Reconciling environmental protection, health, and development, through the monitoring of Pteropus livingstonii populations in the Comoros

Project Leader: Dr IBOUROI Mohamed Thani

Project Rationale:

The Comoros archipelago is an important biodiversity hotspot. It is home to a remarkable faunal and floristic diversity with a high rate of endemism due to a high habitats heterogeneity and the geographical isolation of the islands. The landscape diversities and the number of biogeographic ecoregions make this archipelago one of the richest areas in terms of biodiversity in the Indian Ocean (Louette et al. 2004). However, island ecosystems are particularly vulnerable to sea level rise, landslides and other natural disasters accompanying global change. These natural impacts lead to forest areas reduction, scarcity and biodiversity loss. Such natural impacts are accentuated by direct and indirect human activity effects (unsustainable natural resources use, urbanization, introduction of species, etc.). The high level of endemism of fauna and flora in the Comoros implies that there are no equivalents anywhere else in terms of genetic to be kept as an alternative solution (Herfindal et al. 2014). Indeed, this biodiversity of Comoros faces extreme risk of extinction as the natural habitats of this islands have been lost and altered, mainly due to anthropogenic activities (Ibouroi et al. 2018). More than 85% of the natural habitat was converted into farmland, urban areas, and secondary forests between 1972 and 1987 and the islands are experiencing one of the highest rates of habitat loss in the world (9.3% each year, FAO, 2010; Goodman et al., 2010; Ibouroi et al. 2018). According to a recently published study (Ibouroi et al. 2021), more than 90% of human populations in the Comoros depend highly on forests and natural resources (exploitation of construction timber, cultivation in forest environments, charcoal production, etc.). This overexploitation of natural resources is the result of (1) strong population growth (2.5% per year) combined with high human population density (300 inds/km², Boussougou et al. 2015; Goldewijk, 2005) but also (2) the high levels of poverty (Elvidge et al. 2009), leading to an increase of natural habitats exploitation by local people, to meet their daily needs. This strong dependence on natural resources appears to be the most important blocking point in the hope of preserving the biodiversity of the Comoros island ecosystems. Rural communities in Comoros are however aware of the importance of biodiversity and the impact of their practices on biodiversity and natural habitats (Ibouroi et al. 2021). This unsustainable natural resource use is thus a question of survival for local populations. In this context, ensuring the long-term conservation of biodiversity and natural habitats in the Comoros will only be possible by adopting strategies to tackle poverty in the rural populations and thus reducing their dependence on forest resources in parallel with ecological studies.

 

The Livingstone’s fruit bat (Pteropus livingstonii) is a Critically Endangered species restricted in the mountain forests of the Comoros islands of Anjouan and Mohéli (Ibouroi et al. 2018). The species is considered one of the most threatened bats in the world (UCN Red List 2022). As an important pollinator and seed disperser of both native and cultivated plants, the species is thus of crucial importance for dynamics and natural ecosystems functioning through the regeneration of natural forests as well as cultivated plantations (Ibouroi et al. 2018). Being a geographically isolated species (in Anjouan and Mohéli), it has a relatively small population size (1200 individuals, Ibouroi et al. 2018); it is therefore particularly vulnerable to anthropogenic disturbances and habitat loss. Moreover, being a relatively long-lived species, P. livingstonii exhibits slow population dynamics which makes it even more sensitive to disturbances. It also has a low capacity to restore populations after disturbance. Recent assessments highlighted that the potential habitats of species have experienced significant reductions in recent decades (Sewall et al. 2011, Ibouroi et al. 2018). This reduction leads to disruptions in social structure that can lead to rapid population sizes decreasing (Hutson et al. 2001, Vaughan et al. 1997, Tink et al. 2014). A conservation strategy for the species is urgently needed to ensure the long-term viability of the species. Being a keystone species for the fauna and flora of the Comoros, implementing conservation measures for the species will allow to preserve the whole natural forests of Anjouan and Mohéli and the fauna and flora they harbor.

