Journal of Guangxi Normal University(Natural Science Edition) ›› 2022, Vol. 40 ›› Issue (5): 354-365.doi: 10.16088/j.issn.1001-6600.2021111201

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Research Progress on Interaction between Non-human Primate Gastrointestinal Parasite and Host

LU Meijing1,2, FAN Penglai1,2, SUN Tao1,2*, ZHOU Qihai1,2*   

  1. 1. Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, Guilin Guangxi 541006, China;
    2. Guangxi Key Laboratory of Rare and Endangered Animal Ecology (Guangxi Normal University), Guilin Guangxi 541006, China
  • Received:2021-11-12 Revised:2021-12-08 Online:2022-09-25 Published:2022-10-18

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Abstract: Gastrointestinal parasite is an important part of the host body and have an important impact on the growth and development of the host and immune diseases. With the increasing contact between non-human primates and humans, non-human primates are at increasing risk of gastrointestinal parasites. New diseases caused by gastrointestinal parasites pose a serious threat to the survival of primates and have become an important challenge for primate protection. This article summarizes the types and characteristics of non-human primate gastrointestinal parasites, and discusses the social behavior, growth and development, foraging and nutrition, immunity and disease, defense, and defense of intestinal parasites and non-human primate hosts. The impact of human activities on non-human primate gastrointestinal parasites and other aspects are reviewed, in order to provide a certain theoretical basis and new ideas for the study of the role of non-human primate gastrointestinal parasites and public health.

Key words: primate, zoonosis, gastrointestinal parasite, contagion

CLC Number: 

  • S852.7
[1]CAPITANIO J P, EMBORG M E. Contributions of non-human primates to neuroscience research[J]. The Lancet, 2008, 371(9618): 1126-1135. DOI:10.1016/s0140-6736(08)60489-4.
[2]黄涛, 张海涛, 李志雄, 等. 非人灵长类动物在病毒感染模型中的研究进展[J]. 中国实验动物学报, 2021, 29(2): 248-255. DOI:10.3969/j.issn.1005-4847.2021.02.016.
[3]VEITCH J S M, BOWMAN J, MASRTOMONACO G, et al. Corticosterone response by Peromyscus mice to parasites, reproductive season, and age[J]. General and Comparative Endocrinology, 2021, 300: 113640. DOI:10.1016/j.ygcen.2020.113640.
[4]ALBANI A, DE LIBERATO C, WAHID I, et al. Preliminary assessment of gastrointestinal parasites in two wild groups of endangered moor macaques (Macaca maura) from Sulawesi[J]. International Journal of Primatology, 2019, 40(6): 671-686. DOI:10.1007/s10764-019-00114-w.
[5]LALREMRUATI P, SOLANKI G S. Prevalence and seasonal variation of gastrointestinal parasites among captive Northern Pig-tailed Macaque Macaca leonina (Mammalia: Primates: Cercopithecidae)[J]. Journal of Threatened Taxa, 2020, 12(3): 15370-15374. DOI:10.11609/jott.5050.12.3.15370-15374.
[6]HOUMSOU R S, BUBA U, AMUTA E U, et al. Gastrointestinal parasites of non-human primates and the zoonotic implications in Gashaka-Gumti National Park, Nigeria[J]. Sokoto Journal of Veterinary Sciences, 2019, 17(2): 11-19. DOI:10.4314/sokjvs.v17i2.2.
[7]PATRA G, LALREMRUATI P, GHOSH S, et al. Prevalence of gastrointestinal parasites in captive non-human primates of zoological gardens in North-Eastern region of India[J]. Biological Rhythm Research, 2020, 51(5): 690-698. DOI:10.1080/09291016.2018.1557854.
[8]LI M, ZHAO B, LI B, et al. Prevalence of gastrointestinal parasites in captive non-human primates of twenty-four zoological gardens in China[J]. Journal of Medical Primatology, 2015, 44(3): 168-173. DOI:10.1111/jmp.12170.
[9]MORAND S. (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification[J]. International Journal for Parasitology: Parasites and Wildlife, 2015, 4(1): 80-87. DOI:10.1016/j.ijppaw.2015.01.001.
[10]RUSHMORE J, BISANZIO D, GILLESPIE T R. Making new connections: insights from primate-parasite networks[J]. Trends in Parasitology, 2017, 33(7): 547-560. DOI:10.1016/j.pt.2017.01.013.
