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Red-shanked douc[1]
CITES Appendix I (CITES)[3]
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primates
Suborder: Haplorhini
Infraorder: Simiiformes
Family: Cercopithecidae
Genus: Pygathrix
Species:
P. nemaeus
Binomial name
Pygathrix nemaeus
(Linnaeus, 1771)
Red-shanked douc range

The red-shanked douc (Pygathrix nemaeus) is an arboreal and diurnal Old World monkey belonging to the Colobinae subfamily.[4] They are endemic to Laos, Vietnam and Cambodia.[5] They are known for their bright colors and express exhibit sexual dimorphism through their body size.[6] The species have been declared by the International Union for Conservation of Nature as critically endangered, with the main threats being from hunting, habitat loss and pet trade.[7] They are one of three species from the genus Pygathrix, the other two being the black-shanked douc (Pygathrix nigripes) and the gray-shanked douc (Pygathrix cinerea).[8]

The red-shanked doucs live in fission-fusion, multilevel societies that have a mean of 18 individuals per band.[9] They are folivorous and consume mainly Acacia pruinescens, Ficus racemosa, Millettia nigrescens, Zanthoxylum avicennae and Castanopsis ceratacantha.[10] Their four-chambered stomachs that allow for bacterial fermentation help them with their high fiber diet.[11] In captivity, it was found that they use brachiation as a mode of locomotion approximately half the time while in the wild, it is only 18% of the time.[12] Female doucs have an average menstrual cycle of 26.4 days and remain pregnant for 165-210 days.[6][13]

Geographic Range and Habitat

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The red-shanked douc is native to Indochina; Vietnam, southern Laos and possibly northeastern Cambodia, east of the Mekong river.[5] Before 1967, the douc was completely unstudied.[citation needed] It is the only douc species that inhabits all three countries of Indochina.[4] In Laos, red-shanked doucs occur from the southern Nam Ghong Provincial Protected Area to the central-north part of the country.[5] Laos is believed to have the largest population of red-shanked doucs, with Nakai-Nam Theun National Protected Area in central Laos having the most individuals of approximately 4,420 groups, followed by the Hin Namno National Protected Area.[8] In Vietnam, the species lives between Nghe An and Gia Lai provinces, from 18°29'N to 14°21'N.[14][4] The Son Tra Nature Reserve in central Vietnam holds the greatest Vietnamese population with approximately 700-1300 individuals.[15] The Phong Nha - Ke Bang National Park is also an important Vietnamese site for the species.[4] There was one observation of the red-shanked doucs in Cambodia by Rawson and Ross in 2008 in the Ratanakiri Province at the border of Vietnam.[7] There was a report of a red-shanked douc specimen that was given to the Staatliches Museum by the Dresden Zoological Garden who had said that it originated in Hainan, China but the zoo records no longer exist so it remains uncertain.[16]

Red-shanked doucs are found in evergreen, semi-evergreen and occasionally limestone forests, up to 1,600m in elevation.[4] They are arboreal and spend most of their time in the forest canopy, including to sleep.[7] They occasionally get on the ground to drink water or eat dirt that contains minerals.[citation needed] According to an ecological niche model, red-shanked doucs can live between approximately 14°N to 21°N.[17] Their home range is approximately 36 hectares and they have a core area of 8 hectares, with a smaller range in the dry season of 23.65 hectares and a larger range in the wet season of 32.95 hectares.[6] There are only weak correlations between precipitation, temperature and diet and home range but not enough to draw a conclusion between them.[6]

Characteristics

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Like other doucs, the red-shanked douc is a long, slender monkey. The male has a head and body length of 55-82 cm (21.6-32.3in) with a tail that measures 56-73.5cm (22-29in), and the female is between 59.7-63cm (23.5-24.8in) long with a tail that measures 44-59.7cm (17.3-23.5in) long.[6] Males weigh 8.6-11.4 kilograms (19-25.1lbs), and females 6.6-10.5 kilograms (14.6-23.1lbs).[6]

