Lemurs are the most threatened group of mammals on earth. Lemur catta (ring-tailed lemur) represents one of the most iconic lemur species and faces numerous anthropogenic threats in the wild. In this study, we present population estimates from 32 sites across the range of L. catta, collected from primary and secondary data sources, to assess the number of ring-tailed lemurs left in the wild. We estimate that there are approximately 2,220 individual L. catta remaining in the 32 sites considered. We note local extinctions of populations of L. catta in at least 12 of the 32 sites examined, and that significantly more extinctions occurred in areas without some form of protection. This decrease in extant populations could represent a decrease of more than 95% of all ring-tailed lemurs in Madagascar since the year 2000. While these results should be considered preliminary, we stress the rapid decline of the species and note that habitat loss, bushmeat hunting and the illegal pet trade are driving populations to local extinction. Based on the data presented here, urgent and immediate funding and conservation action are crucial to ensure the viability of the remaining wild populations of ring-tailed lemurs.
Lemurs are the most threatened group of mammals on earth and are endemic to Madagascar, a biodiversity hotspot [Schwitzer et al., 2014]. Lemurs face numerous threats, including habitat loss due to deforestation and climate change [Brown and Yoder 2015], hunting [Schwitzer et al., 2014], and the illegal pet trade [Reuter et al., 2016]. Lemurs have been described as “the single highest primate conservation priority in the world” [Schwitzer et al., 2013, p. 5].
Ring-tailed lemurs (Lemur catta) are a flagship species for conservation, and are, perhaps, Madagascar's best-known primate. These lemurs are characterized by their behavioural flexibility, in that their sociality (e.g., dominance/rank relationships, aggression) and activity budgets vary according to environmental conditions [Sauther et al., 1999], and ecological plasticity, in that they can inhabit a plethora of habitat types [Goodman et al., 2006] and rebound from environmental perturbations [Gould et al., 1999]. The first large-scale population estimates of wild ring-tailed lemur habitats and individuals estimated a 9.5% habitat and 20% population decrease between 1985 and 2000 (population estimated at 751,251 in the year 2000 [Sussman et al., 2006]). Since then, census attempts of specific sites have continued [e.g., Kelley, 2013; Dimilahy et al., 2015; Gould and Andrianomena, 2015], yielding evidence of localized ring-tailed lemur extinctions [Gardner and Davies, 2014] and a suspected population decline rate of over 50% over a 3-generation period [Andriaholinirina et al., 2014].
Population declines of L. catta are driven by various threats. Ring-tailed lemurs represent 28% of individuals kept as in-country illegal pets [Reuter and Schaefer, 2016], and are sometimes killed and consumed by their human owners [Reuter and Schaefer, in press]. This species also faces direct hunting pressure [e.g., Goodman 2003], significant habitat loss [Brinkmann et al., 2014], and population declines resulting from the effects of climate change [Brown and Yoder, 2015]. As a result, L. catta is now restricted to isolated fragments [Sussman et al., 2003] with relatively low population densities [Kelley 2013; Andriaholinirina et al., 2014; Gould and Andrianomena, 2015], and its survival in the wild at most locations remains perilous [but see Dimilahy et al., 2015].
In this study, we present a population estimate for ring-tailed lemurs across 32 locations within their natural and historical range across south-western Madagascar. Moreover, we discuss the consequences of our findings and propose next steps to ensure the long-term viability of remaining wild populations.
Estimating Population Numbers at Known Sites
We assessed the status of populations of L. catta at 32 locations where they are known to occur (Fig. 1; Table 1). Similar to a census of chimpanzees (Pan troglodytes) by Plumptre and Cox , we collected primary and secondary data regarding the largest known and/or protected habitat fragments in which L. catta is found to estimate the total number of individuals left in the wild. L. catta is found at locations outside of these 32 known sites [Goodman et al., 2006, map approx. 100 records of wild populations of L. catta); however, these 32 sites likely comprise the largest remaining populations of L. catta, as many of the previously mentioned “known” sites are now deforested or devoid of animals [Sussman et al., 2006; Gardner and Davies, 2014].
