Tuberculosis in Lemurs and a Fossa at National Zoo, Madagascar, 2022.

We diagnosed Mycobacterium tuberculosis in captive lemurs and a fossa in Antananarivo, Madagascar. We noted clinical signs in the animals and found characteristic lesions during necropsy. The source of infection remains unknown. Our results illustrate the potential for reverse zoonotic infections and intraspecies transmission of tuberculosis in captive wildlife.

Microbial rewilding in the gut microbiomes of captive ring-tailed lemurs (Lemur catta) in Madagascar.

Microbial rewilding, whereby exposure to naturalistic environments can modulate or augment gut microbiomes and improve host-microbe symbiosis, is being harnessed as an innovative approach to human health, one that may also have significant value to animal care and conservation. To test for microbial rewilding in animal microbiomes, we used a unique population of wild-born ring-tailed lemurs (Lemur catta) that were initially held as illegal pets in unnatural settings and, subsequently, relocated to a rescue center in Madagascar where they live in naturalistic environments. Using amplicon and shotgun metagenomic sequencing of lemur and environmental microbiomes, we found multiple lines of evidence for microbial rewilding in lemurs that were transitioned from unnatural to naturalistic environments: A lemur's duration of exposure to naturalistic settings significantly correlated with (a) increased compositional similarly to the gut communities of wild lemurs, (b) decreased proportions of antibiotic resistance genes that were likely acquired via human contact during pethood, and (c) greater covariation with soil microbiomes from natural habitats. Beyond the inherent psychosocial value of naturalistic environments, we find that actions, such as providing appropriate diets, minimizing contact with humans, and increasing exposure to natural environmental consortia, may assist in maximizing host-microbe symbiosis in animals under human care.

Impact of the COVID-19 Pandemic on Primate Research and Conservation.

There is evidence to suggest that the Coronavirus Disease 2019 (COVID-19) pandemic may hamper our achievement of the Sustainable Development Goals (SDGs). Here, we use non-human primates as a case study to examine the impacts of COVID-19 on the ability to achieve biodiversity conservation and management sustainability targets. We collected data through a survey of members of the IUCN SSC Primate Specialist Group from January to March 2022. Of the 93 experts that responded to our survey, we found that 39% had not been able to visit any of their field sites since March 2020, 54% said they had less funding available for their primate-related work, and only one out of ten said they had managed to achieve at least 76-100% of their planned primate-related work since March 2020. Six out of ten respondents (61%) felt that primate conservation efforts in protected areas were worse than before the onset of the COVID-19 pandemic and one-third (33%) felt hunting was happening more frequently than before. This study provides evidence of the impacts of COVID-19 on progress towards achieving the SDGs, and provides practical lessons learned for biodiversity conservation efforts moving forward.

Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota.

BACKGROUND: Inter-population variation in host-associated microbiota reflects differences in the hosts' environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes-an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia. RESULTS: The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal 'signal of captivity' that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota. CONCLUSIONS: As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple 'captive vs. wild' dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.

Drug-Resistant Tuberculosis in Pet Ring-Tailed Lemur, Madagascar.

We diagnosed tuberculosis in an illegally wild-captured pet ring-tailed lemur manifesting lethargy, anorexia, and cervical lymphadenopathy. Whole-genome sequencing confirmed the Mycobacterium tuberculosis isolate belonged to lineage 3 and harbored streptomycin resistance. We recommend reverse zoonosis prevention and determination of whether lemurs are able to maintain M. tuberculosis infection.

Genetic population structure of endangered ring-tailed lemurs (Lemur catta) from nine sites in southern Madagascar.

Madagascar's ring-tailed lemurs (Lemur catta) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring-tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and F ST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, H O = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring-tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate-driven environmental instability, will therefore likely impede the long-term viability of the species.

A national survey of household pet lemur ownership in Madagascar.

Primates are extracted from the wild for the pet trade across the world. In Madagascar, lemurs are kept as illegal pets and an understanding of lemur pet ownership at the national level is lacking. In 2013 and 2016, we undertook a national survey in 11 of Madagascar's 22 administrative regions (n = 28 towns) with 1,709 households. To our knowledge, this is the first national survey of the household ownership of pet primates in a country where they are endemic. In the 1.5 years prior to being surveyed, 8% ± 4% (towns as replicates) of respondents had seen a captive lemur while a further 0.7% ± 0.5% of respondents had owned one personally. We estimate that 33,428 ± 24,846 lemurs were kept in Malagasy households in the six months prior to our survey efforts, with 18,462 ± 12,963 of these pet lemurs estimated in urban household alone. Rates of lemur ownership did not differ by province but increased with the human population of a town and with the popularity of the town on Flickr (a proxy indicator for tourism). We found that the visibility of pet lemur ownership did not differ across the country, but it did increase with the size of the town and popularity with tourists. Areas with visible pet lemurs were not always the areas with the highest rates of pet lemur ownership, highlighting that many pet lemurs are hidden from the general public. Our study highlights the need for conservation programs to consider both the proportion of inhabitants that own pet lemurs and the total number of lemurs that are potentially being kept as pets in those towns. We close by noting that for some species, even just a small amount of localized live extraction for pet ownership could be enough to cause localized population extinctions over time. Moreover, an urgent response is needed to combat a recent and alarming rise in illegal exploitation of biodiversity across Madagascar.