[11]CROSS P C, DREWE J, PATREK V, et al. Wildlife population structure and parasite transmission: implications for disease management[M]// DELAHAY R J, SMITH G C, HOTCHINGS M R. Management of Disease in Wild Mammals. Tokyo: Springer, 2009: 9-29.
[12]APONTE V, LOCKE S A, GENTES M L, et al. Effect of habitat use and diet on the gastrointestinal parasite community of an avian omnivore from an urbanized environment[J]. Canadian Journal of Zoology, 2014, 92(7): 629-636. DOI:10.1139/cjz-2013-0268.
[13]CHAPMAN C A, GILLESIPE T R, GOLDBERG T L. Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions?[J]. Evolutionary Anthropology Issues News & Reviews, 2005, 14(4): 134-144. DOI:10.1002/evan.20068.
[14]SCHMID-HEMPEL P. Parasites and their social hosts[J]. Trends in Parasitology, 2017, 33(6): 453-462. DOI:10.1016/j.pt.2017.01.003.
[15]LANE-DEGRAAF K E, PUTRA I G A A, WANDIA I N, et al. Human behavior and opportunities for parasite transmission in communities surrounding long-tailed macaque populations in Bali, Indonesia[J]. American Journal of Primatology, 2014, 76(2): 159-167. DOI:10.1002/ajp.22218.
[16]BARBOSA A D S, PINHEIRO J L, DOS SANTOS C R, et al. Gastrointestinal parasites in captive animals at the Rio de Janeiro Zoo[J]. Acta Parasitologica, 2020, 65(1): 237-249. DOI:10.2478/s11686-019-00145-6.
[17]叶玭婧, 姚辉, 向左甫. 非人灵长类肠道寄生虫研究进展[J]. 安徽农业科学, 2013(12): 5384-5388. DOI:10.13989/j.cnki.0517-6611.2013.12.074.
[18]ADRUS M, ZAINUDIN R, AHAMAD M, et al. Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia[J]. Journal of Medical Primatology, 2019, 48(1): 22-31. DOI:10.1111/jmp.12389.
[19]吕超超, 王岩, 宁长申, 等. 野生太行猕猴肠道寄生虫感染的初步调查[J]. 动物学杂志, 2009, 44(1): 74-79. DOI:10.3969/j.issn.0250-3263.2009.01.011.
[20]杨天友, 莫忠妹, 熊富玉, 等. 贵州麻阳河自然保护区黑叶猴肠道寄生虫初步调查[J]. 野生动物学报, 2021, 42(4): 1171-1176.
[21]吴伟, 孙丙华, 王希, 等. 雄性短尾猴的等级顺位、睾酮水平与肠道寄生虫感染强度的关系[J]. 兽类学报, 2018, 38(5): 451-457.
[22]LILLY A A, MEHLMAN P T, DORAN D. Intestinal parasites in Gorillas, Chimpanzees, and humans at Mondika research site, Dzanga-Ndoki National Park, Central African Republic[J]. International Journal of Primatology,2002,23(3): 555-573. DOI:10.1023/A:1014969617036.
[23]PEDERSEN A B, DAVIES T J. Cross-species pathogen transmission and disease emergence in primates[J]. EcoHealth, 2009, 6(4): 496-508. DOI:10.1007/s10393-010-0284-3.
[24]JONES B F, CAPPELLO M. Trematodes[M]// JOHNSON L R. Encyclopedia of Gastroenterology. New York: Academic Press, 2004: 523-526.
[25]BRUNET J, PESSON B, CHERMETTE R, et al. First case of peritoneal cysticercosis in a non-human primate host (Macaca tonkeana) due to Taenia martis[J]. Parasites & Vectors, 2014, 7(1): 422. DOI:10.1186/1756-3305-7-422.
[26]TAPPE D, BREHM K, FROSCH M, et al. Echinococcus multilocularis infection of several Old World monkey species in a breeding enclosure[J]. The American Journal of Tropical Medicine and Hygiene, 2007, 77(3): 504-506. DOI:10.4269/ajtmh.2007.77.504.
[27]KAMEL A A, ABDEL-LATEF G K. Prevalence of intestinal parasites with molecular detection and identification of Giardia duodenalis in fecal samples of mammals, birds and zookeepers at Beni-Suef-Zoo, Egypt[J]. Journal of Parasitic Diseases, 2021, 45(3): 695-705. DOI:10.1007/s12639-020-01341-2.
