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Northern pig-tailed macaque

The Northern pig-tailed macaque (Macaca leonina) is a medium-sized Old World monkey of the family Cercopithecidae, distinguished by its short, upward-curving tail, golden-brown fur, and dark facial skin with reddish streaks extending from the eyes.^[1]^[2] Males typically weigh 7-9 kg and measure up to 58 cm in head-body length, while females are smaller at 4-6 kg.^[2] Native to Southeast Asia, it ranges from northeastern India and Bangladesh through Myanmar, Thailand, Laos, Cambodia, Vietnam, and into southern China.^[3] This diurnal, predominantly arboreal species inhabits a variety of tropical forest types, including primary and secondary evergreen forests, mixed deciduous forests, dry dipterocarp woodlands, and riparian zones, often from sea level up to elevations exceeding 2,000 m.^[1]^[3] Omnivorous and opportunistic, its diet centers on fruits and seeds, supplemented by leaves, flowers, insects, and small vertebrates, enabling it to contribute significantly to forest regeneration through seed dispersal.^[3] Socially organized in multimale-multifemale groups of 10-50 individuals, it exhibits flexible behaviors adapting to habitat degradation, though populations have declined markedly due to habitat fragmentation from logging and agriculture, as well as direct persecution via hunting for bushmeat, pets, and biomedical research.^[4]^[1] Assessed as Vulnerable on the IUCN Red List since 2008, the Northern pig-tailed macaque faces ongoing threats that have reduced its numbers by at least 30% over three generations, with regional variations including Endangered status in India and Critically Endangered in Bangladesh.^[5] Conservation efforts emphasize protected areas and anti-poaching measures, yet enforcement challenges and human-primate conflict persist in fragmented landscapes.^[4]

Taxonomy

Classification and phylogeny

The Northern pig-tailed macaque (Macaca leonina) is classified within the order Primates, suborder Haplorhini, infraorder Simiiformes, parvorder Catarrhini, superfamily Cercopithecoidea, family Cercopithecidae, subfamily Cercopithecinae, and genus Macaca.^[6]^[1] The species was formally described by Edward Blyth in 1863 based on specimens from regions including present-day Bangladesh and Myanmar.^[7] It is recognized as monotypic, lacking recognized subspecies, following revisions that elevated it from prior synonymy or subspecific status under M. nemestrina.^[8]^[9] Phylogenetic analyses of mitochondrial genomes position M. leonina within the diverse genus Macaca, which comprises approximately 22 species divided into monophyletic groups including the silenus, sinica, fascicularis, and nemestrina-assarctoides clades.^[10] Within the pig-tailed macaque complex, M. leonina (northern form) shares a recent common ancestry with southern congeners such as M. nemestrina and M. pagensis, with Bornean lineages (M. pagensis) representing the earliest divergence among examined pig-tailed populations.^[11]^[11] This topology reflects historical dispersal events across mainland and island Southeast Asia, driven by Pleistocene sea-level fluctuations and habitat connectivity, rather than deep vicariance.^[11] Nuclear and mitochondrial markers further confirm M. leonina's distinct evolutionary trajectory, supporting its species-level separation via accumulated genetic and morphological divergences, including cranial and pelage traits documented in foundational taxonomic revisions.^[9] The nemestrina group, encompassing pig-tailed species, clusters closely with the fascicularis group in broader macaque phylogenies, indicative of shared Southeast Asian origins predating the genus's radiation across Asia and North Africa.^[10]