Illegal Trade of Wild-Captured Lemur catta within Madagascar.

Lemur catta is the most reported illegal captive lemur. We document 286 L. catta that were held in illegal captive conditions in Madagascar. Coastal tourist destinations are "hot spots" for sightings. Many of the L. catta reported were in businesses (49%) and were perceived to be held captive for the purpose of generating income (41%). Infant/juvenile L. catta were overwhelmingly observed annually in December (41%) and may suffer high mortality rates given that they are not weaned during this month of the year. Population growth modeling suggests that known capture rates may be sustainable in all but small populations of 500 individuals and when infants/juveniles are targeted. However, of the seven remaining populations of L. catta with more than 100 individuals, only one is known to contain more than 500 animals, and we present evidence here that infants/juveniles are targeted. Moreover L. catta face significant other threats including habitat loss, bushmeat hunting, and climate change. Several actions could reduce the illegal capture and ownership of L. catta in Madagascar such as tourist behavior change initiatives, enforcement of laws, and alternative livelihoods for local people. These interventions are urgently needed and could be adapted to protect other exploited wildlife in the future.

A viral video and pet lemurs on Twitter.

Content shared on social media platforms can impact public perceptions of wildlife. These perceptions, which are in part shaped by context (e.g. non-naturalistic setting, presence of a human), can influence people's desires to interact with or acquire wild animals as pets. However, few studies have examined whether this holds true for wild animals featured in viral videos. This study reports on opportunistic data collected on Twitter before, during, and after a video that featured a habituated ring-tailed lemur (Lemur catta), called "Sefo", in southern Madagascar went 'viral' (i.e. circulated rapidly on the internet). Our dataset of 13,953 tweets (from an 18.5-week time period in early 2016) referencing lemurs was collected using targeted keywords on the Twitonomy Service. We identified 613 individual tweets about people wanting a lemur as a pet. In addition, 744 tweets that were captured in our dataset linked to the Sefo viral video. We found that as the number of tweets about the viral video increased, so did the number of tweets where an individual wanted to have a lemur as a pet. Most tweets (91%) did not make reference to a specific species of lemur, but when they did, they often (82%) referenced ring-tailed lemurs (L. catta), ruffed lemurs (Varecia spp.), and mouse lemurs (Microcebus spp.). This study serves as a case study to consider how viral content can impact how wild animals are perceived. We close by noting that social media sites like Twitter, which are increasingly providing their users with news and information, should carefully consider how information about wild animals is shared on their platforms, as it may impact animal welfare.

Restating the Case for a Sharp Population Decline in Lemur catta.

As with many other species in the primate order, ring-tailed lemurs (Lemur catta) are threatened with extinction. Our articles documented declines in wild ring-tailed lemur populations and noted that fewer than 2,500 wild ring-tailed lemurs are known to persist in 32 [Gould and Sauther: Primate Conservation 2016; 30: 89-101] and 34 [LaFleur et al.: Folia Primatologica 2017; 87: 320-330] sites. A criticism of our articles [Murphy et al.: International Journal of Primatology 2017; 38: 623-628] suggested that we have inadequately sampled ring-tailed lemur populations and habitats, and misused the literature. We disagree, and provide both a detailed rebuttal and responses to specific critique points herein. Moreover, we restate our case outlining a dramatic decline of ring-tailed lemurs resulting from anthropogenic pressures (deforestation, severe habitat fragmentation, extraction for the pet and bushmeat trades). We pose several thought-provoking questions as to when is the appropriate time for researchers to "sound the alarm" about a species' decline, and remain committed to understanding the drivers of unsustainable exploitation of this emblematic lemur, and preventing their extinction in the wild.

Exploring the Role of Wealth and Religion on the Ownership of Captive Lemurs in Madagascar Using Qualitative and Quantitative Data.

Primates are kept as pets for various reasons including as indicators of wealth. Ownership of primates can also be influenced by religion. In Madagascar, thousands of lemurs are kept as pets, but the roles of wealth and religion in the ownership of captive lemurs have not been explored. We use quantitative and qualitative data to examine these aspects of ownership. Quantitative data were collected (July to August 2016) in households (n = 596) of 12 urban and rural towns in Madagascar using semi-structured interviews. International standards for research ethics were followed. Research was approved by an ethics oversight committee. We also opportunistically visited 13 religious facilities. Qualitative data were used to frame the context of the quantitative data. We found that pet lemur owners do not speak about their lemurs as a symbol of wealth, but non-owners associate pet lemurs with wealth. Therefore, status/wealth may be a motivating factor in the ownership of pet lemurs. We also found evidence that Catholic entities in Madagascar sometimes take in captive lemurs when the owner can no longer care for the animal (being viewed as animal-friendly institutions). However, we did not find evidence of religion (institutional or traditional) influencing the ownership of pet lemurs.