Red-shanked douc appearance

The red-shanked doucs are among the most colorful primates. They are considered the “queen of primates” thanks to their distinctive and unique appearance.[citation needed] They have agouti hair on their crown, temples, inner thighs, ventral coat, nape of the neck, back, triceps and lateral sides of their arms.[6] Their crown is silver, their temples are red hair and their foreheads are black.[6] They have white whiskers that are approximately 12 cm long for adult males.[6] Their eyes have a high-axis.[6] The fur on their cheeks and on their throat is white.[6] Their collar is orange with black from one shoulder to the other.[6] Their face is a yellow-brown color and they have light blue eyelids.[6] Their inner arms and inner, lateral and back thighs are black while their lower legs are a vibrant red.[6] Their abdomen and back are silver yet their sacral area is white.[6] Both feet and hands are black as well as their nipples.[6] Their tails are white and are oftentimes equal in length to their head and body length.[6]

A red-shanked douc at the Philadelphia Zoo

The coloration has been recorded as gradually becoming less vibrant and having smaller red patches with more southern latitudes.[5] In Nam Ghong Provincial Protected Area in Laos, the red-shanked doucs observed only had small red patches around their ankles.[6]

Although minor, the red-shanked doucs do express sexual dimorphism in their body size, however not in their coloration.[6] There is a slight difference in rump markings between genders: the male has round white spots above the triangle of white on its rump, while the female does not.[18] Males of all ages have a white spot on both sides of the corners of the rump patch, and red and white genitals. [citation needed]

Behavior

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Red-shanked doucs in profile

This monkey communicates using facial expressions. It has a specific play face with the mouth open, teeth partially bared and chin thrust forward.[citation needed] Sometimes, it closes its eyes and paws blindly towards another douc with remarkable disregard for the hazards of doing this when up a tree.[citation needed] A fixed stare is a threat display.[19] A grimace with the mouth open and the teeth exposed is a submissive gesture given in response to a stare and is also used to initiate grooming or play.[19] The red-shanked douc has a low-pitched growl that is given as a threat, and a short, harsh distress squeal.[19] During adult play, they do a eyelid display where they blink their eyes opened and closed to show their light blue eyelids.[19]

They are a fairly peaceful species and agonistic behavior has been very rarely reported.[19] In the San Diego Zoo, researchers observed that in the instances where there was agonistic behavior, it only lasted a few seconds and did not result in injury.[19]

Grooming lasts up to an hour and are most commonly found between adult female doucs.[6] In captivity, young red-shanked doucs were reported to groom and care for infants, showing signs of alloparental care.[6]

Activity Budget

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In a study conducted by Larry Ray Ulibarri and Kylen N. Gartland in 2020, the activity budget of wild red-shanked doucs was: rest at 35.3%, movement at 28.6%, socializing at 21.7%, feeding at 13.7% and self-grooming at 0.7%.[9]

Group Composition

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Group of Red-Shanked Doucs

Red-shanked doucs live in multilevel, fission-fusion societies in one-male/multi-female or multi-male/multi-female groups with a male-to-female ratio of 1.0:1.63 and an adult-to-young ratio of 1.1:1.0.[9] In a study conducted by Lawrence R. Ulibarri and Kylen N. Gartland, the bands contained a mean of 18 individuals in a mean of 2.7 units per band and a mean of 6.5 individuals per unit.[9] Groups of up to 50 have been recorded.[citation needed] A paper published by Lois K Lippold et al. found that group size changed according to the season.[10] Both males and females have their own hierarchies and males are dominant to females.[citation needed] Both males and females will eventually leave the group they were born into.[citation needed]

Red-shanked doucs fuse and fission daily.[9] Units fuse overnight and fission during mornings and early afternoons.[9] When they are fused, they rest more and when they fission, they are more active.[6]

