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Road impact in a protected area with rich biodiversity: the case of the Sebitoli road in Kibale National Park, Uganda

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Abstract

While road network expansion is crucial for economic development, it can cause a notable disturbance of fauna, especially in protected area in terms of habitat fragmentation, risk of collision, and also indirect threat such as pollution. In this study, we monitored the 4.6-km long tarmac road crossing the Kibale National Park in Uganda, home to a rich variety of wild species including the endangered chimpanzees. We evaluated the effects of collisions and pollution, as well as the impact of the renovation process in terms of disturbance and the mitigation measures deployed. This survey reports the death of 24 wild animals killed by cars, including two chimpanzees. The atmospheric concentrations of O3, NO2, SO2, and BTEX did not exceed recommended limits. More than 5000 plastic bottles were collected along the road within 4 months, and for the first time, the presence of BPA and BPS was detected in the hairs of wild chimpanzees. The road bisecting the Kibale National Park poses a high danger in terms of traffic and an underestimated risk related to plastic pollution. Measures (signpost, speed bumps) should be urgently deployed to decrease the risk posed by the renovated road for emblematic species such as chimpanzees, which are crucial for tourism and economy in Uganda.

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References

  • Aguirre AA, Tabor GM (2004) Introduction: marine vertebrates as sentinels of marine ecosystem health. EcoHealth 1:236–238

    Google Scholar 

  • Airparif (2019) Air quality in the Paris region in 2018.

  • Almeida S, Raposo A, Almeida-González M, Carrascosa C (2018) Bisphenol A: food exposure and impact on human health. Compr Rev Food Sci Food Saf 17:1503–1517

    Google Scholar 

  • Annavarapu RN, Kathi S (2016) Cognitive disorders in children associated with urban vehicular emissions. Environ Pollut 208:74–78

    CAS  Google Scholar 

  • Barber JR, Crooks KR, Fristrup KM (2010) The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol 25:180–189

    Google Scholar 

  • Benítez-López A, Alkemade R, Verweij PA (2010) The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biol Conserv 143:1307–1316

    Google Scholar 

  • Bennett AF (1991) Roads, roadsides and wildlife conservation: a review. Nat Conserv 2:Role Corridors 99–117

    Google Scholar 

  • Bennett VJ (2017) Effects of road density and pattern on the conservation of species and biodiversity. Curr Landsc Ecol Rep 2:1–11

    Google Scholar 

  • Béranger R, Hardy EM, Dexet C, Guldner L, Zaros C, Nougadère A, Metten M-A, Chevrier C, Appenzeller BMR (2018) Multiple pesticide analysis in hair samples of pregnant French women: results from the ELFE national birth cohort. Environ Int 120:43–53

    Google Scholar 

  • Bernardino FS, Dalrymple GH (1992) Seasonal activity and road mortality of the snakes of the Pa-hay-okee wetlands of Everglades National Park. USA Biol Conserv 62:71–75

    Google Scholar 

  • Bignal KL, Ashmore MR, Headley AD, Stewart K, Weigert K (2007) Ecological impacts of air pollution from road transport on local vegetation. Appl Geochem 22:1265–1271

    CAS  Google Scholar 

  • Björnsdotter MK, de Boer J, Ballesteros-Gómez A (2017) Bisphenol A and replacements in thermal paper: a review. Chemosphere 182:691–706

    Google Scholar 

  • Bonde RK, Aguirre AA, Powell J (2004) Manatees as sentinels of marine ecosystem health: are they the 2000-pound canaries? EcoHealth 1:255–262

    Google Scholar 

  • Burger J, Gochfeld M (2004) Marine birds as sentinels of environmental pollution. EcoHealth 1:263–274

    Google Scholar 

  • Cantonwine DE, Hauser R, Meeker JD (2013) Bisphenol A and human reproductive health. Expert Rev Obstet Gynecol 8:329–335

    CAS  Google Scholar 

  • Cibot M, Bortolamiol S, Seguya A, Krief S (2015) Chimpanzees facing a dangerous situation: a high-traffic asphalted road in the Sebitoli area of Kibale National Park, Uganda. Am J Primatol 77:890–900