[28]MRAVCOVÖ K, ŠTRKOLCOVÁ G, MUCHA R, et al. Zoonotic assemblages of Giardia duodenalis in captive non-human primates from the largest zoo in Slovakia[J]. Journal of Parasitic Diseases, 2021, 45(2): 302-305. DOI:10.1007/s12639-020-01324-3.
[29]李家诚, 曹杰, 何国声, 等. 野生动物寄生虫的研究进展[J]. 中国兽医寄生虫病, 2007,15(5): 45-48. DOI:10.3969/j.issn.1674-6422.2007.05.013.
[30]WACHTMAN L M, MANSFIELD K G. Opportunistic infections in immunologically compromised nonhuman primates[J]. ILAR Journal, 2008, 49(2): 191-208. DOI:10.1093/ilar.49.2.191.
[31]PAFCO B, TEHLÖROVÖ Z, JIRKU POMAJBíKOVÖ K, et al. Gastrointestinal protists and helminths of habituated agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic[J]. American Journal of Primatology, 2018, 80(2): e22736. DOI:10.1002/ajp.22736.
[32]潘卫庆, 张龙兴, 魏梅雄, 等. 寄生虫生物学研究与应用[M]. 北京: 化学工业出版社,2007: 342.
[33]谢明权, 李国清. 现代寄生虫学[M]. 广州: 广东科技出版社,2003: 564.
[34]FRIANT S, ZIEGLER T E, GOLDBERG T L. Primate reinfection with gastrointestinal parasites: behavioural and physiological predictors of parasite acquisition[J]. Animal Behaviour, 2016, 117: 105-113. DOI:10.1016/j.anbehav.2016.04.006.
[35]KUMAR S, KUMARA H N, SANTHOSH K, et al. Prevalence of gastrointestinal parasites in lion-tailed macaque Macaca silenus in central Western Ghats, India[J]. Primates, 2019, 60(6): 537-546. DOI:10.1007/s10329-019-00751-y.
[36]ZANZANI S A, GAZZONIS A L, EPIS S, et al. Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis)[J].Parasitology Research, 2016, 115(1): 307-312. DOI:10.1007/s00436-015-4748-9.
[37]LARBI J A, AKYEAMPONG S, ABUBAKARI A, et al. Zoonotic gastrointestinal parasites of Baboons (Papio anubis) in the Shai Hill Reserve in Ghana[J]. BioMed Research International, 2020, 2020: 1083251. DOI:10.1155/2020/1083251.
[38]王宏, 李鹤龄, 陈智岗, 等. 猕猴肠道寄生虫研究进展[J]. 安徽农业科学, 2021, 49(14): 1-3,7.
[39]CHAPMAN C A, SPEIRS M L, GILLESPIE T R, et al. Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups[J]. American Journal of Primatology, 2006, 68(4): 397-409. DOI:10.1002/ajp.20233.
[40]GILLESPIE T R,CHAPMAN C A. Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest[J]. American Journal of Primatology, 2008, 70(3): 222-230. DOI:10.1002/ajp.20475.
[41]BOUNDENGA L, MOUSSADJI C, MOMBO I M, et al. Diversity and prevalence of gastrointestinal parasites in two wild Galago species in Gabon[J]. Infection Genetics and Evolution, 2018, 63: 249-256. DOI:10.1016/j.meegid.2018.04.035.
[42]ZHANG Q X,HAN S Y, LIU K S, et al. Occurrence of selected zoonotic fecal pathogens and first molecular identification of Hafnia paralvei in wild Taihangshan Macaques (Macaca mulatta tcheliensis) in China[J]. Biomed Research International, 2019, 2019: 2494913. DOI:10.1155/2019/2494913.
[43]HUSSAIN S, RAM M S, KUMAR A, et al. Human presence increases parasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in Southern India[J]. Plos One, 2013, 8(5): e63685. DOI:10.1371/journal.pone.0063685.
[44]WEYHER A H, ROSS C, SEMPLE S. Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria[J]. International Journal of Primatology, 2006, 27(6): 1519-1534. DOI:10.1007/s10764-006-9089-1.
[45]LI H L, LI Q, DONG L, et al. Prevalence of Balantidium coli infection in bred rhesus monkeys (Macaca mulatta) in Guangxi, southern China[J]. Iranian Journal of Parasitology, 2014, 9(1): 125-128. DOI:10.1016/B978-0-12-800099-1.00005-3.
