Sarah Zohdy

Mapping the social network: tracking lice in a wild primate ( Microcebus rufus ) population to infer social contacts and vector potential

BackgroundStudies of host-parasite interactions have the potential to provide insights into the ecology of both organisms involved. We monitored the movement of sucking lice (Lemurpediculus verruculosus), parasites that require direct host-host contact to be transferred, in their host population of wild mouse lemurs (Microcebus rufus). These lemurs live in the rainforests of Madagascar, are small (40 g), arboreal, nocturnal, solitary foraging primates for which data on population-wide interactions are difficult to obtain. We developed a simple, cost effective method exploiting the intimate relationship between louse and lemur, whereby individual lice were marked, without removal from their host, with an individualized code, and tracked throughout the lemur population. We then tested the hypotheses that 1) the frequency of louse transfers, and thus interactions, would decrease with increasing distance between paired individual lemurs; 2) due to host polygynandry, social interactions and hence louse transfers would increase during the onset of the breeding season; and 3) individual mouse lemurs would vary in their contributions to the spread of lice.ResultsWe show that louse transfers involved 43.75% of the studied lemur population, exclusively males. Louse transfers peaked during the breeding season, perhaps due to increased social interactions between lemurs. Although trap-based individual lemur ranging patterns are restricted, louse transfer rate does not correlate with the distance between lemur trapping locales, indicating wider host ranging behavior and a greater risk of rapid population-wide pathogen transmission than predicted by standard trapping data alone. Furthermore, relatively few lemur individuals contributed disproportionately to the rapid spread of lice throughout the population.ConclusionsUsing a simple method, we were able to visualize exchanges of lice in a population of cryptic wild primates. This method not only provided insight into the previously unseen parasite movement between lemurs, but also allowed us to infer social interactions between them. As lice are known pathogen vectors, our method also allowed us to identify the lemurs most likely to facilitate louse-mediated epidemics. Our approach demonstrates the potential to uncover otherwise inaccessible parasite-host, and host social interaction data in any trappable species parasitized by sucking lice.

Long-Term Lemur Research at Centre Valbio, Ranomafana National Park, Madagascar

We present findings from 25 years of studying 13 species of sympatric primates at Ranomafana National Park, Madagascar. Long-term studies have revealed that lemur demography at Ranomafana is impacted by climate change, predation from raptors, carnivores, and snakes, as well as habitat disturbance. Breeding is seasonal, and each species (except Eulemur rubriventer) gives birth synchronously to be able to wean before winter. Infant mortality is high (30–70%) and partly due to infanticide in Propithecus edwardsi,and perhaps Varecia variegata. Diurnal lemurs can live beyond 30 years in the wild and most females reproduce until death. Small-bodied Microcebus rufuslive up to 9 years without signs of senescence. Prolemur simusmigrates in search of new bamboo and mates, and related V. variegatamothers park their multiple offspring in “kindergartens,” protected by others while mothers forage. Interference competition among sympatric lemurs occurs. Anthropogenic factors, such as past selective logging and climate change may influence the declining density of E. rufifrons, P. simus, and P. edwardsiwhile not affecting the density of pair-living species.

Lice and Ticks of the Eastern Rufous Mouse Lemur, Microcebus rufus, with Descriptions of the Male and Third Instar Nymph of Lemurpediculus verruculosus (Phthiraptera: Anoplura)

Abstract Sucking lice and ticks were collected from live-trapped eastern rufous mouse lemurs, Microcebus rufus Geoffroy, in and around the periphery of Ranomafana National Park, southeastern Madagascar, from 2007 to 2009. Samples of 53 sucking lice (Insecta: Phthiraptera: Anoplura) and 28 hard ticks (Acari: Ixodidae) were collected from 36 lemur captures representing 26 different host individuals. All of the lice were Lemurpediculus verruculosus (Ward) (6 males, 46 females, 1 third instar nymph). Only the holotype female was known previously for this louse and the host was stated to be a “mouse lemur.” Therefore, we describe the male and third instar nymph of L. verruculosus and confirm M. rufus as a host (possibly the only host) of this louse. All of the ticks were nymphs and consisted of 16 Haemaphysalis lemuris Hoogstraal, 11 Haemaphysalis sp., and 1 Ixodes sp. The last 2 ticks listed did not morphologically match any of the Madagascar Haemaphysalis or Ixodes ticks for which nymphal stages have been described.