Bats are known to be reservoirs of a wide variety of infectious agents, and in particular of viruses (coronavirus, filovirus, henipavirus, etc.; Kohl and Kurth, 2014; Kuzmin et al. 2011; Simons et al. 2014). Some bat species of the genus Pteropus, to which the Livingstone flying fox species belongs, host emerging viruses such as Hendra and Nipah, that can have devastating effects on livestock (pigs, horses) and human populations. The first emergence of the Nipah virus resulted, for example, from several factors associated with human activities, in particular deforestation and the replacement of natural habitats of bats by agricultural (mangoes) and intensive pig farming, in Malaysia (Pulliam et al. 2012). The destruction of natural areas and climate change are also identified as factors causing the emergence of the Hendra virus in Australia, and a recent study underlines the importance of implementing an approach integrating environmental change and bat conservation, in order to understand and fight against the risk of emergence of these viruses (Eby et al. 2022). Although transmission pathways of infectious agents between bats and the human population sometimes remain enigmatic (Joffrin et al. 2018), habitat disturbance forces bat to feed on trees in plantations and gardens, and human can then ingest their saliva, urine, or excrement by biting into a fruit that is covered with it. In the Comoros, the ability of P. livingstonii to move between distant forest fragments for instance between roosting and feeding sites, its gregarious social structure, its long lifespan favor its closeness to humans (direct consumption, consumption of fruits that have been in contact with bats, contact via guano, saliva or urine of bats etc.), which increases exposure, could promotes the spread of infectious agents with the potential for rapid and wide-area dispersal and increases the likelihood that an infection transmitted between bats and humans or intermediate hosts (Calisher et al., 2006).

To date, no study has investigated the presence of infectious agents in this species. A significant diversity of viruses, however, has been detected in other fruit bat species from the Southwestern Indian Ocean, including viral families with high zoonotic potential: coronavirus, paramyxovirus, filovirus, etc. (e.g. Razanajatovo et al. 2015; Joffrin et al. 2019; Iehlé et al. 2007; Mélade et al. 2016; Brooke et al. 2019; Lebarbenchon et al. 2022). In this context, identifying the diversity and factors governing viral transmission in P. livingstonii represents a major challenge in a "One Health" development perspective, combining the health of ecosystems, the conservation of this emblematic species, but also the health of human populations and their economic development. How can the conservation of P. livingstonii and its natural habitat be reconciled with the presence and well-being of human populations? Faced with this complexity and the interconnections between environmental degradation, animal health, human health but also the survival of local populations who are highly dependent on forest resources, we propose here an interdisciplinary project which combine biological, ecological, epidemiological and agricultural aspects, implementing original approaches that respect all dimensions of health and conservation.

 

Project Approach:

1-Monitoring population trajectory and demographic parameters with noninvasive genetic sampling of the Critically Endangered Livingstone’s flying fox and assessing long-term conservation strategies. Establishing effective wildlife conservation measures requires demographic information such as population size, survival probability, and recruitment rate (Williams et al. 2002). These parameters, however, can be extremely difficult to obtain, especially for threatened species, which are often rare and sometimes occupy inaccessible areas. To estimate the population size of threatened species, many biologists use direct counts (O’Shea et al. 2003). However, direct counts are biased due to imperfect detection (Thomas et al. 1989, Kunz 2003), meaning this method provides only indices of a population size, potentially leading to erroneous conclusions regarding population trends when detection probability is not constant over time (Kunz et al. 2009, Archaux et al. 2012, Gervasi et al. 2014). Over the last 50 yr, capture–mark–recapture (CMR) approaches have been developed to address the difficulties associated with estimating population size and demographic parameters in animal populations (Nichols 1992, Pradel et al. 1997). However, despite their robustness and methodological flexibility, conventional CMR methods can be problematic to apply for secretive or wide-ranging species occurring at low density such as P. livingstonii (Miller et al. 2005). As CMR requires the physical handling of individuals, it is a time-consuming approach for rare species. Moreover, physical capture often disturbs and can sometimes even injure or kill animals, posing ethical issues, especially as regards threatened species such as P. livingstonii (Ibouroi et al. 2021b). Genetic data obtained from the noninvasive sampling of diverse materials, such as hair or fecal material, can be used to identify individuals, minimizing the risk and stress for animals (Taberlet and Luikart 1999). Noninvasive genetic sampling (NIGS) thus represents an alternative option to traditional CMR methods to acquire the data necessary to estimate demographic parameters— data such as dispersal patterns (Valiere et al. 2003), survival rates and population trends—using a CMR approach (Nichols 1992, Marucco et al. 2009, Ibouroi et al. 2021b). Over the two last decades, NIGS has become increasingly popular for wildlife monitoring (see, e.g., Morin and Woodruff, 1996, Taberlet and Luikart 1999, Bellemain and Taberlet 2004, Horvath et al. 2005, Boston et al. 2012) and has been successfully used to obtain information relevant to conservation issues for many species, including birds (Horvath et al. 2005), brown bears (Ursus arctos; De Barba et al. 2010), or large primates (e.g., Pan troglodytes; Arandjelovic and Vigilant 2018). Despite the fact that NIGS capture–mark–recapture (NIGS-CMR) is a well-established method, few studies have used this method to focus on fruit bat species in tropical forests (though see Baldwin et al. 2010). Ibouroi et al. (2021b) compared (1) NIGS-CMR with conventional CMR to determine their potential in estimating demographic parameters of fruit bats. Using Livingstone’s fruit bats (Pteropus livingstonii) fecal samples, they found that in comparison to conventional CMR, NIGS-CMR offers a better method for estimating demographic parameters and subsequently for conducting long-term population monitoring in flying foxes due to the fact that (1) sample collection is easy and the level of genotyping errors in the laboratory is low and (2) it is cheaper, less time-consuming, and less disturbing to individual animals. The main aim of this first part of the project is to use non-invasive genetic sampling (feces) and markrecapture tools to provide better abundance estimates, population trends and demographic parameter such as survival probability, and recruitment rate of the critically endangered P. livingstonii populations with higher precision of the population’s trajectory, which is needed for long-term conservation strategies.

