Population dynamics of the Manyara monkey (Cercopithecus mitis manyaraensis) and vervet monkey (Chlorocebus pygerythrus) in Lake Manyara National Park, Tanzania.

Estimating population densities and their trends over time is essential for understanding primate ecology and for guiding conservation efforts. From 2011 through to 2019, we counted two guenon species during seasonal road transect surveys in Lake Manyara National Park: the Tanzania-endemic Manyara monkey Cercopithecus mitis manyaraensis (International Union for Conservation of Nature and Natural Resources, IUCN, Red List category of "endangered") and the vervet monkey Chlorocebus pygerythrus (Red List category of "least concern"). To account for imperfect detectability, we analysed the data in a line distance sampling framework, fitted species-specific detection functions, and subsequently estimated seasonal densities. To test for seasonal differences and yearly trends in the species-specific density estimates, we fitted generalized additive models. Seasonal point density estimates fluctuated considerably during the 9 years (2011-2019) of our study, ranging from 3 to 29 individuals km - 2 for Manyara monkeys and from 19 to 83 individuals km - 2 for vervet monkeys. Densities of both taxa did not differ seasonally, and we did not detect marked directional population trends. Our study illustrates the utility and limitations of line distance sampling for long-term primate monitoring. Beyond informing primate ecology and management, our results highlight the conservation importance of Lake Manyara National Park for primate conservation.

Predicting wildlife corridors for multiple species in an East African ungulate community.

Wildlife corridors are typically designed for single species, yet holistic conservation approaches require corridors suitable for multiple species. Modelling habitat linkages for wildlife is based on several modelling steps (each involving multiple choices), and in the case of multi-species corridors, an approach to optimize single species corridors to few or a single functional corridor for multiple species. To model robust corridors for multiple species and simultaneously evaluate the impact of methodological choices, we develop a multi-method approach to delineate corridors that effectively capture movement of multiple wildlife species, while limiting the area required. Using wildlife presence data collected along ground-based line transects between Lake Manyara and Tarangire National Parks, Tanzania, we assessed species-habitat association in both ensemble and stacked species distribution frameworks and used these to estimate linearly and non-linearly scaled landscape resistances for seven ungulate species. We evaluated habitat suitability and least-cost and circuit theory-based connectivity models for each species individually and generated a multi-species corridor. Our results revealed that species-habitat relationships and subsequent corridors differed across species, but the pattern of predicted landscape connectivity across the study area was similar for all seven species regardless of method (circuit theory or least-cost) and scaling of the habitat suitability-based cost surface (linear or non-linear). Stacked species distribution models were highly correlated with the seven species for all model outputs (r = 0.79 to 0.97), while having the greatest overlap with the individual species least-cost corridors (linear model: 61.6%; non-linear model: 60.2%). Zebra was the best single-species proxy for landscape connectivity. Overall, we show that multi-species corridors based on stacked species distribution models achieve relatively low cumulative costs for savanna ungulates as compared to their respective single-species corridors. Given the challenges and costs involved in acquiring data and parameterizing corridor models for multiple species, zebra may act as a suitable proxy species for ungulate corridor conservation in this system.

Road-based line distance surveys overestimate densities of olive baboons.

