Unmonitored releases of small animals? The importance of considering natural dispersal, health, and human habituation when releasing a territorial mammal threatened by wildlife trade
Introduction
Despite evidence on best practices in planning and monitoring translocation projects being available (IUCN/SSC, 2013, see Batson et al., 2015b for a review), unmonitored releases of animals are still frequent and can result in a series of adverse conditions if not well-planned (e.g. genetic changes, diseases, competition with resident individuals; Laikre et al., 2010, Champagnon et al., 2012). The reason for translocation failures is often unknown due to a lack of post-release monitoring (Griffith et al., 1989; Wolf et al., 1996; Fischer and Lindenmayer, 2000; Seddon et al., 2007; Beck, 2016). For example, a survey from 30 rescue centers revealed that only a third of respondents followed criteria to assess translocation success (Guy et al., 2013). Small research centers and non-governmental organizations in developing countries often receive animals brought in by villagers or law authorities and do not have the infrastructure to keep them (Cuarón, 1997, Cuarón, 2005, Agoramoorthy and Hsu, 2007, Nijman et al., 2009, Kenyon et al., 2014). These animals are often former pets or wild animals adapted to live in human-modified habitats that people perceive as forest animals (Kumar et al., 2014). As a result, they are subject to unmonitored releases (Dodd Jr and Seigel, 1991; Agoramoorthy and Hsu, 2007; Moore et al., 2014; Kumar et al., 2014; van der Sandt, 2017; Beck, 2019).
Animals translocated to an area where conspecifics are present may be forced to disperse (Le Gouar et al., 2012), thus translocated animals may share common characteristics with animals dispersing from their natal habitat (Macdonald and Johnson, 2001). Understanding patterns of natal dispersal in wild animals is, thus, fundamental when planning translocations (Armstrong and Seddon, 2008). Dispersal from the release site to another area is usually considered a criterion for failure in translocation projects, but often the information on wild dispersing animals is lacking (Stamps and Swaisgood, 2007; Le Gouar et al., 2012; Villaseñor et al., 2013; Berger-Tal et al., 2019), so such secondary dispersals may be natural for some species (Sutherland et al., 2000 for a review).
The health condition of animals immediately after the release is considered a main factor determining translocation success and should be taken into consideration and monitored (Mathews et al., 2006; Dickens et al., 2010). Health condition (considering both visible signs and pathogens), however, needs to be considered carefully even before the release since it may determine the translocation success (Mathews et al., 2006; Parker et al., 2012; Portas et al., 2016). Furthermore, health monitoring after release is often limited to direct observations of diseases and mortality, while comprehensive health evaluations are often missing (Deem et al., 2012; Portas et al., 2016). Another fundamental factor to be considered before the release is the habitat suitability in the release area, although the definition of suitable habitats is not always clear since it is species-specific (Osborne and Seddon, 2012). An unsuitable release area can determine a post-release dispersal as a consequence of the Natal Habitat Preference Induction (i.e. animals look for stimuli from their natal habitat instead of evaluating the habitat quality of the release site; Stamps and Swaisgood, 2007). An additional factor to be taken into consideration when planning population restoration projects, often neglected, is the involvement and attitudes of the local community, especially for species subjected to hunting and other forms of wildlife trade (Hunter et al., 2007; Nilsen et al., 2007; Jule et al., 2008). Areas with long-term conservation projects that also include conservation education or community outreach programs may thus be more suitable for restoration of threatened populations.
We explored the patterns of post-release and natal dispersal and investigated the role of health state and human habituation on the fate of translocated and natally dispersing Javan slow lorises Nycticebus javanicus, a nocturnal mammal, as part of a long-term conservation and research project. Slow lorises are the only venomous primates and it is suggested that the main use of their venom is against conspecifics (Rode-Margono and Nekaris, 2015). Javan slow lorises are highly territorial and animals can have severe wounds that are usually more frequent during dispersal (Fuller et al., 2018). Slow lorises are widely threatened by illegal trade for pets, medicines and tourist photography props (Nekaris and Starr, 2015; Ni et al., 2018), meaning that a low alert response towards humans may be detrimental for their survival. Furthermore, traders may cut their teeth to prevent venomous bites, which have implications for feeding on their main food resources – exudates, which they must gouge from trees (Nekaris and Starr, 2015). Slow lorises, despite being highly territorial and threatened by wildlife trade, are frequently subjected to unmonitored releases (Kumar et al., 2014). We collected data on translocated and natally dispersing animals and predicted that health state and human habituation would have been significant factors in determining animal survival and success in settling in a stable area. We then compared the presence of wounds and animals' ranging patterns after release or dispersal with those of stable resident animals present in the area to determine whether translocated and natally dispersing animals are similar. This information is important to determine whether post-release dispersal is abnormal or whether it is similar to the process of animals dispersing from their natal range. If unmonitored releases are to continue by welfare charities and governments, these data may provide some information on how to select appropriate release candidates.
Section snippets
Study site and subjects
We examined pre-release and pre-dispersal health conditions, human habituation, post-release and post-dispersal presence of wounds, behavior, and ranging patterns of 11 translocated (4 females, 7 males) and 11 natally dispersing (3 females, 8 males) Javan slow loris Nycticebus javanicus in Cipaganti, Garut District, Java, Indonesia (7° S, 107° E, 1200 m a.s.l.). The habitat consists of a mosaic of agricultural fields, bamboo patches, shrubs, and small agroforest patches in the vicinity of a
Results
The probability of wounds was significantly different between translocated (estimated mean: 0.47 ± SE 0.13), natally dispersing (estimated mean: 0.28 ± SE 0.11), and stable resident individuals (estimated mean: 0.10 ± SE 0.06) (generalized linear model: Wald χ2 = 6.42, p = 0.040), with a significant difference between translocated and stable resident individuals (Sequential Bonferroni: p = 0.029) (Fig. 1). The home range size in the first two months after release or dispersal was also different
Translocated animals may be forced to disperse
Here we showed that translocated animals in re-enforcement programs may act as natally dispersing animals, showing similar home ranges and probability of wounds. It is often assumed that post-release survival and settlement in a release area are the main criteria for a successful translocation (Le Gouar et al., 2012; Parker et al., 2012). As a consequence, many management tools are often used to mitigate post-release dispersal (Richardson et al., 2015b). The biology and ecology of a
CRediT authorship contribution statement
Marco Campera:Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft, Visualization.Ella Brown:Investigation, Writing - review & editing.Muhammad Ali Imron:Writing - review & editing, Project administration.K.A.I. Nekaris:Conceptualization, Methodology, Investigation, Resources, Writing - original draft, Supervision, Project administration, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Indonesia RISTEK and the regional Perhutani and BKSDA for authorising the study. Amersfoort Zoo, Augsburg Zoo, Brevard Zoo, Cleveland Zoo and Zoo Society, Columbus Zoo and Aquarium, Cotswolds Wildlife Park, Disney Worldwide Conservation Fund, Henry Doorly Zoo, International Primate Protection League, Little Fireface Project, Mohamed bin al Zayed Species Conservation Fund (152511813), Margot Marsh Biodiversity Fund, Memphis Zoo, Moody Gardens Zoo, National Geographic (GEFNE101-13),
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