There does not seem to be any difference in daily fission-fusion from wet to dry season yet overall fission-fusion events increased during part of the wet season, from October to December.[9] In the study by Ulibarri and Gartland at the Son Tra Nature Reserve, 55.32% of their observations were fusion events and 44.68% were fission events.[9] Fission-fusion behavior is believed to help with regulating feeding competition.[9] Red-shanked doucs are very inflexible with membership into their groups.[9]

Locomotion

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Red-shanked douc moving in tree

In captivity, red-shanked doucs have been observed to use brachiation as almost half of their locomotion whereas, in the wild, it was found that arm-swinging accounts for an average of 18% of locomotion.[12] In a study done in the wild by Katie E. Bailey et al., it was found that juveniles used arm-swinging the most (34.3%), followed by subadults (21.7%), adult females (17.6%), adult females carrying infants (15.5%), and then adult males (9.8%).[12] This showed that with increased body weight there is a decreased amount of brachiation.[12]

When they travel by foot, their tail will usually hang down.[20] Like all other Old World monkeys, its tail is not prehensile.[citation needed] It uses its tail solely for balance, and it uses its arms and legs to move through the forest along established routes.[citation needed] When on the move, the group is led by adult males, with juvenile males bringing up the rear and the females and infants staying safe in the middle.[citation needed] This douc is an aerial specialist, moving high up in the canopy.[citation needed] It is very agile and frequently makes breath-taking leaps of up to 6 meters (20 feet), leaping with its arms outstretched over its head, pushing off with its legs and landing on two feet.[citation needed]

When the group is untroubled, the red-shanked douc will move noisily from branch to branch through the forest, crashing through foliage, swinging under branches and leaping with two feet together, displaying its remarkable sense of balance.[citation needed] But when a group is disturbed, by either a predator or other dangers, it can flee silently through the trees, away from danger.[citation needed] If it is startled, it may produce loud barks and rush around the trees slapping branches with its hands and feet.[citation needed]

Mating and Development

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Mating

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In captivity, it was found that female red-shanked doucs reach sexual maturity at four years old and males reach it at four years and eight months.[7] Mating occurs all year but has peaks between August-December.[7] In a study at the San Diego Zoo, it was observed that mating was initiated by both genders jutting their jaw forward, raising and lowering their eyebrows, shaking their head and squinting their eyes.[19] Every copulation event observed occurred after the female crouches and presents her sex organ to the male.[19] Single-mount and multiple-mount matings have been reported.[citation needed] Copulation can still happen while the female is pregnant.[6] Female red-shanked doucs go into estrus every 28-30 days and with it, there is a reddening of their rump.[6]

Menstruation and Pregnancy

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According to a study done by Michael Heistermann et al. of red-shanked doucs in captivity, female doucs have an average menstrual cycle of 26.4 days, with their follicular phase lasting an average of 13.1 days and their luteal phase lasting 14.8 days.[13] The same study found that estradiol and estrone are the main types of estrogen present in female red-shanked doucs.[13]

Births occurs all year but has peaks in the fall and the spring; August, September, October, February, March and April.[6] The birth interval is between 16-38 months.[21] The gestation period lasts between 165 and 210 days, resulting in the birth of a single offspring or very rarely, twins.[7][6] In captivity, it was observed that the pregnant female will find a high place in the enclosure to give birth.[6] The head of the infant emerges after 90 minutes of labour which is followed by the placenta that weighs 90-120g.[21] The oldest recorded birth was from a 26 year old female.[6]

Development

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The young are born with their eyes open and they latch on to their mothers instinctively.[citation needed] The baby's body coloration is lighter than an adult's. Its face is more of a blue color and the body is a lighter beige.[6] As it grows older, its body darkens while its face lightens, achieving adult colors at 10 months.[6] In captivity, other group members may look after an infant, and other females may even suckle it.[citation needed] In one study, an orphaned infant was fed by two females in the group and also cared for by a male.[citation needed] The first six months of a red-shanked douc's life is the most challenging.[7] In captivity, red-shanked doucs can live up to 25 years old.[7]