[46]BLERSCH R, BONNEL T R, BARRETT L, et al. Seasonal effects in gastrointestinal parasite prevalence, richness and intensity in vervet monkeys living in a semi-arid environment[J]. Journal of Zoology, 2021, 314(3):163-173. DOI:10.1111/jzo.12877.
[47]张波, 叶玭婧, 卢浪, 等. 生态旅游对川金丝猴肠道寄生虫的影响[J]. 兽类学报, 2017, 37(1): 66-77.
[48]KLAUS A, ZIMMERMANN E, ROPER K M, et al. Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo[J]. International Journal for Parasitology. Parasites and Wildlife, 2017, 6(3): 320-329. DOI:10.1016/j.ijppaw.2017.09.005.
[49]WEERASEKARA L,WIJESOORIYA K, RANAWANA K, et al. Gastrointestinal parasites of endemic and endangered free-ranging purple-faced leaf monkey (Semnopithecus vetulus) in Sri Lanka: effect of host group size and habitat type[J]. Primates, 2021, 62(4): 629-635. DOI:10.1007/s10329-021-00902-0.
[50]MARTÍNEZ-MOTA D, POZO-MONTUY G, BONILLA SÖNCHEZ Y M, et al. Effects of anthropogenic stress on the presence of parasites in a threatened population of black howler monkeys (Alouatta pigra)[J]. Therya, 2018, 9(2): 161-169. DOI:10.12933/therya-18-572.
[51]HABIG B, JANSEN D A W A M, AKINYI M Y, et al. Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus)[J]. Behavioral Ecology and Sociobiology, 2019, 73(10): 134. DOI:10.1007/s00265-019-2748-y.
[52]MACINTOSH A J J, HERNANDEZ A D, HUFFMAN M A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques[J]. Primates, 2010, 51(4): 353-364. DOI:10.1007/s10329-010-0211-9.
[53]BALASUBRAMANIAM K N, BEISNER B A, HUBBARD J A, et al. Affiliation and disease risk: social networks mediate gut microbial transmission among rhesus macaques[J]. Animal Behaviour, 2019, 151: 131-143. DOI:10.1016/j.anbehav.2019.03.009.
[54]HOFMANN H A, BEERY A K, BLUMSTEIN D T, et al. An evolutionary framework for studying mechanisms of social behavior[J]. Trends in Ecology and Evolution, 2014, 29(10): 581-589. DOI:10.1016/j.tree.2014.07.008.
[55]STOCKMAIER S, STROEYMEYT N, SHATTUCK E C, et al. Infectious diseases and social distancing in nature[J]. Science, 2021, 371(6533): eabc8881. DOI:10.1126/science.abc8881.
[56]POULIN R, FILION A. Evolution of social behaviour in an infectious world: comparative analysis of social network structure versus parasite richness[J]. Behavioral Ecology and Sociobiology, 2021, 75(7): 105. DOI:10.1007/s00265-021-03039-8.
[57]RIMBACH R, BISANZIO D, GALVIS N, et al. Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics[J]. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 2015, 370(1669): 20140110. DOI:10.1098/rstb.2014.0110.
[58]DUBOSCQ J, ROMANO V, SUEUR C, et al. Network centrality and seasonality interact to predict lice load in a social primate[J]. Scientific Reports 2016, 6(1): 22095. DOI:10.1038/srep22095.
[59]MACLNTOSH A J J, JACOBS A, GARCIA C, et al. Monkeys in the middle: parasite transmission through the social network of a wild primate[J]. PLoS One, 2012, 7(12): e51144. DOI:10.1371/journal.pone.0051144.
[60]POULIN R. Modifcation of host social networks by manipulative parasites[J]. Behaviour, 2018, 155: 671-688.
[61]GHAI R R, FUGÈRE V, CHAPMAN C A, et al. Sickness behaviour associated with non-lethal infections in wild primates[J]. Proceedings of the Royal Society B-Biological Sciences, 2015, 282(1814): 20151436. DOI:10.1098/rspb.2015.1436.
[62]CHAPMAN C A, FRIANT S, GODFREY K, et al. Social behaviours and networks of vervet monkeys are influenced by gastrointestinal parasites[J]. PLoS One, 2016, 11(8): e0161113. DOI:10.1371/journal.pone.0161113.
[63]MARCOGLIESE D J. Parasites: small players with crucial roles in the ecological theater [J]. EcoHealth, 2004, 1(2): 151-164. DOI:10.1007/s10393-004-0028-3.