To assess the status of populations of L. catta at these 32 sites, we used a mixture of methods: in-person site visits (M.L. and T.A.C.), personal communication with other researchers, and information gleaned from the published literature (Table 1). We could not visit all 32 field sites due to time and budget limitations; for in-person site surveys, we prioritized locations where previous researchers suggested that populations of L. catta were under significant extraction pressure [e.g., Kirindy Mitea Sud hunting pressure, Goodman, 2003; Andohahela hunting pressure, Siers, 2007].
For in-person site surveys (n = 10 sites, Table 1), M.L. and T.A.C. spent a minimum of 2 days at each site in June-August 2016 and used rapid assessment methods [Gilles and Reuter, 2014] to confirm or fail to confirm the presence of L. catta. Since we aimed to confirm the presence of ring-tailed lemurs in the locations visited, we took steps to increase the chances of detecting animals. These included speaking to local officials and villagers in order to understand where animals had been seen in the recent past, or where ring-tailed lemur troops' sleep sites or frequently used trees may be located. Once target areas were identified, we then walked on both forest trails and off-trail locations for between 5 and 12 km/day, while trying to detect the presence of ring-tailed lemurs. Confirmation of the presence of L. catta included hearing calls or observing animal(s), or indirect indicators of presence such as seeing footprints, spur markings on vegetation, bite marks on plants/foods, and/or presence of faeces. Indirect indicators of animal presence are reliable when efforts are standardized and consistent [Macdonald et al., 1999], and can be used to detect population changes in wildlife [Gese, 2001]. At all sites where the presence of L. catta could not be confirmed, M.L. and T.A.C. spoke with park managers, tour guides, and/or local community members to understand when and how many L. catta had last been seen at that site, and whether the animals had faced any known threats in the past. At 7 out of 10 sites, M.L. and T.A.C. were unable to confirm the presence of L. catta and therefore consider these populations to be locally extinct unless otherwise noted (Table 1). At the remaining 3 sites (Isalo Maki canyon, Namaza circuit, Tsimanampesotse northern boundary), we estimated how many L. catta were likely present by counting animals in known groups. More specifically, at Isalo (Maki canyon), we walked a circuit until we encountered ring-tailed lemur groups and then followed the animals for a minimum of 1 h, in order to ascertain how many animals were travelling with the group. At Isalo (Namaza circuit), we remained in a tourist picnic spot, and when ring-tailed lemur groups came through we monitored/followed individuals to determine the group size and identity. At Tsimanampesotse, we monitored known groups and detailed any intergroup encounters with neighbouring/unknown groups. For sites not visited in person (n = 22), we collected data from the literature and from colleagues who had visited these sites (Table 1).
Given the variations in sample size, methodological approach, sampling effort, and date of assessment, our compiled data largely violate assumptions of parametric and non-parametric statistics. Thus, the majority of our analyses are descriptive in nature. We present the mean, range, and median numbers of ring-tailed lemurs present at each of the 32 study sites, and compare the likelihood of local extinction between protected and unprotected areas (Fisher exact test, p = 0.05). We recognize that the data presented here are limited and must be treated with caution. Both over- and underestimations are possible in the data presented here. Overestimations are possible in the data that were collected several years ago [Gould and Andrianomena, 2015], as animals may no longer be present. Underestimates are also possible in areas where sampling effort has not been sufficient, such as large protected areas without extensive monitoring (i.e., Tsimanampesotse National Park, Isalo National Park). Despite these limitations, the data presented here are still informative in understanding decreasing population trends and the urgent conservation threats faced by ring-tailed lemurs.
Parameters of the Data Set
We sourced data for 84% of the sites (n = 27 out of 32) from information made public in 2010 or thereafter (Table 1). Ring-tailed lemurs' historical range covers roughly 100,000 km2 throughout southern Madagascar, although this generalized estimate includes both habitable (e.g., forested) and uninhabitable (e.g., rivers, cities) areas [Sussman et al., 2006]. The sites assessed here covered the habitable area of approximately 33,208 km2 (Table 1).