Diet

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Ficus Racemosa

In an eleven year study, conducted by Lois K Lippold et al. in the Son Tra Nature Reserve, they found that red-shanked doucs are highly folivorous, consuming 54.8% buds and young leaves, 22.6% mature leaves, 3.7% leaf petioles and 18.9% other plant parts.[10] Per month, they found that the red-shanked doucs consumed a mean of 18 species per month and a total of 226 species consumed altogether.[10] Out of the 226 species, there are five species that were eaten 47-82% of the time.[10] These are: Acacia pruinescens, Ficus racemosa, Millettia nigrescens, Zanthoxylum avicennae and Castanopsis ceratacantha.[10] The study found that red-shanked doucs are selective feeders and flexible eaters because of their ability to eat a wide variety of food in all seasons.[10] Fruit is consumed mainly in the morning, which is common amongst leaf-eating monkeys as this is where they derive their energy for the day.[10] They have different eating patterns during the wet season and the dry season both in what they eat and in the parts of the plants that they eat, although it is not a drastic change.[10] Figs however, were found to be consumed all year long and made up 16-36% of their diet.[10] It is the second most commonly consumed plant by the red-shanked doucs and they ate the fruit, leaves and flowers of it.[10]

They eat peacefully together, not quarreling over food, and have been known to share their food with others.[22] Often, they will share the same clump of foliage and may even break pieces off and hand them to each other, a type of active generosity that is rare among Old World monkeys.[22] They do not have cheek pouches.[citation needed]

Digestion

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Belonging to the subfamily Colobinae, or leaf-eating monkeys, the red-shanked douc has a large four-chambered stomach containing bacteria that breaks down the cellulose and fiber in the leaves through fermentation, giving the douc its pot-bellied look.[11] This also makes it burp frequently from the resulting gas.[citation needed] They have a saccus gastricus and a presaccus with a stratified squamous epithelium lining, due to their high level of folivory.[11][6] These are parts of their complex stomach that helps with bacterial fermentation and is thought to be a synapomorphic trait.[11] Their teeth are also adapted to chew leaves; they are characterized by high crowned molars and small incisors.[10]

Conservation

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In 2000, the IUCN Red List of Threatened Species classified the red-shanked douc langur as endangered.[13] In 2020, the IUCN updated their classification of the species to critically endangered due to the population’s continual decline.[15] It was also listed in the Vietnam Red Book in 2007.[15] In 2019, the Vietnamese Prime Minister classified them as a high risk species that needs protection in Decree 06.[15] The species is listed in CITES I which prohibits commercial international trade.[citation needed] More than half of the species has been lost in the past 30-40 years.[5]

The main threat for the red-shanked douc is from hunting. The meat is used for food, traditional medicine and for international sale or trade.[8] Local people often hunt the species for consumption, pets or making glue.[citation needed] Although hunting of the species is technically illegal, it is not strictly enforced and has little effect.[5] In Dong Ampham National Protected Area in Laos on the border of Vietnam, local hunters estimated that approximately 50 red-shanked doucs are killed each year.[5] From 2015-2018, the Bach Ma National Park Forestry Protection department in Vietnam confiscated 13kg of red-shanked douc meat.[15] Their behavioral characteristics are believed to make the species particularly easy to hunt.[4] In this region, the meat of the red-shanked douc is reported as being a favorite food.[5] Vietnam has the highest hunting levels of the species.[5]

Red-shanked douc in captivity

Their other main threats are pet trade, habitat fragmentation, creation of agricultural land and military installation.[5][14]

With Laos having the biggest population of red-shanked doucs, the country has been marked as being the most important for conservation of the species.[5] A study conducted by Camille N. Z. Coudrat et al. stated that the best approach to conserving the species is to focus on the largest populations, specifically in Laos.[5] At present, there is no conservational action in Laos.[8] There have been efforts to breed red-shanked doucs in captivity since the late 1960s but they are difficult to keep in zoos due to factors such as their diet and so currently, there are only 33 individuals in captivity worldwide.[10][13]

