The urgent need to reverse anthropogenic impacts on ecosystems and biodiversity is one of the biggest challenges for modern society (Svenning et al., 2016; Perino et al., 2019; Moreno-Mateos et al., 2020). Discussions on post-2020 biodiversity strategies by the signatory countries of the Convention on Biological Diversity are currently being initiated, and the United Nations General Assembly has recently declared 2021–2030 the “decade of ecosystem restoration” (United Nations, 2019). Due the designation, policy- and decision-makers will push animal restoration topics to the forefront of discussions about how to reach post-2021 biodiversity goals, especially because restoration projects could provide a buffer to species extinction (Galetti et al., 2017) and restore plant–animal interactions and ecological processes impaired by defaunation (Pires, 2017; Genes et al., 2019; Mittelman et al., 2020). However, changes in animal population dynamics and community composition following species (re)introduction may have unanticipated consequences for a variety of downstream ecosystem processes, including food web structure (Lovari et al., 2014), predator-prey systems (Bovendorp and Galetti, 2007) and infectious disease emergence (Lafferty and Gerber, 2002). This highlights the need to develop frameworks to anticipate, monitor, and mitigate the unintended ecosystem consequences of ‘re-wilding’ projects.

In recent years, bats have received growing attention as reservoirs of pathogens linked to emerging zoonotic diseases that cause significant human and animal morbidity and mortality. Key examples include Ebola, Nipah and potentially the ongoing COVID-19 pandemic, given that viral strains closely related to SARS-CoV-2 have been detected in bats (Letko et al., 2020). In the Neotropics, the most notorious bat-transmitted pathogen is rabies virus (Rhabdoviridae, Lyssavirus), which causes a nearly universally lethal infection in all mammals (including humans) and is maintained by a wide variety of bat species (Streicker et al., 2010; Fisher et al., 2018). Among the three species of vampire bats (Desmodus rotundus, Diaemus youngi, and Diphylla ecaudata) that rely on blood as their food source, D. rotundus is the only known reservoir for rabies. D. rotundus frequently bites domestic and wild animals and more rarely humans during feeding (Bobrowiec et al., 2015; Galetti et al., 2016; Gnocchi and Srbek-Araujo, 2017; Zórtea et al., 2018; Gonçalves et al., 2020), creating opportunities for the transmission of rabies virus and potentially other saliva-borne viruses (Bergner et al., 2020).

Official guidelines for managing rabies transmitted by vampire bats involve pre-exposure vaccination of livestock, post-exposure vaccination of humans bitten by vampire bats (and more rarely pre-exposure human vaccination) and bat population control (Benavides et al., 2020a; Recuenco, 2020). Although bat culls sometimes involve vigilante action such as burning or destruction of bat roosts, governments actively discourage these non-specific actions in favor of topical, anticoagulant poisons (“vampiricides”) which spread intra-specifically by vampire bat grooming. Similar poisons can be applied to the wounds of bitten livestock, and ingested when bats return to feed (Thompson et al., 1972). Policies for vampire bat monitoring and initiating culls are country-specific and implemented by Ministries of Health and/or Ministries of Agriculture. In general, culls are reactive to reports of increased vampire bat bites on livestock or detection of rabies cases via passive surveillance systems. While culling effectively reduces vampire bat bites, some studies suggest that significant mitigation of the burden of rabies in humans and domestic livestock would require implementing culls over impractically large geographical areas (Streicker et al., 2012; Blackwood et al., 2013; Bakker et al., 2019). Other proposed strategies for controlling vampire bat populations involve modified farming practices that reduce the accessibility to bats (e.g., artificial lighting, protected corrals, altering the composition and locations of herds) or hormonal reproductive control of bats, though the latter is in early research stages (Benavides et al., 2020a).

D. rotundus has specialized on blood of medium to large-bodied mammal species and demonstrates strong plasticity of foraging strategies due to changes in local prey availability across regions (Table 1). Due to the proliferation of livestock production in much of the Neotropics and its relative reliability compared to native wildlife, livestock are generally preferred prey (Voigt and Kelm, 2006; Gonçalves et al., 2017; Bohmann et al., 2018). However, dietary shifts to humans and wildlife have also been reported following changes in local prey abundance. For example, in Brazil, conversion of pasture into plantation agriculture forced vampire bats switch from the formerly abundant livestock animals to wild animals (Galetti et al., 2016). In Belize, removal of livestock increased D. rotundus feeding on human beings (McCarthy, 1989) and removal of wildlife by hunting was speculated to increase human rabies risk in Peru (Stoner-Duncan et al., 2014). In the context of rewilding, released species may be at particular risk since candidate areas for restoration tend to have low availability of medium to large-bodied wild prey due to historical human disturbance (Galetti et al., 2017; Fernandez et al., 2017). In addition, rewilding projects typically rely on captive born animals (Fernandez et al., 2017) that have diminished functional traits associated with adaptation to captivity, including exposure to predators (Jule et al., 2008), which could heighten vulnerability to vampire bats.