Estimated Population Size across 32 Sites
We estimate the presence/absence and total number of animals remaining at the 32 sites considered in this study. L. catta were deemed locally extinct or nearly locally extinct (i.e., we were unable to detect the animals' presence; fewer than 5 animals remaining at last known sighting) in 37.5% of the sites included in this study (n = 12 of 32, Table 1). A higher percentage of areas with some form of protection or management status (69% of n = 29 sites) had extant ring-tailed lemur populations, when compared to unprotected areas (0% of n = 3 sites, Fisher exact test, n = 32, p = 0.0444, sites with extinct and likely extinct populations grouped together).
The sites had an average of 72 ± 110 (mean ± SD; range: 0-562; median 36) individuals of L. catta per site (Table 1). In 2 instances the numbers of animals were reported as a range including 35-50 individual ring-tailed lemurs at Cap Sainte-Marie [Kelley, 2013] and 4-5 individual ring-tailed lemurs at Tsinjoriake [Youssouff, pers. commun.]. For these 2 instances we included the high estimates of the number of animals present (Table 1). Only 8 of 32 sites had populations of more than 100 individuals (Table 1). Sites with some protection (n = 28 sites) had an average of 79 ± 113 individuals, while sites without protection (n = 3 sites) had an average of 3 ± 1 individuals left at the site. From the sum of all sites examined, we estimate that there are approximately 2,220 ring-tailed lemurs remaining in the sites included in this study (Table 1).
We estimate that there are 2,220 L. catta remaining at the 32 sites included in this study. This estimate may not account for all small forest fragments where ring-tailed lemurs could persist or all possible groups of animals in unmonitored areas of large National Parks (i.e., Tsimanampesoste, Isalo), and thus could underestimate the total number of animals remaining. Alternatively, the estimate could include animals that have been extirpated very recently, and thus be inflated. Given that the previous estimates for individual wild ring-tailed lemurs were 2 orders of magnitude larger (i.e., 751,251 [Sussman et al., 2006]), we are confident that there has been a rapid decrease in the numbers of animals living in the wild in Madagascar. Though we acknowledge that both ours and the population estimates of Sussman et al.  were calculated with caveats, this sharp decline is concerning. Both complete deforestation of land parcels and decline of their lemur inhabitants [e.g., Kelley et al., 2007, Antserananomby Forest] and localized extirpations of ring-tailed lemurs without forest clearing (e.g., Ranobe area [Gardner and Davies, 2014]) have been previously documented. Current and detailed data regarding the numbers of ring-tailed lemurs persisting in all of their habitats are urgently needed to understand fully the dramatic decline in wild ring-tailed lemurs and prevent complete extinction in the wild.
The rapid decline in populations of L. catta has implications for conservation of the species. First, we found only 1 site with a population of >500 L. catta (Table 1). In Uganda, sites with <500 chimpanzees (Pan troglodytes) are of conservation concern as smaller populations are not able to sustain genetic viability in the long term [Plumptre and Cox 2006]. In the case of L. catta, Clarke et al.  found that ring-tailed lemur populations with fewer than 500 individuals in the central highlands maintain moderate levels of genetic diversity. These populations, however, are likely exhibiting a time lag response whereby genetic diversity will decrease substantially in the future due to continued population fragmentation and associated impacts [Clarke et al., 2015]. Both the low numbers of individuals at isolated sites (and the individuals' potential inability to find mates), and the consequences of low genetic diversity are problematic for ring-tailed lemurs' long-term survival in the wild. Second, we found that unprotected areas are more likely to experience population extinctions of ring-tailed lemurs. The general effectiveness of protected areas in maintaining species presence has been documented globally [see Naughton-Treves et al., 2005], and within the order Primates [see Pusey et al., 2007], although effective management of protected areas is also necessary, as has been noted for lemur species specifically [Schwitzer et al., 2014]. Madagascar has been plagued with political turmoil, yet even during times of crisis, conservation threats are more significant outside protected areas [Schwitzer et al., 2014]. The combination of higher levels of genetic diversity within larger populations and better survivorship within protected areas suggests that conservation priorities for ring-tailed lemurs should include areas with more animals and established protection (Table 1).