Estimating population density and population dynamics is essential for understanding primate ecology and relies on robust methods. While distance sampling theory provides a robust framework for estimating animal abundance, implementing a constrained, non-systematic transect design could bias density estimates. Here, we assessed potential bias associated with line distance sampling surveys along roads based on a case study with olive baboons (Papio anubis) in Lake Manyara National Park (Tanzania). This was achieved by comparing density estimates of olive baboons derived from road transect surveys with density estimates derived from estimating the maximum number of social groups (via sleeping site counts) and multiplying this metric with the estimated average size of social groups. From 2011 to 2019, we counted olive baboons along road transects, estimated survey-specific densities in a distance sampling framework, and assessed temporal population trends. Based on the fitted half-normal detection function, the mean density was 132.5 baboons km-2 (95% CI: 110.4-159.2), however, detection models did not fit well due to heaping of sightings on and near the transects. Density estimates were associated with relatively wide confidence intervals that were mostly caused by encounter rate variance. Based on a generalized additive model, baboon densities were greater during the rainy seasons compared to the dry seasons but did not show marked annual trends. Compared to estimates derived from the alternative method (sleeping site survey), distance sampling along road transects overestimated the abundance of baboons more than threefold. Possibly, this overestimation was caused by the preferred use of roads by baboons. While being a frequently used technique (due to its relative ease of implementation compared to spatially randomized survey techniques), inferring population density of baboons (and possibly other species) based on road transects should be treated with caution. Beyond these methodological concerns and considering only the most conservative estimates, baboon densities in LMNP are among the highest across their geographic distribution range.

Camera-trap data do not indicate scaling of diel activity and cathemerality with body mass in an East African mammal assemblage.

Diel activity patterns of animal species reflect constraints imposed by morphological, physiological, and behavioral trade-offs, but these trade-offs are rarely quantified for multispecies assemblages. Based on a systematic year-long camera-trap study in the species-rich mammal assemblage of Lake Manyara National Park (Tanzania), we estimated activity levels (hours active per day) and circadian rhythms of 17 herbivore and 11 faunivore species to determine the effects of body mass and trophic level on activity levels and cathemerality (the degree to which species are active throughout the day and night). Using generalized least squares and phylogenetic generalized least squares analyses, we found no support for the hypothesis that trophic level is positively associated with activity levels. We found no support for activity levels to scale positively with body mass in herbivores or to differ between ruminants and nonruminants; in faunivores, we also did not detect relationships between body mass and activity levels. Cathemerality was positively associated with activity levels but did not scale significantly with body mass. Overall, our findings caution against trophic level or body mass-associated generalized conclusions with regard to diel activity patterns.

Long-term persistence of wildlife populations in a pastoral area.

Facilitating coexistence between people and wildlife is a major conservation challenge in East Africa. Some conservation models aim to balance the needs of people and wildlife, but the effectiveness of these models is rarely assessed. Using a case-study approach, we assessed the ecological performance of a pastoral area in northern Tanzania (Manyara Ranch) and established a long-term wildlife population monitoring program (carried out intermittently from 2003 to 2008 and regularly from 2011 to 2019) embedded in a distance sampling framework. By comparing density estimates of the road transect-based long-term monitoring to estimates derived from systematically distributed transects, we found that the bias associated with nonrandom placement of transects was nonsignificant. Overall, cattle and sheep and goat reached the greatest densities and several wildlife species occurred at densities similar (zebra, wildebeest, waterbuck, Kirk's dik-dik) or possibly even greater (giraffe, eland, lesser kudu, Grant's gazelle, Thomson's gazelle) than in adjacent national parks in the same ecosystem. Generalized linear mixed models suggested that most wildlife species (8 out of 14) reached greatest densities during the dry season, that wildlife population densities either remained constant or increased over the 17-year period, and that herbivorous livestock species remained constant, while domestic dog population decreased over time. Cross-species correlations did not provide evidence for interference competition between grazing or mixed livestock species and wildlife species but indicate possible negative relationships between domestic dog and warthog populations. Overall, wildlife and livestock populations in Manyara Ranch appear to coexist over the 17-year span. Most likely, this is facilitated by existing connectivity to adjacent protected areas, effective anti-poaching efforts, spatio-temporal grazing restrictions, favorable environmental conditions of the ranch, and spatial heterogeneity of surface water and habitats. This long-term case study illustrates the potential of rangelands to simultaneously support wildlife conservation and human livelihood goals if livestock grazing is restricted in space, time, and numbers.

Community-based wildlife management area supports similar mammal species richness and densities compared to a national park.