Physical description

Morphology

The Northern pig-tailed macaque (Macaca leonina) exhibits a stocky, thick-set build typical of medium-sized Old World monkeys, with a broad chest and relatively long legs that support both arboreal and terrestrial locomotion. When standing quadrupedally, adults measure 40–65 cm in head-body length, complemented by a short, thick tail of 14–25 cm that is often arched or curled over the back, giving the species its distinctive "pig-tailed" appearance.^[3]^[1] Body weights vary, generally ranging from 4.4 to 14.5 kg across individuals, reflecting environmental and nutritional influences observed in wild populations.^[3]^[1] The pelage consists of coarse, olive-gray to golden-brown fur, denser on the dorsal surface and forming a darker brown crown on the head, which lightens with age from the darker natal coat of juveniles. Facial skin is pinkish and largely naked, featuring pale patches around the eyes, prominent red streaks extending from the outer eye corners toward the ears, and exaggerated cheek ruffs particularly in mature individuals. Ischial callosities and genital regions display a darker red hue, while the overall morphology includes a moderately long snout and robust limbs adapted for foraging in varied forest strata.^[3]^[1]

Sexual dimorphism

The Northern pig-tailed macaque (Macaca leonina) exhibits moderate sexual dimorphism, primarily in body size and mass, with adult males substantially larger than females. This size difference is characteristic of many macaque species and correlates with male-male competition for mating opportunities.^[3]

Trait	Males	Females
Head-body length	50–60 cm	40–49 cm
Tail length	16–25 cm	14–20 cm
Weight	6.2–9.1 kg	4.4–5.7 kg

Males also display more prominent cheek ruffs, enhancing their facial distinction from females.^[3] While canine size dimorphism is typical in macaques, with males possessing larger projecting canines used in agonistic displays, specific measurements for M. leonina remain underreported in available literature.^[2] Females exhibit cyclical anogenital swelling during estrus, signaling reproductive status, though this trait varies in prominence compared to other macaques.^[3]

Geographic distribution and habitat

Current range

The northern pig-tailed macaque (Macaca leonina) occupies a fragmented range spanning northeastern India, eastern Bangladesh, Myanmar, Thailand, Laos, Cambodia, Vietnam, and southern China. In India, populations are documented in Arunachal Pradesh, Assam, Manipur, Meghalaya, Mizoram, and Nagaland, primarily north of the Brahmaputra River.^[12] ^[13] The species' distribution reaches southern Vietnam and includes peninsular Thailand north of approximately 8–9°N, where it abuts the range of the southern pig-tailed macaque (M. nemestrina), with evidence of restricted hybridization in contiguous areas.^[14] ^[1] Suitable habitats within this range include tropical and subtropical forests, but ongoing deforestation has led to population declines and range contraction, particularly outside protected areas. Northern pig-tailed macaques persist in reserves such as Khao Yai National Park in Thailand, Chunati Wildlife Sanctuary and Lawachara National Park in Bangladesh, and various sites in Vietnam and Cambodia.^[14] ^[4] Comprehensive population estimates remain scarce, with the species classified as Vulnerable by the IUCN due to habitat loss and hunting pressures.^[3]

Habitat types and adaptations

The Northern pig-tailed macaque (Macaca leonina) primarily inhabits tropical and subtropical forests across Southeast Asia, including primary and secondary evergreen, deciduous, bamboo, and cloud forests, ranging from lowlands to elevations of approximately 1,500 meters.^[3]^[4] In southwestern China, populations favor broadleaved evergreen forests at higher elevations while avoiding heavily disturbed or open areas.^[15] These macaques demonstrate flexibility in habitat use, occupying both intact primary forests and fragmented secondary growth, which allows persistence amid anthropogenic degradation.^[16]^[17] Adaptations to these diverse habitats include semi-terrestrial locomotion, with northern populations exhibiting greater arboreality compared to southern pig-tailed macaques, facilitating access to understory vegetation and fruits in stratified forest layers.^[1] Their frugivorous diet, supplemented by leaves, seeds, insects, and opportunistic foraging on crops during fruit scarcity, supports survival in variable resource environments, while seed dispersal contributes to forest regeneration.^[3]^[18] In degraded fragments, they shift reliance to old-growth plantations for supplemental fruits, adjusting ranging patterns and dietary composition based on native fruit availability to mitigate seasonal shortages.^[16]^[19] This behavioral plasticity, including wider niche breadth relative to sympatric species like rhesus macaques, enables coexistence in fragmented landscapes through differential habitat partitioning and resource exploitation.^[17]