    Google Scholar 

  • Clemons GK, Garcia JF (1980a) Changes in thyroid function after short-term ozone exposure in rats. J Environ Pathol Toxicol 4:359–369

    CAS  Google Scholar 

  • Clemons GK, Garcia JF (1980b) Endocrine aspects of ozone exposure in rats. Arch Toxicol Suppl Arch Toxikol Suppl 4:301–304

    CAS  Google Scholar 

  • Clemons GK, Wei D (1984) Effect of short-term ozone exposure on exogenous thyroxine levels in thyroidectomized and hypophysectomized rats. Toxicol Appl Pharmacol 74:86–90

    CAS  Google Scholar 

  • Clevenger AP, Chruszcz B, Gunson KE (2003) Spatial patterns and factors influencing small vertebrate fauna road-kill aggregations. Biol Conserv 109:15–26

    Google Scholar 

  • Conseil départemental de l'Orne (2018) Le Trafic Routier dans l'Orne, Les données. Pôle infrastructures territoriales, Direction gestion des routes Bureau exploitation sécurité routière. https://www.orne.fr/sites/default/files/2019-11/brochure2018.pdf

  • Cooper JE, Kendig EL, Belcher SM (2011) Assessment of bisphenol A released from reusable plastic, aluminium and stainless steel water bottles. Chemosphere 85:943–947

    CAS  Google Scholar 

  • Crittenden PD, Read DJ (1978) The effects of air pollution on plant growth with special reference to sulphur dioxide. II Growth Studies with Lolium perenne L. New Phytol 80:49–62

    CAS  Google Scholar 

  • da Silva VP, Deffaci AC, Hartmann MT, Hartmann PA (2017) Birds around the road: effects of a road on a savannah bird community in Southern Brazil. Ornitol Neotropical 28:119–128

    Google Scholar 

  • Duca R-C, Hardy E, Salquèbre G, Appenzeller BMR (2014) Hair decontamination procedure prior to multi-class pesticide analysis. Drug Test Anal 6(Suppl 1):55–66

    CAS  Google Scholar 

  • Eckardt M, Simat TJ (2017) Bisphenol A and alternatives in thermal paper receipts - a German market analysis from 2015 to 2017. Chemosphere 186:1016–1025

    CAS  Google Scholar 

  • EEA (2019) Air quality in Europe 2019 report 10/2019.

  • Fernie KJ, Marteinson SC, Chen D, Palace V, Peters L, Soos C, Smits JEG (2019) Changes in thyroid function of nestling tree swallows (Tachycineta bicolor) in relation to polycyclic aromatic compounds and other environmental stressors in the Athabasca Oil Sands Region. Environ Res 169:464–475

    CAS  Google Scholar 

  • Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34

    CAS  Google Scholar 

  • Forman RTT (1995) Some general principles of landscape and regional ecology. Landsc Ecol 10:133–142

    Google Scholar 

  • Forman RTT, Reineking B, Hersperger AM (2002) Road traffic and nearby grassland bird patterns in a suburbanizing landscape. Environ Manag 29:782–800

    Google Scholar 

  • Fossi MC, Casini S, Caliani I, Panti C, Marsili L, Viarengo A, Giangreco R, Notarbartolo di Sciara G, Serena F, Ouerghi A, Depledge MH (2012) The role of large marine vertebrates in the assessment of the quality of pelagic marine ecosystems. Mar Environ Res 77:156–158

    CAS  Google Scholar 

  • Garriga N, Santos X, Montori A, Richter-Boix A, Franch M, Llorente GA (2012) Are protected areas truly protected? The impact of road traffic on vertebrate fauna. Biodivers Conserv 21:2761–2774

    Google Scholar 

  • Geens T, Aerts D, Berthot C, Bourguignon J-P, Goeyens L, Lecomte P, Maghuin-Rogister G, Pironnet A-M, Pussemier L, Scippo M-L, van Loco J, Covaci A (2012) A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol 50:3725–3740