Community-based conservation models have been widely implemented across Africa to improve wildlife conservation and livelihoods of rural communities. In Tanzania, communities can set aside land and formally register it as Wildlife Management Area (WMA), which allows them to generate revenue via consumptive or nonconsumptive utilization of wildlife. The key, yet often untested, assumption of this model is that economic benefits accrued from wildlife motivate sustainable management of wildlife. To test the ecological effectiveness (here defined as persistence of wildlife populations) of Burunge Wildlife Management Area (BWMA), we employed a participatory monitoring approach involving WMA personnel. At intermittent intervals between 2011 and 2018, we estimated mammal species richness and population densities of ten mammal species (African elephant, giraffe, buffalo, zebra, wildebeest, waterbuck, warthog, impala, Kirk's dik-dik, and vervet monkey) along line transects. We compared mammal species accumulation curves and density estimates with those of time-matched road transect surveys conducted in adjacent Tarangire National Park (TNP). Mammal species richness estimates were similar in both areas, yet observed species richness per transect was greater in TNP compared to BWMA. Species-specific density estimates of time-matched surveys were mostly not significantly different between BWMA and TNP, but elephants occasionally reached greater densities in TNP compared to BWMA. In BWMA, elephant, wildebeest, and impala populations showed significant increases from 2011 to 2018. These results suggest that community-based conservation models can support mammal communities and densities that are similar to national park baselines. In light of the ecological success of this case study, we emphasize the need for continued efforts to ensure that the BWMA is effective. This will require adaptive management to counteract potential negative repercussions of wildlife populations on peoples' livelihoods. This study can be used as a model to evaluate the effectiveness of wildlife management areas across Tanzania.

Comparative knowledge, attitudes, and practices regarding anthrax, brucellosis, and rabies in three districts of northern Tanzania.

BACKGROUND: Knowledge, attitudes, and practices (KAP) surveys regarding zoonotic diseases are crucial to understanding the extent of knowledge among citizens and for guiding health-related education programs. METHOD: Employing a structured questionnaire, we interviewed residents (n = 388) in three districts of northern Tanzania (Karatu n = 128, Monduli n = 114, Babati n = 146) to assess knowledge, attitudes and reported practices regarding three zoonotic diseases that occur in the region (anthrax, brucellosis, and rabies). We used generalized linear mixed effects models and multi-model inference to identify demographic correlates of knowledge. RESULTS: Proportional average district- and disease- specific knowledge scores ranged from 0.14-0.61. We found positive correlations between age and knowledge of symptoms, causes and treatments of anthrax (three districts), brucellosis (three districts), and rabies (one district). Gender, ethnic identity, formal education and ownership of livestock or dogs had variable effects on knowledge among the interviewed population. Risk perceptions regarding different diseases varied across districts and were positively correlated with knowledge of the specific diseases. Direct interactions with livestock and domestic dogs were reported to occur across all demographic groups, suggesting that most people living in rural settings of our study area are potentially exposed to zoonotic diseases. Behaviors which may favor transmission of specific pathogens (such as consumption of raw milk or meat) were occasionally reported and varied by district. Wildlife was generally regarded as negative or neutral with regard to overall veterinary and human health. CONCLUSION: The combination of variable knowledge about zoonotic diseases in the three districts, reported occurrence of practices that are conducive to pathogen transmission, and previously documented circulation of pathogens causing anthrax, brucellosis and rabies in our study system, call for health education programs embedded in a holistic One Health approach.

Large mammal declines and the incipient loss of mammal-bird mutualisms in an African savanna ecosystem.