Ecology and behavior

Northern pig-tailed macaques (Macaca leonina) exhibit a social structure typical of the genus Macaca, consisting of stable, multi-male, multi-female groups with female philopatry and male dispersal. Females remain in their natal groups, forming matrilineal kinship networks that underpin linear dominance hierarchies, where rank is inherited maternally and determines priority access to food, grooming, and mating.^[20] Adult males typically disperse from their birth groups around adolescence, immigrating into other troops where they may challenge residents for status or form peripheral associations, often facing aggression from established members.^[21] Group sizes vary by habitat and population density but average approximately 23 individuals, ranging from 10 to over 50 in some forests; larger groups may fission into temporary foraging subunits to optimize resource exploitation while maintaining cohesion through vocalizations and spatial proximity. In Bangladeshi forests like Satchari National Park, observed troops numbered around 29 members, with densities of 1.23 groups per km².^[3]^[13] Social bonds are maintained primarily through allogrooming, which serves both hygienic and affiliative functions, with subordinates directing more grooming toward dominants to mitigate aggression and secure tolerance, though reciprocity occurs among peers.^[22] Cognitive abilities in northern pig-tailed macaques align with those of other macaques, emphasizing social intelligence adapted to navigating complex hierarchies and kin relations, including recognition of maternal rank inheritance and selective affiliation to reduce conflict. Limited empirical studies on wild populations highlight adaptive behaviors such as habitat-specific sleeping site selection to minimize predation risk, indicating environmental problem-solving. Captive observations reveal structured ethograms of activities like foraging and social interactions, but peer-reviewed data on advanced cognition, such as tool use or deception, remain sparse compared to congeners like long-tailed macaques, suggesting reliance on observational learning within social contexts rather than individual innovation.^[23]^[24]^[25]

Diet and foraging strategies

The northern pig-tailed macaque (Macaca leonina) maintains an omnivorous diet dominated by fruits, which comprise the majority of its intake and include over 100 plant species across its range. Supplementary foods encompass leaves, seeds, flowers, bark, roots, fungi, invertebrates (such as insects and earthworms), and occasionally small vertebrates or bird eggs. This composition supports nutritional needs in seasonal tropical forests, where ripe fruits provide high-energy rewards during abundance periods.^[3] Foraging emphasizes semi-terrestrial strategies, with individuals and groups spending substantial time on the forest floor—more so than many arboreal macaques—to access ground-level resources like fallen fruits, tubers, and buried invertebrates. Digging with hands, snouts, or tools facilitates extraction of roots and soil prey, while opportunistic scanning for scattered items drives movement in small subgroups of 2–6 animals that maintain vocal contact with the larger troop. Extractive techniques are refined for challenging items; for instance, toxic caterpillars are processed in a sequenced manner: picked from foliage, transported to a substrate, rubbed vigorously to dislodge stinging setae, ingested, and followed by post-consumption behaviors like substrate wiping.^[1]^[26] Seasonal fruit scarcity prompts dietary shifts toward fallback foods such as mature leaves, bark, or increased invertebrate hunting, correlating with expanded ranging (e.g., daily path lengths up to several kilometers) and altered patch use in sites like Khao Yai National Park, Thailand. Fruit phenology directly influences core area fidelity and transit time, with low availability leading to more discontinuous foraging bouts interspersed with travel to distant patches. Nest predation on bird eggs exemplifies opportunistic supplementation, involving systematic searching and selective consumption based on egg detectability rather than random encounter. These adaptive tactics buffer against resource variability, prioritizing energy efficiency in heterogeneous habitats.^[27]^[28]^[16]