    CAS  Google Scholar 

  • Goosem M, Marsh H (1997) Fragmentation of a small-mammal community by a powerline corridor through tropical rainforest. Wildl Res 24:613–629

    Google Scholar 

  • Gruzieva O, Merid SK, Gref A, Gajulapuri A, Lemonnier N, Ballereau S, Gigante B, Kere J, Auffray C, Melén E et al (2017) Exposure to traffic-related air pollution and serum inflammatory cytokines in children. Environ Health Perspect:125

  • Guida M, Troisi J, Ciccone C, Granozio G, Cosimato C, Sardo ADS, Ferrara C, Guida M, Nappi C, Zullo F, di Carlo C (2015) Bisphenol A and congenital developmental defects in humans. Mutat Res Mol Mech Mutagen 774:33–39

    CAS  Google Scholar 

  • Hansen CA, Barnett AG, Jalaludin BB, Morgan GG (2009) Ambient air pollution and birth defects in Brisbane, Australia. PLoS One 4:e5408

    Google Scholar 

  • Hardy EM, Duca RC, Salquebre G, Appenzeller BMR (2015) Multi-residue analysis of organic pollutants in hair and urine for matrices comparison. Forensic Sci Int 249:6–19

    CAS  Google Scholar 

  • Harris L, Scheck J (1991) From implications to applications: the dispersal corridor principle applied to the conservation of biological diversity. Nat Conserv:189–200

  • Hartmann PA, Hartmann MT, Martins M (2011) Snake road mortality in a protected area in the Atlantic Forest of southeastern Brazil. South Am J Herpetol 6:35–42

    Google Scholar 

  • Heagle AS, Body DE, Heck WW (1973) An open-top field chamber to assess the impact of air pollution on plants 1. J Environ Qual 2:365–368

    CAS  Google Scholar 

  • Hockings KJ, Anderson JR, Matsuzawa T (2006) Road crossing in chimpanzees: a risky business. Curr Biol CB 16:R668–R670

    CAS  Google Scholar 

  • Honour SL, Bell JNB, Ashenden TW, Cape JN, Power SA (2009) Responses of herbaceous plants to urban air pollution: effects on growth, phenology and leaf surface characteristics. Environ Pollut Barking Essex 1987 157:1279–1286

    CAS  Google Scholar 

  • Hwang B-F, Jaakkola JJK (2008) Ozone and other air pollutants and the risk of oral clefts. Environ Health Perspect 116:1411–1415

    CAS  Google Scholar 

  • Jaarsma CF, van Langevelde F, Botma H (2006) Flattened fauna and mitigation: traffic victims related to road, traffic, vehicle, and species characteristics. Transp Res Part Transp Environ 11:264–276

    Google Scholar 

  • Khreis H, Kelly C, Tate J, Parslow R, Lucas K, Nieuwenhuijsen M (2017) Exposure to traffic-related air pollution and risk of development of childhood asthma: a systematic review and meta-analysis. Environ Int 100:1–31

    CAS  Google Scholar 

  • Kinch CD, Ibhazehiebo K, Jeong J-H, Habibi HR, Kurrasch DM (2015) Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. Proc Natl Acad Sci 112:1475–1480

    CAS  Google Scholar 

  • Kirenga BJ, Meng Q, Van Gemert F, Aanyu-Tukamuhebwa H, Chavannes N, Katamba A, Obai G, der Molen TV, Schwander S, Mohsenin V (2015) The state of ambient air quality in two Ugandan cities: a pilot cross-sectional spatial assessment. Int J Environ Res Public Health 12:8075–8091

    CAS  Google Scholar 

  • Krief S, Berny P, Gumisiriza F, Gross R, Demeneix B, Fini JB, Chapman CA, Chapman LJ, Seguya A, Wasswa J (2017) Agricultural expansion as risk to endangered wildlife: pesticide exposure in wild chimpanzees and baboons displaying facial dysplasia. Sci Total Environ 598:647–656

    CAS  Google Scholar 

  • Laurance WF, Croes BM, Tchignoumba L, Lahm SA, Alonso A, Lee ME, Campbell P, Ondzeano C (2006) Impacts of roads and hunting on central African rainforest mammals. Conserv Biol 20:1251–1261