For the population in Sơn Trà, habitat loss due to development plans poses the biggest risk to them.[citation needed] Historically, Son Tra had a military installation and so many animals in the region were shot as practice targets.[14] Currently, the red-shanked doucs in Son Tra Nature Reserve are protected by the Army, Police and Forest Protection departments of Danang and Son Tra.[10]

References

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  1. ^ Groves, C. P. (2005). Wilson, D. E.; Reeder, D. M. (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Baltimore: Johns Hopkins University Press. p. 173. ISBN 0-801-88221-4. OCLC 62265494.
  2. ^ Coudrat, C.N.Z.; Quyet, L.K.; Duc, H.; Phiaphalath, P.; Rawson, B.M.; Nadler, T.; Ulibarri, L.; Duckworth, J.W. (2020). "Pygathrix nemaeus". IUCN Red List of Threatened Species. 2020: e.T39826A17941247. doi:10.2305/IUCN.UK.2020-2.RLTS.T39826A17941247.en. Retrieved 19 November 2021.
  3. ^ "Appendices | CITES". cites.org. Retrieved 2022-01-14.
  4. ^ a b c d e f Anh, Nguyen Tuan; Minh, Le Duc; Hung, Pham Viet; Duyen, Vu Thi (2019-09-13). "Modeling the Red-shanked Douc (Pygathrix nemaeus) distribution in Vietnam using Maxent". VNU Journal of Science: Earth and Environmental Sciences. 35 (3). doi:10.25073/2588-1094/vnuees.4390. ISSN 2588-1094.
  5. ^ a b c d e f g h i j k l Coudrat, Camille N. Z.; Duckworth, John W.; Timmins, Robert J. (2012-10). "Distribution and Conservation Status of the Red-Shanked Douc (Pygathrix nemaeus) in Lao PDR: An Update: Conservation of Pygathrix nemaeus in Laos". American Journal of Primatology. 74 (10): 874–889. doi:10.1002/ajp.22027. {{cite journal}}: Check date values in: |date= (help)
  6. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z aa ab ac ad ae Ray., Ulibarri, Larry (2013). The socioecology of red-shanked doucs (Pygathrix nemaeus) in Son Tra Nature Reserve, Vietnam. ISBN 978-1-303-64903-5. OCLC 890512525.{{cite book}}: CS1 maint: multiple names: authors list (link)
  7. ^ a b c d e f g h Huy, Phong Nguyen-Phong. Primates (Red-shanked Douc Langur and Pygmy Slow Loris) Report.
  8. ^ a b c d Coudrat, C. N. Z.; Nanthavong, C.; Nekaris, K. A. I. (2014-10). "Conservation of the red-shanked douc Pygathrix nemaeus in Lao People's Democratic Republic: density estimates based on distance sampling and habitat suitability modelling". Oryx. 48 (4): 540–547. doi:10.1017/S0030605313000124. ISSN 0030-6053. {{cite journal}}: Check date values in: |date= (help)
  9. ^ a b c d e f g h i j Ulibarri, Lawrence R.; Gartland, Kylen N. (2021). "Group Composition and Social Structure of Red-Shanked Doucs (Pygathrix nemaeus) at Son Tra Nature Reserve, Vietnam". Folia Primatologica. 92 (4): 191–202. doi:10.1159/000518594. ISSN 0015-5713. {{cite journal}}: no-break space character in |first2= at position 6 (help); no-break space character in |first= at position 9 (help)
  10. ^ a b c d e f g h i j k l m n Lippold, Lois K.; Thanh, Vu Ngoc; Nghia, Tran Dinh; Duc, Nguyen Anh (2022). "Feeding Ecology of Red-Shanked Douc Langurs at Son Tra Nature Reserve, Da Nang, Vietnam". Primate Conservation. 36.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  11. ^ a b c d Clayton, Jonathan B.; Shields‐Cutler, Robin R.; Hoops, Susan L.; Al‐Ghalith, Gabriel A.; Sha, John C. M.; Johnson, Timothy J.; Knights, Dan (2019-10). "Bacterial community structure and function distinguish gut sites in captive red‐shanked doucs ( Pygathrix nemaeus )". American Journal of Primatology. 81 (10–11). doi:10.1002/ajp.22977. ISSN 0275-2565. PMC 6800578. PMID 30997937. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link)