Activity patterns and locomotion

The northern pig-tailed macaque (Macaca leonina) is diurnal, exhibiting activity primarily during daylight hours and retreating to sleep sites at night.^[29]^[30] Observations in northeastern Bangladesh using scan sampling at 5-minute intervals identified nine main activity patterns, including locomotion, resting, feeding, grooming, and social interactions, with diurnal variations peaking in mid-morning and late afternoon.^[31] Activity budgets fluctuate seasonally; for instance, in Assam's Inner Line Reserve Forest, groups devoted the most time to locomotion (often exceeding 40%), followed by feeding and resting, adapting to resource availability and environmental conditions.^[32] Locomotion constitutes the dominant behavioral category, comprising up to 46.11% of daily time in studied populations, reflecting their need to traverse large areas for foraging and group cohesion.^[31] These macaques employ quadrupedalism as their primary gait, with a pronograde posture facilitating efficient movement on both terrestrial and arboreal substrates, though they are predominantly arboreal compared to more terrestrial congeners.^[29] They navigate forest canopies via climbing, bridging between branches, and short leaps, occasionally descending to the ground for travel or supplemental feeding, which enhances their adaptability in mixed habitats. Daily path lengths range from 690 to 2,240 meters, varying with fruit distribution—longer when resources are sparse—and moderated by rainfall or heat, which may reduce midday activity to conserve energy. This ranging supports seed dispersal but exposes groups to predation risks during extended terrestrial segments.^[32]

Reproduction and life history

Mating systems

The northern pig-tailed macaque (Macaca leonina) employs a polygynandrous or promiscuous mating system in its multi-male, multi-female social groups, where both sexes mate with multiple partners.^[12] Dominant resident males typically secure priority access to receptive females via prolonged consortships, during which they guard and copulate preferentially, while subordinate males employ alternative tactics such as surreptitious copulations or opportunistic intrusions.^[33] Extra-group males, including subordinate opportunists and super-dominant intruders, also contribute substantially to matings despite limited group residency.^[33] Breeding occurs year-round without strict seasonality, though mating peaks from November to January and birth clusters align with moderate seasonality (33–67% of births in a 3-month period).^[12]^[33] Female receptivity is signaled by perineal swelling, prompting solicitation behaviors like presenting and proceptive mounting toward preferred males; females often mate multiply, rejecting some dominant advances in favor of subordinates or others exhibiting traits like darker red anogenital coloration, which correlates with higher mating rates and consortship formation.^[34]^[35] Male dominance rank correlates positively with observed mating success, yet genetic paternity deviates from strict priority-of-access predictions: high-ranking males sire fewer offspring than expected, middle-ranking residents more, and extra-group males a notable share, reflecting female choice and tactical diversity amid female reproductive synchrony.^[33] Both copulatory (with ejaculation) and non-copulatory mounts occur, the latter serving affiliation or conciliation alongside reproductive functions.^[12]

Gestation, birth, and parental care

The gestation period for female northern pig-tailed macaques (Macaca leonina) lasts approximately 170-180 days, resulting in the birth of a single offspring, with twinning being rare.^[14]^[12] Births occur year-round, though some evidence suggests potential seasonality influenced by environmental factors in wild populations.^[4]^[36] Newborn infants are born with fur and open eyes, immediately clinging to the mother's ventral surface for transport and protection.^[3] Maternal care is the primary form of parental investment, with mothers providing nursing, grooming, and defense against threats during the infant's early development.^[1] Little assistance from other group members is typically observed, though older siblings or matrilineal kin may occasionally interact with the young.^[1] Infants remain dependent on the mother for locomotion and feeding for the first year, gradually weaning as they develop foraging independence around 12 months of age.^[37]