    Google Scholar 

  • Laurance WF, Campbell MJ, Alamgir M, Mahmoud MI (2017) Road expansion and the fate of Africa’s tropical forests. Front Ecol Evol 5

  • Lavers JL, Bond AL, Hutton I (2014) Plastic ingestion by flesh-footed shearwaters (Puffinus carneipes): implications for fledgling body condition and the accumulation of plastic-derived chemicals. Environ Pollut 187:124–129

    CAS  Google Scholar 

  • Le HH, Carlson EM, Chua JP, Belcher SM (2008) Bisphenol A is released from polycarbonate drinking bottles and mimics the neurotoxic actions of estrogen in developing cerebellar neurons. Toxicol Lett 176:149–156

    CAS  Google Scholar 

  • Liao C, Kannan K (2014) A survey of bisphenol A and other bisphenol analogues in foodstuffs from nine cities in China. Food Addit Contam Part Chem Anal Control Expo Risk Assess 31:319–329

    CAS  Google Scholar 

  • Liao C, Liu F, Alomirah H, Loi VD, Mohd MA, Moon H-B, Nakata H, Kannan K (2012) Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ Sci Technol 46:6860–6866

    CAS  Google Scholar 

  • Liu J, Dinu I, Martin LJ, Field C, Dewey D, Martin JW, Team, T.Ap.S (2018) Prenatal exposure to bisphenol A and bisphenol S and neurodevelopment in children at 2 years of age. ISEE Conf Abstr

  • Lu L, Zhan T, Ma M, Xu C, Wang J, Zhang C, Liu W, Zhuang S (2018) Thyroid disruption by bisphenol S analogues via thyroid hormone receptor β: in vitro, in vivo, and molecular dynamics simulation study. Environ Sci Technol 52:6617–6625

    CAS  Google Scholar 

  • Mader H-J (1984) Animal habitat isolation by roads and agricultural fields. Biol Conserv 29:81–96

    Google Scholar 

  • Malo JE, Suárez F, Díez A (2004) Can we mitigate animal–vehicle accidents using predictive models? J Appl Ecol 41:701–710

    Google Scholar 

  • Markiewicz A, Björklund K, Eriksson E, Kalmykova Y, Strömvall A-M, Siopi A (2017) Emissions of organic pollutants from traffic and roads: priority pollutants selection and substance flow analysis. Sci Total Environ 580:1162–1174

    CAS  Google Scholar 

  • McLennan MR, Asiimwe C (2016) Cars kill chimpanzees: case report of a wild chimpanzee killed on a road at Bulindi. Uganda Primates J Primatol 57:377–388

    Google Scholar 

  • Mkanda FX, Chansa W (2011) Changes in temporal and spatial pattern of road kills along the Lusaka-Mongu (M9) Highway, Kafue National Park. Zambia Afr J Wildl Res 41:68–78

    Google Scholar 

  • Moon MK (2019) Concern about the safety of bisphenol A substitutes. Diabetes Metab J 43:46–48

    Google Scholar 

  • Morgan D, Sanz C (2007) Best practice guidelines for reducing the impact of commercial logging on great apes in Western Equatorial Africa. Occas Pap IUCN Species Surviv Comm IUCN Eng No 34

  • North, M.A., Rodriguez-Estival, J., and Smits, J.E.G. (2017). Biomarker sensitivity to vehicle exhaust in experimentally exposed European starlings

    Google Scholar 

  • Olgun H, Mohammed MK, Mzee AJ, Green MEL, Davenport TRB, Georgiev AV (2020) The impact and implications of vehicle collisions on the endangered and endemic Zanzibar red colobus (Piliocolobus kirkii). BioRxiv 2020(01):17.906909

    Google Scholar 

  • Palazzi P, Mezzache S, Bourokba N, Hardy EM, Schritz A, Bastien P, Emond C, Li J, Soeur J, Appenzeller BMR (2018) Exposure to polycyclic aromatic hydrocarbons in women living in the Chinese cities of BaoDing and Dalian revealed by hair analysis. Environ Int 121:1341–1354