Over the past half-century, large mammal populations have declined substantially throughout East Africa, mainly due to habitat loss and unsustainable direct exploitation. While it has been acknowledged that the loss of large mammals can have direct and cascading effects on community composition and ecosystem characteristics, limited quantitative work has been done on how declines of large herbivore populations impacts the abundance of mutualistic symbionts. Using a space-for-time observational approach, we quantified the large mammal community alongside the densities, host preferences and behaviors of mutualistic red-billed oxpeckers (Buphagus erythrorhynchus), and yellow-billed oxpeckers (Buphagus africanus) in northern Tanzania. At the landscape scale, mammal community composition was substantially less diverse in highly human-dominated areas when compared with more protected areas, with an observed complete loss of large wild mammal species in two study areas. Mirroring this trend, oxpecker densities were lowest in the least protected areas, and highest in fully protected areas. Using resource selection functions implemented via generalized linear models at different scales, we found that oxpeckers (1) were predominantly (67% of red-billed oxpeckers; 70% of yellow-billed oxpeckers) feeding on larger (between 500kg and 1500kg) ungulate host species within the mammal community, (2) usually preferred feeding on larger individuals (adults and males) within a specific host species population, and (3) preferred hosts that were more tolerant of their presence. In particular, cattle were especially intolerant of oxpecker presence and were relatively effective in displacing oxpeckers. We found little evidence that oxpecker feeding was parasitic across all host species; wound feeding was only observed on giraffe, comprising 6% and 4% of feeding behavior in red-billed and yellow-billed oxpeckers respectively. Thus, a loss of large-bodied and oxpecker tolerant host species is a likely explanation for declines of oxpecker populations in human dominated landscapes, which may have further cascading effects.

Effects of acaricide treatment and host intrinsic factors on tick acquisition and mortality in Boran cattle.

Ticks and associated pathogens pose serious threats to the health of livestock. To assess the efficacy of acaricide dip treatment (cypermethrin, chlorpyrifos, piperonyl butoxide, citronella), we assessed post-treatment tick acquisition and tick mortality of free-ranging Boran cattle inhabiting a wildlife-cattle ranch in Northern Tanzania. Because host intrinsic variables and exposure to ticks may substantially affect tick acquisition, we incorporated host sex, body mass, health condition, and distance traveled in models of tick acquisition. Using generalized linear mixed models that accounted for non-independence of individuals, we found that tick species richness increased with host body mass but was not significantly related to other factors. In contrast, tick abundance increased with time since acaricide treatment, was positively correlated with host body mass, and was higher in female than male cattle. Distance traveled and health condition did not predict tick acquisition. Overall, these patterns were similar when separately analyzing acquisition of the more common tick species (Rhipicephalus pulchellus, R. sanguineus sensu lato, and R. praetextatus). Logistic regression models suggested that tick mortality was high for a few days after acaricide dip treatment but declined steeply post-treatment; 3.5 days after treatment, only 50% of ticks were dead, and mortality declined further thereafter. Our results provide new information regarding tick acquisition patterns in this system including female-biased tick parasitism and support for the hypothesis that increased host body mass provides greater resources and thus supports higher ectoparasite abundance and species richness. The limited acaricide duration of action and effectiveness on all tick species calls for adjusting tick management practices.

Ethnoecological knowledge of ticks and treatment of tick-borne diseases among Maasai people in Northern Tanzania.

AIM: The aim of this study was to understand traditional knowledge of tick ecology and remedies for tick-borne diseases (TBDs) among the Maasai people in northern Tanzania. MATERIALS AND METHODS: Semi-structured interviews were conducted among specific groups likely to be knowledgeable about tick ecology and TBDs in livestock among the Maasai people. RESULTS: A total of 25 plant species belonging to 18 families were used to treat 8 different TBDs of livestock. Most of the plant species used were of Fabaceae and Burseraceae families. Aloe volkensii, Cissus grandifolia, and Terminalia brownii were the most commonly used plant species. The major plant growth form used was trees, while stems and bark were the main plant parts used. Most treatments were taken orally. CONCLUSION: Maasai people have substantial knowledge on tick ecology exemplified by their ability to differentiate between different tick species and the range of remedies for each of the TBDs. Because traditional ethnoveterinary remedies are frequently utilized, their effectiveness should be further investigated.