Conservation and human interactions

Population status and trends

The Northern pig-tailed macaque (Macaca leonina) is classified as Vulnerable on the IUCN Red List, with its global population suspected to have declined by more than 30% over the past three generations (approximately 36 years) due to ongoing habitat loss and exploitation, and projected to decline further at a similar or greater rate over the next three generations.^[14] No comprehensive global population estimate exists, reflecting fragmented data and limited surveys across its range from northeastern India through Indochina to southern China; however, available site-specific and national assessments indicate small, declining subpopulations in most countries.^[38]^[3] In China, the population is estimated at fewer than 1,700 individuals, primarily in fragmented forest patches, with no recent updates suggesting stabilization.^[14] Bangladesh hosts a small, isolated subpopulation considered nationally Critically Endangered, with an estimated decline exceeding 20% between 2015 and 2020; a 2021 survey in Satchari National Park documented approximately 117 individuals across three multimale-multifemale groups and six solitary males, yielding a density of 1.2 groups per km² in suitable habitat.^[13]^[39] In India, group sizes in Assam range from 16 to 33 individuals, but broader trends show rapid decline without quantitative national totals.^[40] Laos records groups rarely exceeding 20 individuals, consistent with habitat fragmentation patterns.^[14] Population declines are driven by deforestation for agriculture, logging, and human encroachment, compounded by hunting for bushmeat, traditional medicine, and the pet trade, with no evidence of recovery in protected areas lacking enforcement.^[3] Recent assessments (post-2020) remain sparse, but extrapolated trends from habitat loss rates indicate continued fragmentation and reduced viability, particularly in peripheral ranges like Bangladesh and Myanmar where subpopulations are most precarious.^[13]^[41]

Primary threats

The primary threats to the Macaca leonina stem from extensive habitat loss and fragmentation, driven by commercial logging, agricultural conversion, and infrastructure projects including roads, dams, and hydropower developments that fragment contiguous forests into isolated patches.^[3] These activities reduce availability of fruiting trees and arboreal sleeping sites critical for the species' arboreal lifestyle, while increasing human-wildlife conflict at forest edges.^[3] In Southeast Asia, slash-and-burn cultivation and monoculture plantations further degrade semi-evergreen and mixed deciduous forests, with roadkill and electrocution emerging as direct mortality factors in fragmented landscapes.^[13]^[41] Direct persecution through hunting poses an acute risk, with individuals targeted for bushmeat, trophies, and the illegal pet trade, often using indiscriminate methods like snares that affect all age and sex classes.^[3] In China, hunting pressure compounds habitat disturbance, while in Myanmar and Laos, trade for traditional medicine and live export sustains poaching despite legal protections.^[14]^[41] Gold mining and shifting cultivation by indigenous groups add localized habitat pressures, particularly in border regions of India, Bangladesh, and Vietnam.^[14] These combined factors have precipitated a inferred population reduction exceeding 30% over the past three generations (approximately 45 years, based on a generation length of 15 years), supporting the species' classification as Vulnerable on the IUCN Red List. Empirical surveys in protected areas like India's Inner-Line Reserve Forest document ongoing declines linked to these threats, underscoring the inadequacy of current enforcement against encroachment and poaching.^[13]^[42]

Conservation measures and outcomes

The Northern pig-tailed macaque (Macaca leonina) is listed on Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), which requires permits for international trade to ensure it does not threaten the species' survival.^[43] ^[3] National legislation in range countries provides additional safeguards; for instance, in India, it is protected under Schedule I of the Wildlife (Protection) Act, 1972, prohibiting hunting and trade, while Thailand and Vietnam enforce similar wildlife protection laws banning capture and export.^[12] Captive management programs, such as India's National Studbook, support breeding and research to inform wild conservation, though releases are limited.^[12] Habitat conservation emphasizes protected areas across its range, where the species persists in sites including Khao Yai National Park (Thailand), Lawachara National Park and Chunati Wildlife Sanctuary (Bangladesh), Inner Line Reserve Forest (India), and Keo Seima Wildlife Sanctuary (Cambodia).^[14] ^[13] Anti-poaching patrols and community-based monitoring occur in some reserves, such as in Bangladesh's Satchari National Park, aiming to reduce encroachment and logging.^[44] However, these efforts are uneven, with enforcement often hampered by resource shortages and border issues in transboundary habitats. Outcomes remain limited, as the species' global population is estimated to have declined by more than 30% over the past three generations (approximately 36 years), primarily from persistent habitat fragmentation despite protections.^[14] ^[3] Local studies indicate stable troops in select reserves like Inner Line (20-30 individuals observed in 2023), but overall trends show contraction, with extirpations in fragmented lowlands and no evidence of recovery from reintroductions.^[45] Weak implementation, ongoing illegal logging, and agricultural expansion undermine measures, necessitating stronger habitat connectivity and trade enforcement for viability.^[14] ^[3]