    CAS  Google Scholar 

  • Palazzi P, Hardy EM, Appenzeller BMR (2019) Biomonitoring of children exposure to urban pollution and environmental tobacco smoke with hair analysis – a pilot study on children living in Paris and Yeu Island, France. Sci Total Environ 665:864–872

    CAS  Google Scholar 

  • Panti C, Baini M, Lusher A, Hernandez-Milan G, Bravo Rebolledo EL, Unger B, Syberg K, Simmonds MP, Fossi MC (2019) Marine litter: one of the major threats for marine mammals. Outcomes from the European Cetacean Society workshop. Environ Pollut 247:72–79

    CAS  Google Scholar 

  • Peres CP, Lake IR (2003) Extent of nontimber resource extraction in tropical forests: accessibility to game vertebrates by hunters in the Amazon Basin. Conserv Biol 17:521–535

    Google Scholar 

  • Pivnenko K, Pedersen GA, Eriksson E, Astrup TF (2015) Bisphenol A and its structural analogues in household waste paper. Waste Manag 44:39–47

    CAS  Google Scholar 

  • Rai PK (2010) Heavy metal pollution in lentic ecosystem of sub-tropical industrial region and its phytoremediation. Int J Phytoremediation 12:226–242

    Google Scholar 

  • Rai A, Kulshreshtha K, Srivastava PK, Mohanty CS (2010) Leaf surface structure alterations due to particulate pollution in some common plants. Environmentalist 30:18–23

    Google Scholar 

  • Ramakrishnan A, Lupo PJ, Agopian AJ, Linder SH, Stock TH, Langlois PH, Craft E (2013) Evaluating the effects of maternal exposure to benzene, toluene, ethyl benzene, and xylene on oral clefts among offspring in Texas: 1999–2008. Birt Defects Res A Clin Mol Teratol 97:532–537

    CAS  Google Scholar 

  • Rao A, Ahmed MK, Taub PJ, Mamoun JS (2016) The correlation between maternal exposure to air pollution and the risk of orofacial clefts in infants: a systematic review and meta-analysis. J Oral Maxillofac Res 7:e2

    Google Scholar 

  • Rebolj D, Sturm PJ (1999) A GIS based component-oriented integrated system for estimation, visualization and analysis of road traffic air pollution. Environ Model Softw 14:531–539

    Google Scholar 

  • Reijnen R, Foppen R, Braak CT, Thissen J (1995) The effects of car traffic on breeding bird populations in woodland. III. Reduction of Density in Relation to the Proximity of Main Roads. J Appl Ecol 32:187–202

    Google Scholar 

  • Reijnen R, Foppen R, Meeuwsen H (1996) The effects of traffic on the density of breeding birds in Dutch agricultural grasslands. Biol Conserv 75:255–260

    Google Scholar 

  • Reijnen R, Foppen R, Veenbaas G (1997) Disturbance by traffic of breeding birds: evaluation of the effect and considerations in planning and managing road corridors. Biodivers Conserv 6:567–581

    Google Scholar 

  • Rico A, Kindlmann P, Sedláček F (2009) Can the barrier effect of highways cause genetic subdivision in small mammals? Acta Theriol (Warsz) 54:297–310

    Google Scholar 

  • Rico A, Kindlmann P, Sedláček F (2017) Barrier effects of roads on movements of small mammals. Folia Zool 56(1):1–12

    Google Scholar 

  • Rivas-Arancibia S, Guevara-Guzmán R, López-Vidal Y, Rodríguez-Martínez E, Zanardo-Gomes M, Angoa-Pérez M, Raisman-Vozari R (2010) Oxidative stress caused by ozone exposure induces loss of brain repair in the hippocampus of adult rats. Toxicol Sci Off J Soc Toxicol 113:187–197

    CAS  Google Scholar 

  • Robinson JG, Bodmer RE (1999) Towards wildlife management in tropical forests. J Wildl Manag 63:1–13

    Google Scholar 

  • Rochester JR (2013) Bisphenol A and human health: A review of the literature. Reprod Toxicol 42:132–155