Seasonal patterns of mixed species groups in large East African mammals.

Mixed mammal species groups are common in East African savannah ecosystems. Yet, it is largely unknown if co-occurrences of large mammals result from random processes or social preferences and if interspecific associations are consistent across ecosystems and seasons. Because species may exchange important information and services, understanding patterns and drivers of heterospecific interactions is crucial for advancing animal and community ecology. We recorded 5403 single and multi-species clusters in the Serengeti-Ngorongoro and Tarangire-Manyara ecosystems during dry and wet seasons and used social network analyses to detect patterns of species associations. We found statistically significant associations between multiple species and association patterns differed spatially and seasonally. Consistently, wildebeest and zebras preferred being associated with other species, whereas carnivores, African elephants, Maasai giraffes and Kirk's dik-diks avoided being in mixed groups. During the dry season, we found that the betweenness (a measure of importance in the flow of information or disease) of species did not differ from a random expectation based on species abundance. In contrast, in the wet season, we found that these patterns were not simply explained by variations in abundances, suggesting that heterospecific associations were actively formed. These seasonal differences in observed patterns suggest that interspecific associations may be driven by resource overlap when resources are limited and by resource partitioning or anti-predator advantages when resources are abundant. We discuss potential mechanisms that could drive seasonal variation in the cost-benefit tradeoffs that underpin the formation of mixed-species groups.

Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood.

BACKGROUND: Antenatal immune experience with Wuchereria bancrofti due to maternal filariasis may influence susceptibility to infection. We tested the hypothesis that filarial-specific T cell responses at birth that are indicative of in utero tolerance or sensitization affect the evolution of filarial-specific immunity and susceptibility to W. bancrofti infection during childhood. METHODS: A birth-cohort study of 159 Kenyan newborns was performed. Cord blood and peripheral blood were obtained annually to age 7 years and were assayed for filarial infection and filarial antigen-driven interferon (IFN)- gamma , interleukin (IL)-2, IL-5, and IL-13 production by lymphocytes. RESULTS: There was a 12.9-fold (95% confidence interval [CI], 2.5-107.2-fold) and a 4.8-fold (95% CI, 1.7-12.9-fold) increased risk of infection for immune-tolerant newborns (maternal infection present during gestation, with no filarial antigen-driven cord blood T cell response [n = 25]), compared with immune-sensitized (maternal infection present with cord blood T cell response [n = 24]) and unexposed (maternal infection absent [n = 110]) newborns. Cytokine responses developed at a later age in tolerant newborns, were characterized by impaired IFN-gamma responses, and contrasted with those of filarial-sensitized newborns, who had sustained and elevated IL-5 and IL-13 responses to age 7 years. CONCLUSION: Prenatal immune experience, as determined by whether in utero priming to filarial antigen occurs, is a major determinant of childhood susceptibility to W. bancrofti infection.

The effects of maternal helminth and malaria infections on mother-to-child HIV transmission.

OBJECTIVE: To investigate the effect of helminth and/or malaria infection on the risk of HIV infection in pregnant women and its transmission to their offspring. DESIGN: A retrospective cohort study of pregnant Kenyan women and their offspring from term, uncomplicated vaginal deliveries (n = 936) with a nested case-control study. METHODS: We determined the presence of HIV, malaria, schistosomiasis, lymphatic filariasis, and intestinal helminthes in mothers and tested for HIV antibodies in 12-24 month-old offspring of HIV-positive women. We related these findings to the presence of cord blood lymphocyte activation and cytokine production in response to helminth antigens. RESULTS: HIV-positive women (n = 83, 8.9% of all women tested) were 2-fold more likely to have peripheral blood and/or placental malaria (P < 0.025) and a 2.1-fold greater likelihood of lymphatic filariasis infection (P < 0.001) compared to location-and-parity matched HIV-negative women. Women with HIV and malaria tended to show an increased risk for mother-to-child-transmission (MTCT) of HIV, although this difference was not significant. MTCT of HIV, however, was significantly higher in women co-infected with one or more helminthes (48%) verses women without helminth infections (10%, P < 0.01; adjusted odds ratio, 7.3; 95% confidence interval, 2.4-33.7). This increased risk for MTCT of HIV correlated with cord blood lymphocytes production of interleukin-5/interleukin-13 in response to helminth antigens (P < 0.001). CONCLUSION: Helminth co-infection is associated with increased risk for MTCT of HIV, possibly by a mechanism in which parasite antigens activates lymphocytes in utero. Treatment of helminthic infections during pregnancy may reduce the risk of MTCT of HIV.

Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya.

To determine whether maternal filariasis influences the risk of infection by and immunity to Wuchereria bancrofti in children, we performed a cross-sectional study in an area of Kenya where filariasis is endemic. Residents of 211 households were enrolled; 376 parents and 938 of their offspring between the ages of 2 and 17 years were examined for filarial infection status as determined by blood-borne microfilariae and filarial antigenemia. Children of infected mothers had a three- to fourfold increased risk of filarial infection, as ascertained by circulating filarial antigen, relative to children of uninfected mothers (P < 0.001). Paternal infection did not correlate with childhood infection status, indicating a specific maternal effect. Peripheral blood mononuclear cells from children of filaria-infected mothers (n = 33) had higher levels of constitutive interleukin-5 (IL-5) and IL-10, increased microfilarial antigen-specific IL-5 production, and diminished microfilarial antigen-driven lymphocyte proliferation than cells from children of uninfected mothers (n = 46; P < 0.05). In contrast, there were no differences between the two groups in adult worm antigen-driven gamma interferon, IL-2, IL-4, IL-5, and IL-10 production and lymphocyte proliferation. These data indicate that maternal filarial infection increases childhood susceptibility to W. bancrofti and skews filaria-specific immunity toward a Th2-type cytokine response. The results support the notion that in utero exposure to filarial antigens affects the natural history of filariasis during childhood.

Acquired immune responses to Plasmodium falciparum merozoite surface protein-1 in the human fetus.

Infants born in areas of stable malaria transmission are relatively protected against severe morbidity and high density Plasmodium falciparum blood-stage infection. This protection may involve prenatal sensitization and immunologic reactivity to malaria surface ligands that participate in invasion of red cells. We examined cord blood T and B cell immunity to P. falciparum merozoite surface protein-1 (MSP-1) in infants born in an area of stable malaria transmission in Kenya. T cell cytokine responses to the C-terminal 19-kDa fragment of MSP-1 (MSP-1(19)) were detected in 24 of 92 (26%) newborns (4-192 IFN-gamma and 3-88 IL-4-secreting cells per 10(6)/cord blood lymphocytes). Peptide epitopes in the N-terminal block 3 region of MSP-1 also drove IFN-gamma and/or IL-13 production. There was no evidence of prenatal T cell sensitization to liver-stage Ag-1. A total of 5 of 86 (6%) newborns had cord blood anti-MSP-1(19) IgM Abs, an Ig isotype that does not cross the placenta and is therefore of fetal origin. The frequency of neonatal B cell sensitization was higher than that indicated by serology alone, as 5 of 27 (18%) cord blood samples contained B cells that produced IgG when stimulated with MSP-1(19) in vitro. Neonatal B cell IgG responses were restricted to the Q-KNG allele of MSP-1(19), the major variant in this endemic area, whereas T cells responded to all four MSP-1(19) alleles evaluated. In utero sensitization to MSP-1 correlated with the presence of malaria parasites in cord blood (chi(2) = 20, p < 0.0001). These data indicate that prenatal sensitization to blood-stage Ags occurs in infants born in malaria endemic areas.