  12. ^ a b c d Bailey, Katie E.; Winking, Jeffrey W.; Carlson, David L.; Tran Van Bang; Ha Thang Long (2020-08-01). "Arm-Swinging in the Red-Shanked Douc (Pygathrix nemaeus): Implications of Body Mass". International Journal of Primatology. 41 (4): 583–595. doi:10.1007/s10764-020-00163-6. ISSN 1573-8604.
  13. ^ a b c d e Heistermann, Michael; Ademmer, Christelle; Kaumanns, Werner (2004-06). "Ovarian Cycle and Effect of Social Changes on Adrenal and Ovarian Function in Pygathrix nemaeus". International Journal of Primatology. 25 (3): 689–708. doi:10.1023/b:ijop.0000023581.17889.0f. ISSN 0164-0291. {{cite journal}}: Check date values in: |date= (help)
  14. ^ a b c Lippold, Lois K.; Thanh, Vu Ngoc (2008-11). "The Time is Now: Survival of the Douc Langurs of Son Tra, Vietnam". Primate Conservation. 23 (1): 75–79. doi:10.1896/052.023.0108. ISSN 0898-6207. {{cite journal}}: Check date values in: |date= (help)
  15. ^ a b c d e Van Minh, Nguyen. Conservation of the Red-Shanked Douc Langurs (Pygathix nemaeus) in Bach Ma National Park: An Update on Distribution and Population Size.
  16. ^ Fooden, Jack; Feiler, Alfred (1988-06). "Pygathrix nemaeus in Hainan? new evidence, no resolution". International Journal of Primatology. 9 (3): 275–279. doi:10.1007/bf02737404. ISSN 0164-0291. {{cite journal}}: Check date values in: |date= (help)
  17. ^ Bett, Nolan N.; Blair, Mary E.; Sterling, Eleanor J. (2012-08). "Ecological Niche Conservatism in Doucs (Genus Pygathrix)". International Journal of Primatology. 33 (4): 972–988. doi:10.1007/s10764-012-9622-3. ISSN 0164-0291. {{cite journal}}: Check date values in: |date= (help)
  18. ^ Gron, K. J. (2009). "Primate Factsheets: Douc langur (Pygathrix)". Retrieved 2012-04-20.
  19. ^ a b c d e f g h Kavanagh, Michael (1978-01). "The social behaviour of doucs (Pygathrix nemaeus nemaeus) at San Diego Zoo". Primates. 19 (1): 101–114. doi:10.1007/bf02373228. ISSN 0032-8332. {{cite journal}}: Check date values in: |date= (help)
  20. ^ Stevens, N. J., Wright, K. A., Covert, H. H., & Nadler, T. (2008). "ail postures of four quadrupedal leaf monkeys (Pygathrix nemaeus, P. cinerea, Trachypithecus delacouri and T. hatinhensis) at the Endangered Primate Rescue Center, Cuc Phuong National Park, Vietnam" (PDF). Vietnamese Journal of Primatology 1. 2.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  21. ^ a b RUEMPLER, U. (1998-01). "Husbandry and breeding of Douc langurs Pygathrix nemaeus nemaeus at Cologne Zoo". International Zoo Yearbook. 36 (1): 73–81. doi:10.1111/j.1748-1090.1998.tb02887.x. ISSN 0074-9664. {{cite journal}}: Check date values in: |date= (help)
  22. ^ a b KAVANAGH, MICHAEL (1972-10). "Food-sharing Behaviour within a Group of Douc Monkeys (Pygathrix nemaeus nemaeus)". Nature. 239 (5372): 406–407. doi:10.1038/239406a0. ISSN 0028-0836. {{cite journal}}: Check date values in: |date= (help)
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