    CAS  Google Scholar 

  • Rochester JR, Bolden AL (2015) Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect 123:643–650

    CAS  Google Scholar 

  • Rytwinski T, Fahrig L (2015) The impacts of roads and traffic on terrestrial animal populations. In: Handbook of Road Ecology. John Wiley & Sons, Ltd, pp 237–246

  • Rytwinski T, Soanes K, Jaeger JAG, Fahrig L, Findlay CS, Houlahan J, van der Ree R, van der Grift EA (2016) How effective is road mitigation at reducing road-kill? A meta-analysis. PLOS ONE 11:e0166941

    Google Scholar 

  • Schutt P (2008) Analysis of road kill data from Ankarafantsika National Park, Madagascar (Master thesis). Duke University, North Carolina, USA.

  • Selvan KM, Sridharan N, John S (2012) Roadkill animals on national highways of Karnataka. India J Ecol Nat Environ 4:363–365

    Google Scholar 

  • Spirhanzlova P, Fini J-B, Demeneix B, Lardy-Fontan S, Vaslin-Reimann S, Lalere B, Guma N, Tindall A, Krief S (2019) Composition and endocrine effects of water collected in the Kibale national park in Uganda. Environ Pollut 251:460–468

    CAS  Google Scholar 

  • Teuten EL, Saquing JM, Knappe DRU, Barlaz MA, Jonsson S, Björn A, Rowland SJ, Thompson RC, Galloway TS, Yamashita R, Ochi D, Watanuki Y, Moore C, Viet PH, Tana TS, Prudente M, Boonyatumanond R, Zakaria MP, Akkhavong K, Ogata Y, Hirai H, Iwasa S, Mizukawa K, Hagino Y, Imamura A, Saha M, Takada H (2009) Transport and release of chemicals from plastics to the environment and to wildlife. Philos Trans R Soc B Biol Sci 364:2027–2045

    CAS  Google Scholar 

  • Thompson RC, Moore CJ, vom Saal FS, Swan SH (2009) Plastics, the environment and human health: current consensus and future trends. Philos Trans R Soc B Biol Sci 364:2153–2166

    CAS  Google Scholar 

  • Ullah H, Jahan S, Ain QU, Shaheen G, Ahsan N (2016) Effect of bisphenol S exposure on male reproductive system of rats: A histological and biochemical study. Chemosphere 152:383–391

    CAS  Google Scholar 

  • van der Schalie WH, Gardner HS, Bantle JA, De Rosa CT, Finch RA, Reif JS, Reuter RH, Backer LC, Burger J, Folmar LC et al (1999) Animals as sentinels of human health hazards of environmental chemicals. Environ Health Perspect 107:309–315

    Google Scholar 

  • Vanjonack WJ, Johnson HD (1974) Effect of sulphur dioxide (SO2) and heat (35°C) stressors on plasma glucocorticoids and thyroxine levels in mice. Int J Biometeorol 18:301–305

    CAS  Google Scholar 

  • Volk HE, Lurmann F, Penfold B, Hertz-Picciotto I, McConnell R (2013) Traffic-related air pollution, particulate matter, and autism. JAMA Psychiatry 70:71–77

    Google Scholar 

  • Wang L, Xiang X, Mi B, Song H, Dong M, Zhang S, Bi Y, Zhao Y, Li Q, Zhang Q et al (2018a) Association between early prenatal exposure to ambient air pollution and birth defects: evidence from newborns in Xi’an, China. J Public Health Oxf Engl

  • Wang W, Zhang X, Wang Z, Qin J, Wang W, Tian H, Ru S (2018b) Bisphenol S induces obesogenic effects through deregulating lipid metabolism in zebrafish (Danio rerio) larvae. Chemosphere 199:286–296

    CAS  Google Scholar 

  • Wei P, Zhao F, Zhang X, Liu W, Jiang G, Wang H, Ru S (2018) Transgenerational thyroid endocrine disruption induced by bisphenol S affects the early development of zebrafish offspring. Environ Pollut Barking Essex 1987 243:800–808