Recently, an unprecedented study in Brazil showed changes in vampire bat feeding following a rewilding project (Gonçalves et al., 2020). Specifically, in a land-bridge island where 100 individuals of 15 non-volant mammal species were introduced with the intent of ‘‘restoring’’ the local fauna, D. rotundus fed primarily on introduced capybaras (Gonçalves et al., 2020). Thirty-six years following restoration, the relative abundance of common vampire bats was higher on the islands than the mainland nearby due to the increased prey availability. The restoration further transformed the land-bridge island into a high-risk area for rabies transmission as three introduced capybaras were confirmed to have died from bat transmitted rabies (Gonçalves et al., 2020).

Due the lessons learned from ongoing rewilding projects combined with public health risk if rabies infections from (re)introduced species lead to human exposures, we present a novel approach on how to prevent and control vampire bats and rabies in rewilding projects (Fig. 1). While we highlight vampire bats as a focal example, we seek to establish a generalizable rewilding-monitoring framework that can anticipate and detect how indirect processes may alter the outcomes of restoration projects.

Fig. 1.

Generalizable rewilding-monitoring framework that can anticipate and mitigate the unintended ecosystem consequences of ‘re-wilding’ projects.

(0.56MB).

The first step of the framework should assess the presence and infection status of natural reservoir hosts in the focal area. In the case of vampire bats, presence could be verified by field surveys or questionnaires to local people about bat bites on domestic animals (a strong indicator of D. rotundus presence). If vampire bats are confirmed present, viral circulation could be assessed using serological surveys in wild bats to detect antibodies from recent exposures (Meza et al., 2020). Since naïve domestic animals are increasingly recognized to sometimes survive and mount detectable antibody responses to rabies virus exposures, serological surveys of livestock reported to be un-vaccinated by their owners could similarly indicate viral circulation (Benavides et al., 2020b). Finally, recent records of rabies incidence in humans, domestic or wild animals from national surveillance systems could provide further evidence of rabies circulation. If vampire bats are present and there is evidence of viral circulation, multidisciplinary teams of scientists and managers should develop plans that assess the benefits and costs of the rewilding project, both in terms of the success of restoration (particularly how added rabies mortality would affect the initial establishment of rare/threatened species) and potential public health risks arising from human exposures to rabies cases in restored wildlife.

Reduction of vampire bat populations may be considered prior to release by a multidisciplinary teams of scientist that have to evaluate the ethical issues on both, to mitigate effects on re-introduced prey (blood loss, rabies transmission) and on other bat species which may compete with D. rotundus for roost space. In much of its range, D. rotundus populations are controlled using topical, anticoagulant poisons, which are either applied directly to captured bats and spread by grooming or can be applied to livestock to be ingested when bats feed (Johnson et al., 2014). Although social disruption of culls is predicted to increase rabies transmission in endemic areas (Streicker et al., 2012; Blackwood et al., 2013), culls carried out in rabies free populations may reduce the likelihood of viral incursions (Bakker et al., 2019). Reproductive control by sterilization (Serrano et al., 2007) is less explored alternative. Although the time lag between sterilization campaigns and diminished population sizes makes this tool ineffective at the pre-release stage, it could be a valuable long-term strategy to manage vampire bat population sizes (see phase 3).

Presumably, if vampires are present and rabies is detected, all mammals (> 1 kg) should be vaccinated against rabies before release. Under this phase, prevention educational program of rabies risk transmitted by bats should begin by a multi-disciplinary task force, included public and animal health services and universities, focusing on local people living in the destined site and those actually working on the rewilding project.

We pinpoint a series of precautions and the need for long-term monitoring of vampire bats and rabies responses to rewilding projects. We highlighted the importance of multidisciplinary teams of scientist and managers, including national surveillance systems, focusing on prevention educational program of rabies risk transmitted by bats in rewilding projects. In addition, monitoring the relative abundance of vampire bats, considering reproductive control by sterilization and oral vaccines that autonomously transfer among bats would reduce the probability, size and duration of rabies outbreaks. The rewilding assessment framework presented here responds to calls to better integrate the science and practice of rewilding (Nogués-Bravo et al., 2016) and also the urgent need for long-term studying of bat-transmitted pathogen in the Neotropical area as the region is considered a geographic hotspots of “missing bat zoonoses” (Olival et al., 2017). Although there are challenges remaining, we believe that the implementation and further development of our monitoring framework will help catalyse a positive and ambitious vision for rewilding. Furthermore, the application of this framework provides guidance for practitioners, funders and decision-makers to incorporate or demand a multifaceted perspective for rewilding and, simultaneously, incentivize conservation initiatives to go beyond the recovery of species and habitats and include ecosystem function and processes. The framework is applicable to management a variety of bat-transmitted pathogens in restoration projects that aims to promote beneficial interactions between society and nature, range from conservation translocation to all variation of rewilding (Corlett, 2016).

The authors declare that there is no conflict of interest.