2- Assessing pathogen-host interactions in Livingstone’s flying fox Bats are natural reservoirs for a variety of emerging viruses that cause significant disease in humans and domestic animals. The emergence of zoonotic diseases is increasing globally and mammals, including flying fox, are major sources of emerging and re-emerging pathogens. According to many studies, emerging viruses are permanently maintained in a population, often in the absence of disease so the population of Livingstone’s flying is a potential reservoir of these emerging viruses. Because of (1) the high rate of natural habitat conversion into agricultural in the Anjouan Islands (Ibouroi et al. 2018a) favoring bats proximity and interactions with humans and domestic animals; and (2) the fact that drivers of disease emergence include anthropogenic pressures (e.g., agricultural intensification) and climate change at global scale, assessing the diversity of infectious agents on this species and identifying those that may represent a threat to local communities and livestock is of primary importance. The main objective of this second part of the project is to identify the diversity of infectious agents including virus and bacteria, and the associated health risks. More specifically, we aim at: (1) Identifying the presence and diversity of viruses, in particular for viral families of zoonotic potential: Henipavirus, Filovirus, Coronavirus, etc. (2) Characterizing the bacterial community (microbiota) associated with P. livingstonii, and potential pathogenic bacteria. (3) Set-up a long-term monitoring of infectious agents associated with the species, to prevent spillover to other hosts, including humans. We will also use non-invasive genetic sampling to address these objectives. Previous studies based on the collection of fresh feces have provided detailed information on virus shedding dynamics in tropical bat colonies, with limited disturbance and stress associated with sampling (e.g. Joffrin et al. 2022). This second part of the project will therefore not require additional field sampling; we will rather optimize laboratory protocols in order to use every single feces sample to both the demographic and epidemiological studies.

3- Developing and maintaining sustainable production of crops for local human benefit to reduce natural habitats fragmentation and loss in the Anjouan Island. According to recent studies, the Comoros Islands are experiencing one of the highest rates of habitat loss in the word. Other studies highlighted that poverty and a lack of access to basic services are main drivers of unsustainable natural resource use by rural people in Comoros. Ibouroi et al. (2021) concluded that biodiversity conservation of the Comoros archipelagos may benefit for plan aiming at (1) developing and maintaining sustainable production of crops that could allow enhancing livelihoods and well-being of all social groups and thus limiting natural habitat disturbances and reducing the conversion of forest into farmland. Such an alternative livelihood project is used as a tool for achieving biodiversity conservation. In this third part of our project, we aim at implementing a joint development plan, which will allow developing economic income-generating activities to the benefit of local populations in near forests with colonies of Livingstone’s flying fox in Anjouan. More specifically, we aim at supporting the development of ylang-ylang plantations for local population of Anjouan which could allow them to be less dependent to forest resources.

Projet 2:

Saving Critically Endangered Species: Using conservation genetic and socio-economic tools to inform the mongoose lemur population restoration in Madagascar and Comoros

 

Project Leader: Dr IBOUROI Mohamed Thani

Summary

 

Madagascar holds one of the most important biodiversity hotspots worldwide. This biodiversity faces extreme risk of extinction due to anthropogenic activities. Mongoose lemur (a species located in Madagascar and Comoros) is among the fauna most threatened by forest disturbance in Madagascar. Most of the species’ habitats (in Madagascar) have been completely lost and more than 80% of the population has been lost recently. Due the high rate of habitat loss in this region, the species will become more and more vulnerable to extinction if conservation measures are not put in place urgently. In Comoros, the species seems to be less threatened based on its large population and recent studies suggest that this population of Comoros can be considered an important genetic reservoir for the viability and translocation to Madagascar. As Malagasy people depend heavily on forest resources for subsistence, establishing relevant conservation strategies such as the Mongoose lemur population restoration requires the consideration of multiple stakeholders’ perspectives toward biodiversity and the ecosystem restoration. In this study, we apply conservation genetic and socioeconomic tools to inform the Mongoose lemur population restoration in Madagascar