    CAS  Google Scholar 

  • Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon H-B, Jeong Y, Kannan P, Achyuthan H, Munuswamy N, Kannan K (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotoxicol Environ Saf 122:565–572

    CAS  Google Scholar 

  • Yin N, Liang X, Liang S, Liang S, Yang R, Hu B, Cheng Z, Liu S, Dong H, Liu S, Faiola F (2019) Embryonic stem cell- and transcriptomics-based in vitro analyses reveal that bisphenols A, F and S have similar and very complex potential developmental toxicities. Ecotoxicol Environ Saf 176:330–338

    CAS  Google Scholar 

  • Zhao Y, Cao Z, Li H, Su X, Yang Y, Liu C, Hua J (2019) Air pollution exposure in association with maternal thyroid function during early pregnancy. J Hazard Mater 367:188–193

    CAS  Google Scholar 

  • Zhu Y, Zhang C, Liu D, Grantz KL, Wallace M, Mendola P (2015) Maternal ambient air pollution exposure preconception and during early gestation and offspring congenital orofacial defects. Environ Res 140:714–720

    CAS  Google Scholar 

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Acknowledgments

We would like to thank Uganda Wildlife Authority and Uganda National Council for Science and Technology for authorizing our research in the Kibale National Park, Uganda. We are thankful to Jean-Michel Krief, co-director of the Great Ape Conservation Project. We are very grateful to all field assistants of the Sebitoli Chimpanzee Project, namely, Emmanuel Balinda, Deogratius Kiomuhangi, Joseph Alinaitwe, Ibrahim Nyakana, Wilson Muzahura, Edward Kalyegira, and Sulaiti Tusabe. We offer our profound thanks to Daniela Zainabu Birungi, Robert Asimwe, and Robert Nyakahuma for their assistance for the plastic waste collection as well as Clovice Alikonyera, Charles Twesige, and Philip Musinguzi for the road patrols. We are grateful to Christophe Sutour and Tatiana Mace for their consultations and advice. We would also like to thank Dr. Nicole Kane-Maguire for critical reading of the manuscript.

Funding

Field trips, analysis, station, and team support in Sebitoli were granted by the Projet pour la Conservation des Grands Singes, Fondation Nicolas Hulot pour la Nature et l’Homme, Fondation de France, the Fondation Prince Albert II, and Fonds Français pour l’Environnement Mondial.

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Authors and Affiliations

  1. UMR 7206 CNRS/MNHN/P7, Eco-anthropologie, Hommes et Environnements, Muséum national d’Histoire naturelle, Musée de l’Homme, 17 place du Trocadéro, 75016, Paris, France

    Sabrina Krief & Petra Spirhanzlova

  2. Great Ape Conservation Project (GACP), Sebitoli Research Station, Kibale National Park, Fort Portal, Uganda

    Sabrina Krief, John Paul Okimat & Petra Spirhanzlova

  3. Department of Population Health, Luxembourg Institute of Health, 1A-B, rue Thomas Edison, L-1445 Strassen, Luxembourg, Luxembourg

    Alba Iglesias-González & Brice Marc René Appenzeller

  4. UMR 7221 Molecular Physiology of Adaptation, Museum national d’Histoire naturelle, 7 rue Cuvier, 75005, Paris, France

    Jean-Baptiste Fini & Barbara Demeneix

  5. Laboratoire de Métrologie et d’Essais, rue Gaston Boissier, 75724, Paris cedex 15, France

    Sophie Vaslin-Reimann, Sophie Lardy-Fontan & Petra Spirhanzlova

  6. Uganda Wildlife Authority, Kampala, Uganda

    Nelson Guma

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  1. Sabrina Krief
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  2. Alba Iglesias-González
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  3. Brice Marc René Appenzeller
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Correspondence to Sabrina Krief.

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Krief, S., Iglesias-González, A., Appenzeller, B.M.R. et al. Road impact in a protected area with rich biodiversity: the case of the Sebitoli road in Kibale National Park, Uganda. Environ Sci Pollut Res 27, 27914–27925 (2020). https://doi.org/10.1007/s11356-020-09098-0

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  • DOI: https://doi.org/10.1007/s11356-020-09098-0

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