Teeth, Sex, and Testosterone: Aging in the World's Smallest Primate

Mouse lemurs (Microcebus spp.) are an exciting new primate model for understanding human aging and disease. In captivity, Microcebus murinus develops human-like ailments of old age after five years (e.g., neurodegeneration analogous to Alzheimers disease) but can live beyond 12 years. It is believed that wild Microcebus follow a similar pattern of senescence observed in captive animals, but that predation limits their lifespan to four years, thus preventing observance of these diseases in the wild. Testing whether this assumption is true is informative about both Microcebus natural history and environmental influences on senescence, leading to interpretation of findings for models of human aging. Additionally, the study of Microcebus longevity provides an opportunity to better understand mechanisms of sex-biased longevity. Longevity is often shorter in males of species with high male-male competition, such as Microcebus, but mouse lemurs are sexually monomorphic, suggesting similar lifespans. We collected individual-based observations of wild brown mouse lemurs (Microcebus rufus) from 2003–2010 to investigate sex-differences in survival and longevity. Fecal testosterone was measured as a potential mechanism of sex-based differences in survival. We used a combination of high-resolution tooth wear techniques, mark-recapture, and hormone enzyme immunoassays. We found no dental or physical signs of senescence in M. rufus as old as eight years (N = 189, ages 1–8, mean = 2.59±1.63 SE), three years older than captive, senescent congeners (M. murinus). Unlike other polygynandrous vertebrates, we found no sex difference in age-dependent survival, nor sex or age differences in testosterone levels. While elevated male testosterone levels have been implicated in shorter lifespans in several species, this is one of the first studies to show equivalent testosterone levels accompanying equivalent lifespans. Future research on captive aged individuals can determine if senescence is partially a condition of their captive environment, and studies controlling for various environmental factors will further our understanding of senescence.

Lemur Habitat and Dental Senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.

Diversity and Prevalence of Diarrhea-Associated Viruses in the Lemur Community and Associated Human Population of Ranomafana National Park, Madagascar

Diarrhea-associated viruses are common causes of morbidity in humans in developing countries; however, they have seldom been studied in wild primates despite their pathogenic and zoonotic potential. This is of particular concern in Madagascar, one of the world’s poorest and most biodiverse countries. To improve our understanding of diarrhea-associated viruses in human and nonhuman wild primates in Madagascar, we noninvasively collected fecal samples from 7 of the 12 lemur species of Ranomafana National Park, Madagascar and concurrently sampled humans living in proximity to the lemurs. We used standard molecular techniques to screen 84 lemur and 107 human samples for viral groups commonly associated with diarrheal disease in human populations: adenovirus, enterovirus, rotavirus, and norovirus (genogroups GI and GII). Of the seven lemur taxa examined, all were positive for one or more viral group and humans were positive for all viral groups. Norovirus GII was the most common, found in 27 % of lemurs and 37 % of humans, followed by adenovirus, found in 25 % of lemurs and 35 % of humans. The high prevalence (30–50 %) of most viral groups in mouse lemurs (Microcebus rufus) highlights their potential to serve as sentinals of pathogen spillover from humans to wild lemur populations. These results improve our understanding of the diversity and prevalence of key viral taxa in lemur and associated human populations. Further characterization of these viral group sequences has the potential to reveal novel viruses in lemurs and humans in Madagascar and would be needed to determine the zoonotic potential of the viruses detected.

A biogeographical perspective on the variation in mouse lemur density throughout Madagascar

Madagascar is home to the smallest primates in the world, the mouse lemurs (Microcebus species). Twenty-four species of mouse lemur are currently recognised and are found in variable ecosystems, from dry forests and spiny deserts to humid forests. Due to their widespread distribution and the large number of sympatric species, mouse lemurs can be used as a model to understand the linkages among species richness, population density, and habitat. As all lemurs are threatened by habitat loss and fragmentation, this information can also be used to inform conservation management. We hypothesise that on an island-wide scale, we will find higher population densities in western dry forests than in eastern humid forests because the western dry forests exhibit lower species richness, more sympatric habitat use, and lower resource stability than the eastern humid forests. We conducted a literature review of population density estimates of known mouse lemur species, and used those data to conduct a meta-analysis and estimate overall average population density by geographic region. Our findings suggest that mouse lemur species living in western dry forest generally exhibit higher densities than those in eastern humid forests. This may be partly explained by higher habitat fragmentation in western dry forests, where species co-occur, but is likely to be a function of the magnitude and variability in seasonally available resources in each forest type. Higher seasonality results in less constant food availability and lower levels of environmental predictability, fostering species capable of coping with environmental change and maintaining high densities throughout periods of resource paucity. Our study highlights the importance of conducting Microcebus population density research that adheres to standardised methodological approaches. We point to the need for population density estimates for several species for which data are lacking. Such knowledge is important to assess the conservation status of these species, but also to enhance our ability to identify the macro-biogeographical and local ecological drivers of interspecific and intraspecific variability in population density.