At the global scale, population extinctions are a more sensitive indicator of the loss of biodiversity than species extinctions [Ceballos and Ehrlich, 2002]. Likewise, because L. catta is known for its ecological flexibility [Sauther et al., 1999], it could be a proxy for biodiversity loss as its population decline underscores the difficulty that other, less adaptable species have in overcoming a multitude of threats. As a well-known and frequently encountered species (i.e., globally in zoos, and at select popular tourist sites in Madagascar), the overarching perception is that L. catta is not globally threatened, nor in imminent threat of extinction. A primate species' prevalence in the media has been associated with the belief that wild populations are stable and not threatened by extinction [Leighty et al., 2015; Nekaris et al., 2016]. This false impression that ring-tailed lemurs are not threatened with extinction could be devastating for the species (and larger communities of biodiversity in Madagascar) as it may impede the ability to secure funding for rapid conservation action. That being said, L. catta is currently under consideration for inclusion in the 2016-2018 “World's 25 Most Endangered Primates” listing, which is published bi-annually by the IUCN/SSC Primate Specialist Group [IUCN, 2016]. Inclusion of ring-tailed lemurs in this list will highlight the threats these animals are facing and inform the larger conservation community about the fact that even adaptable, flexible species such as ring-tailed lemurs can experience rapid decline.
Several urgent conservation actions should be considered with regard to protecting L. catta from extinction in the wild. First, it has been suggested that primate populations threatened with extinction should be regularly monitored using routine site visits [Plumptre and Cox, 2006]. For L. catta this monitoring is especially necessary at sites that have large remaining populations and in areas that are data deficient; a complete site-based census of L. catta sites is recommended. Second, long-term genetic viability is greater in populations with more individuals [Plumptre and Cox, 2006]. Since there are likely only 8 ring-tailed lemur populations remaining that have more than 100 individual animals (Table 1), these populations should be targeted for protection in order to maintain genetic diversity of the species. Additionally, reintroduction of captive ring-tailed lemurs, particularly those confiscated from the illegal pet trade [LaFleur et al., 2015] could be used as a mechanism to increase wild genetic diversity and to repopulate forested areas where populations are now extinct. Reintroductions are not without risks however, and comprehensive assessments of both prospective animals and release sites would need to be carried out, as per IUCN reintroduction guidelines [IUCN/SSC, 2013]. Third, live capture for the within-country pet trade poses a significant threat to many lemur species. More than 28,000 lemurs were kept in illegal captivity between 2010 and mid-2013, and of these ring-tailed lemurs were the most prevalent, comprising 28% of reported animals [Reuter et al., 2016]. Information regarding drivers and locations of capture, trade routes, and absolute numbers of ring-tailed lemurs in the illegal pet trade is imperative to future conservation initiatives [Reuter and Schaefer, 2016].
Madagascar is one of the world's poorest countries, and poverty is a significant predictor of extinction for primate species [Estrada, 2013]. The primary threats to ring-tailed lemurs, including deforestation and capture for the bushmeat and pet trades, can each be linked to poverty in that subsistence living depends heavily on natural resource exploitation [Brimont et al., 2015] and that forest products, including lemurs, can be sold to generate income [Gardner and Davis, 2014]. It is critical to link conservation efforts with social and economic development projects, in order to ensure that both Madagascar's human population and wildlife thrive.
The authors thank the Government of Madagascar, Ministry of the Environment and Ecology of Forests, Madagascar National Parks, the University of Toliara, and MICET, for their permissions and facilitations of our research. We also wish to thank Lydia Greene and Holly Schneider-Brown for their dedication to forwarding lemur conservation and awareness. Additionally, we thank Dr. Anna Nekaris and 3 anonymous reviewers for their feedback, which significantly improved this paper. Funding was provided by the Margot Marsh Biodiversity Foundation, Margot Marsh Primate Action Fund, Duke University's Arts and Sciences Council: Committee on Faculty Research Grant (awarded to T.A.C.), and Lemur Love Inc. private donors.
We understand Folia Primatologica's declaration of interests and declare that we have no competing interests.