binding capacity. Several biochemical variables were higher in immature individuals, probably due to active growth. The large number of interhabitat differences suggests that habitat disturbance has an impact on physiological health within this population, perhaps reflecting dietary stress and/or immunosuppression. These results, combined with previous data showing altered diet, slower juvenile growth, and reduced activity in disturbed forest fragments, suggest that fragment sifakas may be less healthy than continuous forest groups. Finally, Tsinjoarivo sifakas have extremely low blood urea nitrogen (perhaps reflecting protein limitation) and selenium levels relative to other lemurs. Despite their survival and reproduction in the short term in fragments, these sifakas may represent a riskier conservation investment than conspecifics in undisturbed forest, and may be more susceptible to environmental stressors. However, more data on the fitness consequences of these biochemical differences are needed for a better interpretation of their impacts on long‐term viability prospects. Am. J. Primatol. Am. J. Primatol. 72:1013–1025, 2010.