[64]SPRINGER A, KAPPELER P M. Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar[J]. Primate Biology, 2016, 3(2): 51-63. DOI:10.5194/pb-3-51-2016.
[65]BELDOMENICO P M, BEGON M. Disease spread, susceptibility and infection intensity: vicious circles?[J]. Trends in Ecology and Evolution 2010, 25(1): 21-27. DOI:10.1016/j.tree.2009.06.015.
[66]FORBES K M, MAPPES T, SIRONEN T, et al. Food limitation constrains host immune responses to nematode infections[J]. Biology Letters, 2016, 12(9): 20160471. DOI:10.1098/rsbl.2016.0471.
[67]EBERHARDT A T, COSTA S A, MARINI M R, et al. Parasitism and physiological trade-offs in stressed capybaras[J]. Plos One, 2013, 8(7): e70382. DOI:10.1371/journal.pone.0070382.
[68]AGOSTINI I, VANDERHOEVEN E, DI BITETTI M S, et al. Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys[J]. Scientific Reports, 2017, 7(1): 12778. DOI:10.1038/s41598-017-12803-8.
[69]RESASCO J, BITTERS M E, CUNNINGHAM S A, et al. Experimental habitat fragmentation disrupts nematode infections in Australian skinks[J]. Ecology, 2019, 100(1): e02547. DOI:10.1002/ecy.2547.
[70]PETKEVI Č S. The interaction between intestinal helminth infection and host nutrition. Review[J]. Veterinarija ir Zootechnika, 2007, 37(59): 53-60.
[71]CLOUGH D, PRYKHODKO O, RÅBERG L. Effects of protein malnutrition on tolerance to helminth infection[J]. Biology Letters, 2016, 12(6): 20160189. DOI:10.1098/rsbl.2016.0189.
[72]VITONE N D, ALTIZER S, NUNN C L. Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates[J]. Evolutionary Ecology Research, 2004, 6(2): 183-199. DOI:10.1111/j.0014-3820.2004.tb01661.x.
[73]CHAPMAN C A, WASSERMAN M D, GILLESPIE T R, et al. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?[J]. American Journal of Physical Anthropology, 2006, 131(4): 525-534. DOI:10.1002/ajpa.20477.
[74]李宗起, 钱雄, 赵西斌. 小儿肠道寄生虫感染对生长发育的影响分析[J].中国地方病防治杂志, 2019, 34(2): 236-237,240.
[75]叶玭婧. 川金丝猴投食群与野生群秋冬季肠道寄生虫研究[D]. 长沙: 中南林业科技大学, 2013.
[76]MAIZELS R M. Parasitic helminth infections and the control of human allergic and autoimmune disorders[J]. Clinical Microbiology and Infection, 2016, 22(6): 481-486. DOI:10.1016/j.cmi.2016.04.024.
[77]MUEHLENBEIN M P,WATTS D P. The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees[J]. BioPsychoSocial Medicine, 2010, 4(1): 21. DOI:10.1186/1751-0759-4-21.
[78]吴阳, 任红玲, 徐珊珊, 等. 寄生虫感染与宿主细胞自噬相互作用研究进展[J]. 中国血吸虫病防治杂志, 2020, 32(6): 654-656,660. DOI:10.16250/j.32.1374.2019241.
[79]HUFFMAN M A, CATON J M. Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees[J]. International Journal of Primatology, 2001, 22(3): 329-346. DOI:10.1023/A:1010734310002.
[80]CAZELLES-DURAND N, MALOUEKI U, RACHID L, et al. Première observation d’un comportement de Leaf Swallowing chez des chimpanzés vivant en captivité à la Réserve Africaine de Sigean, France[J]. Revue de Primatologie, 2020, 11:1. DOI:10.4000/primatologie.8231.
[81]BARELLI C, HUFFMAN M A. Leaf swallowing and parasite expulsion in Khao Yai white-handed gibbons (Hylobates lar), the first report in an Asian ape species[J]. American Journal of Primatology, 2017, 79(3): e22610. DOI:10.1002/ajp.22610.
[82]SMITH R L, HAYES S E, SMITH P, et al. Sleeping site preferences in Sapajus cay Illiger 1815 (Primates: Cebidae) in a disturbed fragment of the Upper Paraná Atlantic Forest, Rancho Laguna Blanca, Eastern Paraguay[J]. Primates, 2018, 59(1): 79-88. DOI:10.1007/s10329-017-0626-7.