Utilization in biomedical research

Northern pig-tailed macaques (Macaca leonina) serve as a valuable non-human primate model in biomedical research, particularly for studies of human immunodeficiency virus type 1 (HIV-1) pathogenesis and persistence, owing to their susceptibility to HIV-1 infection and replication in vivo, which contrasts with the restrictive TRIM5α-mediated block observed in many other Old World monkeys.^[46]^[47] This susceptibility stems from polymorphisms in their TRIM5 gene that permit efficient HIV-1 reverse transcription and integration in peripheral blood mononuclear cells (PBMCs), enabling long-term viral reservoirs akin to those in humans.^[48]^[49] Research utilizing this species has elucidated host-virus interactions, including the role of APOBEC3 proteins in restricting HIV-1 variants and the adaptive evolution of viral accessories like Vpu to counteract tetherin-mediated restriction in M. leonina cells.^[47]^[50] Studies have demonstrated that HIV-1 infection in these macaques induces a heightened interferon-α antiviral state compared to simian immunodeficiency virus (SIV)mac239, highlighting species-specific immune responses that inform HIV-1-specific therapies.^[51] Additionally, genomic analyses of chronically infected northern pig-tailed macaques have revealed transcriptional signatures of nonpathogenic infection states, providing insights into viral latency and potential eradication strategies.^[52] Beyond HIV-1, baseline physiological data from captive colonies, such as serum immunoglobulin, complement, and C-reactive protein levels, support colony management for research sustainability, though primary applications remain virology-focused.^[53] The model's utility is tempered by ethical considerations of sourcing from vulnerable wild populations, but its genetic and immunological parallels to human HIV dynamics justify continued targeted use in controlled settings.^[54]

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leonina were susceptible to human immunodeficiency virus type 1 (HIV-1), which may be due to the absence of a TRIM5 protein restricting HIV-1 replication.
[49]
HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and ...
Our results suggested that NPMs can be infected with HIV-1 and a long-term viral reservoir was formed in NPMs, which might serve as a potential model for HIV-1 ...
[50]
A Novel Vpu Adaptive Mutation of HIV-1 Degrades Tetherin in ...
Mar 27, 2023 · Macaca leonina (northern pig-tailed macaque [NPM]) is susceptible to HIV-1, but host-specific restriction factors limit virus replication in ...
[51]
HIV-1 but not SIVmac239 induces higher interferon-α antiviral state ...
Original article. HIV-1 but not SIVmac239 induces higher interferon-α antiviral state in chronic infected northern pig-tailed macaques (Macaca leonina).
[52]
Genomic Evidence for the Nonpathogenic State in HIV-1–Infected ...
May 3, 2023 · In this study, to understand this macaque–HIV-1 interaction, we assembled a de novo genome and longitudinal transcriptome for this species ...
[53]
Analysis of immunoglobulin, complements and CRP levels in serum ...
This study provides basic serum immunoglobulin and complement data of captive northern pig-tailed macaques, which may prove useful for future breeding efforts ...
[54]
Analysis of immunoglobulin, complements and CRP levels in serum ...
Abstract. The northern pig-tailed macaque (NPM，Macaca leonina) has become a widely used animal model in biomedical research. · References. Ahmed SA, Penhale W, ...