Rapid Decrease in Populations of Wild Ring-Tailed Lemurs (Lemur catta) in Madagascar.

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.

Seasonal feeding ecology of ring-tailed lemurs: a comparison of spiny and gallery forest habitats.

Although Lemur catta persists in many habitat types in southern Madagascar, its ecology has been primarily studied within gallery forests. We compare plant food selection and properties for ring-tailed lemurs in the spiny and gallery forests over the synchronized lactation period (September to March) that includes both the dry and wet seasons. We found no significant habitat-specific differences in the type of plant part consumed per month (i.e. flower, fruit, leaf) or between the intake of soluble carbohydrates. However, the presence and use of Tamarindus indica plants appear to elevate protein and fiber intake in the gallery forest lemurs' diets. Protein is especially important for reproductive females who incur the added metabolic costs associated with lactation; however, fiber can disrupt protein digestion. Future work should continue to investigate how variations of protein and fiber affect ring-tailed lemur dietary choice and nutrient acquisition.

Reproductive Female Feeding Strategies in Spiny Forest-Dwelling Lemur catta in Southern and Southwestern Madagascar: How Do Females Meet the Challenges of Reproduction in this Harsh Habitat?

The spiny forest ecoregion of southern and southwestern Madagascar is characterized by low annual rainfall, high temperatures, short-stature xeric vegetation and lack of canopy. Lemur catta is often the only diurnal primate persisting in this habitat. For reproductive females living in spiny forests, gestation and early-to-mid lactation periods occur during the dry season when food resources are limited. We conducted a between-site comparison of variables important to the feeding ecology of reproductive female L. catta inhabiting spiny forest at 3 sites: Berenty spiny forest (BSF), Cap Sainte-Marie (CSM) and Tsimanampesotse National Park (TNP). We hypothesize that the ability for pregnant and lactating females to adequately obtain plant foods high in protein, low in fiber and with a high water content is crucial to their survival and successful reproduction in spiny habitat. We found favorable or relatively equal protein-to-fiber ratios in plant foods most frequently consumed by reproductive females, and preferred foods contained high water content. Some overlap in preferred plant species at the 3 sites suggests important plant foods for reproductive females inhabiting spiny forests. We suggest that choosing foods high in protein, relatively low in fiber and with high water content are behavioral adaptations allowing female L. catta to reproduce and survive in this habitat.

Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations.

Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered "strictly diurnal". We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010-April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25% of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5% of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53% nighttime, 43% daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.

Biological variation in a large sample of mouse lemurs from Amboasary, Madagascar: implications for interpreting variation in primate biology and paleobiology.

A thorough knowledge of biological variation in extant primates is imperative for interpreting variation, and for delineating species in primate biology and paleobiology. This is especially the case given the recent, rapid taxonomic expansion in many primate groups, notably among small-bodied nocturnal forms. Here we present data on dental, cranial, and pelage variation in a single-locality museum sample of mouse lemurs from Amboasary, Madagascar. To interpret these data, we include comparative information from other museum samples, and from a newly collected mouse lemur skeletal sample from the Beza Mahafaly Special Reserve (BMSR), Madagascar. We scored forty dental traits (n = 126) and three pelage variants (n = 19), and collected 21 cranial/dental measures. Most dental traits exhibit variable frequencies, with some only rarely present. Individual dental variants include misshapen and supernumerary teeth. All Amboasary pelage specimens display a "reversed V" on the cap, and a distinct dorsal median stripe on the back. All but two displayed the dominant gray-brown pelage coloration typical of Microcebus griseorufus. Cranial and dental metric variability are each quite low, and craniometric variation does not illustrate heteroscedasticity. To assess whether this sample represents a single species, we compared dental and pelage variation to a documented, single-species M. griseorufus sample from BMSR. As at Amboasary, BMSR mouse lemurs display limited odontometric variation and wide variation in non-metric dental traits. In contrast, BMSR mouse lemurs display diverse pelage, despite reported genetic homogeneity. Ranges of dental and pelage variation at BMSR and Amboasary overlap. Thus, we conclude that the Amboasary mouse lemurs represent a single species - most likely (in the absence of genetic data to the contrary) M. griseorufus, and we reject their previous allocation to Microcebus murinus. Patterns of variation in the Amboasary sample provide a comparative template for recognizing the degree of variation manifested in a single primate population, and by implication, they provide minimum values for this species' intraspecific variation. Finally, discordance between different biological systems in our mouse lemur samples illustrates the need to examine multiple systems when conducting taxonomic analyses among living or fossil primates.