[83]POIROTTE C, SARABIAN C, NGOUBANGOYE B, et al. Faecal avoidance differs between the sexes but not with nematode infection risk in mandrills[J]. Animal Behaviour, 2019, 149: 97-106. DOI:10.1016/j.anbehav.2019.01.013.
[84]SARABIAN C, NGOUBANGOYE B, MACINTOSH A J J. Divergent strategies in faeces avoidance between two cercopithecoid primates[J]. Royal Society Open Science, 2020, 7(3): 191861. DOI:10.1098/rsos.191861.
[85]TASDEMIR D, MACLNTOSH A J J, STERGIOU P, et al. Antiprotozoal and antihelminthic properties of plants ingested by wild Japanese macaques (Macaca fuscata yakui) in Yakushima Island[J]. Journal of Ethnopharmacology, 2020, 247: 112270. DOI:10.1016/j.jep.2019.112270.
[86]COUSINS D, HUFFMAN M A. Medicinal properties in the diet of gorillas: an ethno-pharmacological evaluation[J]. African Study Monographs, 2002, 23(2): 65-89. DOI:10.14989/68214.
[87]王文琴, 刘述先. 不同宿主感染血吸虫后的自愈现象[J]. 中国寄生虫学与寄生虫病杂志, 2003, 21(3): 179-182. DOI:10.3969/j.issn.1000-7423.2003.03.016.
[88]CHAKRABORTY D, REDDY M, TIWARI S, et al. Land use change increases wildlife parasite diversity in Anamalai Hills, Western Ghats, India[J]. Scientific Reports, 2019, 9(1): 11975. DOI:10.1038/s41598-019-48325-8.
[89]ARROYO-RODRÍGUEZ V, DIAS P A D. Effects of habitat fragmentation and disturbance on howler monkeys: a review[J]. American Journal of Primatology, 2010, 72(1): 1-16. DOI:10.1002/ajp.20753.
[90]VAN DYKE F. Conservation biology: foundations concepts applications[M]. Boston: McGraw-Hill, 2003: 413.
[91]POULIN R. Best practice guidelines for studies of parasite community ecology[J]. Journal of Helminthology, 2019, 93(1): 8-11. DOI:10.1017/S0022149X18000767.
[92]BARELLI C, GONZALEZ-ASTUDILLO V, MUNDRY R, et al. Correction: altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum[J]. PLoS One, 2021, 16(5): e0251617. DOI:10.1371/journal.pone.0225142.
[93]ZHAO X M, REN B P, LI D Y, et al. Effects of habitat fragmentation and human disturbance on the population dynamics of the Yunnan snub-nosed monkey from 1994 to 2016[J]. PeerJ, 2019, 7: e6633. DOI:10.7717/peerj.6633.
[94]BLOOMFIELD L S P, MCINTOSH T L, LAMBIN E F. Habitat fragmentation, livelihood behaviors, and contact between people and nonhuman primates in Africa[J]. Landscape Ecology, 2020, 35(4): 985-1000. DOI:10.1007/s10980-020-00995-w.
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[4] WENG Ye, SHAO Desheng, GAN Shu. Principal Component Liu Estimation Method of the Equation    Constrained Ⅲ-Conditioned Least Squares[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(4): 115 -125 .
[5] QIN Chengfu, MO Fenmei. Structure ofC3-and C4-Critical Graphs[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(4): 145 -153 .
[6] HE Qing, LIU Jian, WEI Lianfu. Single-Photon Detectors as the Physical Limit Detections of Weak Electromagnetic Signals[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(5): 1 -23 .
[7] TIAN Ruiqian, SONG Shuxiang, LIU Zhenyu, CEN Mingcan, JIANG Pinqun, CAI Chaobo. Research Progress of Successive Approximation Register Analog-to-Digital Converter[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(5): 24 -35 .
[8] ZHANG Shichao, LI Jiaye. Knowledge Matrix Representation[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(5): 36 -48 .
[9] LIANG Yuting, LUO Yuling, ZHANG Shunsheng. Review on Chaotic Image Encryption Based on Compressed Sensing[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(5): 49 -58 .
[10] HAO Yaru, DONG Li, XU Ke, LI Xianxian. Interpretability of Pre-trained Language Models: A Survey[J]. Journal of Guangxi Normal University(Natural Science Edition), 2022, 40(5): 59 -71 .
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