Field evaluation of synthetic lure (3-methyl-1-butanol) when compared to non odor-baited control in capturing Anopheles mosquitoes in varying land-use sites in Madagascar

BackgroundMalaria is the 4th largest cause of mortality in Madagascar. To better understand malaria transmission dynamics, it is crucial to map the distribution of the malaria vectors, mosquitoes belonging to the genus Anopheles. To do so, it is important to have a strong Anopheles-specific lure to ensure the maximum number of captures. Previous studies have isolated volatiles from the human skin microbiota and found the compound 3-methyl-1-butanol to be the most attractive to the malaria mosquito, Anopheles gambiae, in a laboratory setting; and recommended 3-methyl-1-butanol as a compound to increase An. gambiae captures in the field. To date, this compound’s ability to lure wild mosquitoes in differing land-use settings has not been tested. In this study, we evaluate the role of the synthetic compound, 3-methyl-1-butanol in combination with field produced CO2 in attracting Anopheles mosquitoes in varying land-use sites in Madagascar.MethodsCDC miniature light traps in combination with field produced CO2 were deployed in and around six villages near Ranomafana National Park, Madagascar. To test the role of 3-methyl-1-butanol in luring Anopheles mosquitoes, two traps were set in each land-use site (village, agricultural sites, and forested habitats affiliated with each village). One was baited with the synthetic odor and the other was kept as a non-baited control.ResultsWhile 3-methyl-1-butanol baited traps did capture An. gambiae s.l. in this study, we did not find traps baited with synthetic 3-methyl-1-butanol to be more successful in capturing Anopheles mosquitoes, (including Anopheles gambiae s.l.) than the non odor-baited control traps in any of the land-use sites examined; however, regardless of odor bait, trapping near livestock pens resulted in the capture of significantly more Anopheles specimens.ConclusionsA strong synthetic lure in combination with insecticide has great potential as a mosquito control. Our findings suggest that trapping mosquitoes near livestock in malaria endemic regions, such as Madagascar, may be more successful at capturing Anopheles mosquitoes than the proposed 3-1-methyl-butanol lure.

The Mouse Lemur, a Genetic Model Organism for Primate Biology, Behavior, and Health

Systematic genetic studies of a handful of diverse organisms over the past 50 years have transformed our understanding of biology. However, many aspects of primate biology, behavior, and disease are absent or poorly modeled in any of the current genetic model organisms including mice. We surveyed the animal kingdom to find other animals with advantages similar to mice that might better exemplify primate biology, and identified mouse lemurs (Microcebus spp.) as the outstanding candidate. Mouse lemurs are prosimian primates, roughly half the genetic distance between mice and humans. They are the smallest, fastest developing, and among the most prolific and abundant primates in the world, distributed throughout the island of Madagascar, many in separate breeding populations due to habitat destruction. Their physiology, behavior, and phylogeny have been studied for decades in laboratory colonies in Europe and in field studies in Malagasy rainforests, and a high quality reference genome sequence has recently been completed. To initiate a classical genetic approach, we developed a deep phenotyping protocol and have screened hundreds of laboratory and wild mouse lemurs for interesting phenotypes and begun mapping the underlying mutations, in collaboration with leading mouse lemur biologists. We also seek to establish a mouse lemur gene “knockout” library by sequencing the genomes of thousands of mouse lemurs to identify null alleles in most genes from the large pool of natural genetic variants. As part of this effort, we have begun a citizen science project in which students across Madagascar explore the remarkable biology around their schools, including longitudinal studies of the local mouse lemurs. We hope this work spawns a new model organism and cultivates a deep genetic understanding of primate biology and health. We also hope it establishes a new and ethical method of genetics that bridges biological, behavioral, medical, and conservation disciplines, while providing an example of how hands-on science education can help transform developing countries.

Aggression and hormones are associated with heterogeneity in parasitism and parasite dynamics in the brown mouse lemur

Animal behaviours, like aggression, can directly affect host health by influencing exposure to parasites. Aggressive individuals may experience an increase in agonistic interactions and contact rates with conspecifics, which might increase their probability of acquiring parasites. However, aggression is not the only factor that shapes parasitism; proximate mechanisms like hormone-modulated immunosuppression can also have broad impacts. Here, we hypothesized that high levels of aggression, cortisol and testosterone would be positively associated with parasitism and that aggressive individuals would play a larger role spreading parasites to conspecifics than would docile individuals. We measured aggression using the level of aggressive response to human handling during capture. Our aim was to examine associations between aggression and hormones (cortisol and testosterone) on variation in endo- and ectoparasitism in a population of wild mouse lemurs ( Microcebus rufus ) over a 3-year period. By tracking the movement of lice (directly transmitted parasites) in the population, we also examined the effect of host aggression on population-wide parasite dynamics. We show that animals with high testosterone and cortisol were more likely to exhibit aggressive behaviours, and cortisol was associated with significantly higher ectoparasite infestations. Aggressive individuals were significantly more infested by lice, and also donated significantly more lice to conspecifics in the population. Taken together, our results offer insight into the individual and population health costs of aggression, and empirical support of a trade-off between aggression and ectoparasitism, which may have driven the evolution of aggression and interactions with conspecifics.