Behavioral and Environmental Correlates of Parasite Burden in Eulemur cinereiceps from Southeastern Madagascar
Martin, Sara Katharine
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The grey-headed lemur, Eulemur cinereiceps, is among the top 25 most endangered primates. This work investigated behavioral and environmental correlates of parasite exposure through the evaluation of parasite burden in two wild metapopulations of E. cinereiceps in southeastern Madagascar. Understanding the relationship between primate behavior, environment and primate disease risk is critical for the conservation of primates and their ecosystems. The presence and distribution of parasites among primate populations is the result of primate exposure to parasites through both behavioral and environmental variables. Primate exposure to parasites is often the result of either host social behaviors or habitat use behaviors. Behavior data and non-invasive fecal sampling were collected during two field seasons in 2008 at the Agnalazaha and Manombo Forests. Both forests are comprised of low canopy coastal rainforest with mixtures of unforested areas, however the Agnalazaha forest is substantially more disturbed when taking local community use and deforestation into account. Phenology and GPS data were also recorded at this time. This is one of the few studies to unite repetitive fecal sample collection and specific behavioral data from habituated and identified individuals. In addition, data collection at two field sites allowed for a comparison of environmental characteristics, primarily habitat disturbance. This is the first study to identify parasites infecting E. cinereiceps. Four nematodes and one protozoan parasite were found in the fecal samples. Two pinworms, Callistoura and Lemuricola, were the most commonly found parasites during both field seasons. Trichuris was found in only one forest fragment during the second field season. Additionally, an Entamoeba species and Ascarididae species were identified. All of the parasites identified in this study are likely transferred through fecal-oral contamination and are expected to be relatively asymptomatic in E. cinereiceps, allowing host-parasite interactions to be studied without strong confounding parasite-avoidance behaviors. In addition, this study may serve as a model for more virulent parasites in other systems. A field and laboratory diagnostic study validated fecal parasite recovery techniques. Preservation solution had significant impacts on parasite recovery and results indicate that 10% formalin is superior to 90% ethanol. Recovery technique also had an impact on parasite recovery. Fecal sedimentation was a more sensitive method than fecal flotation, although the difference was not significant. When using 90% ethanol as a preservation solution, parasite recovery approached those stored in 10% formalin when using fecal sedimentation rather than fecal flotation. Maximum fecal parasite species richness occurred when at least 2-3 grams of feces, or 67-75% of the fecal sample was utilized in repeated fecal flotation trials. Flotation solution and homogeneity of the feces did not affect parasite recovery yields. The behavioral and environmental correlates of Eulemur cinereiceps parasite infection parameters varied by parasite species. Overall, neither behavior, nor environmental variables were a better predictor of parasite burden in the Agnalazaha and Manombo E. cinereiceps populations. Parasite infection frequency and prevalence increased during the fall/dry season. In some cases this may relate to behavioral differences between the two seasons, although it is unlikely to be the result of increased physical contact due to infant births. Callistoura infection was best predicted by social behaviors including group size and physical contact between conspecifics. Lemuricola infection was best predicted by habitat use behaviors, travel time and time spent on the ground, which are both likely mediated by environment disturbance variables. Lemuricola frequency and prevalence was significantly greater in the more disturbed forest where travel time and time spent on the ground were also significantly greater. These results support previous research on Lemuricola infection in other lemur host species. Trichuris infection was found during only one field season in only one forest fragment and it's potential for cross-species contamination is currently unknown. Entamoeba infection was best predicted by environmental variables and the corresponding habitat use behaviors. Previous studies identifying ascarid parasites in other lemur species found that infection correlated negatively with habitat quality and age. The ascarid eggs found in the current study do not resemble those found in other primate studies. Ascarid infection in E. cinereiceps was best predicted by environmental variables; ascarid eggs were recovered only from study groups whose home range overlapped areas of water. Although height in the canopy was predicted to correlate negatively with parasite burden due to the mode of fecal contamination transmission, height did not vary significantly with parasite species richness or any parameters of parasite burden. Each of the parasites identified in this study are likely transferred between host individuals by fecal-oral contamination. However, the host behavioral and environmental variables mediating host exposure and parasite burden varies for each parasite species suggesting that even parasites with similar modes of transmission may transfer between hosts and spread through populations using different mechanisms. This further suggests that clumping parasite families or those with general similarities may distract from more detailed patterns of host-parasite infection in wildlife communities.