Abstract
Agriculture expansion is a major cause of habitat loss and exposure to phytochemical pollution for non-human primates. In addition to endocrine disruption, exposure to pesticides may have other sublethal physiological consequences for animals, such as generation of oxidative damage to macromolecules. In this study, we analyzed the pesticides contained in the river water across the home range of wild chimpanzees (Pan troglodytes) in Sebitoli area located on the Northern part of Kibale National Park (Uganda). We tested whether levels of three urinary markers of oxidative damage vary among individuals in relation to their ranging patterns, as a proxy for pesticide exposure intensity. To better characterize the foraging habitat use, the trophic level, and the energetic status of study individuals, we also quantified urinary levels of carbon and nitrogen stable isotope signatures and of C-peptide. Among the 511 pesticides screened, 18 compounds including herbicides, insecticides, and fungicides were found in the water sampled in the Western part of the home range of chimpanzees. In this area, chimpanzees used to feed on maize crops. By contrast, in the Eastern part where crop feeding was never observed, we found only seven pesticides. According to their ranging patterns and thus crop feeding frequency, the 139 urine samples collected from 43 Sebitoli chimpanzees were categorized as belonging to low, medium, and high exposure level. Chimpanzees from the high exposure zone had higher oxidative DNA damage (8-OHdG) than chimpanzees from both the low and medium exposure groups, who had similar levels of oxidative DNA damage. In addition, individuals with higher C-peptide tended to have significantly higher oxidative DNA damage and lipid peroxides. The three exposure groups had similar levels of urinary 8-isoprostanes and of urinary lipid peroxides. These results were robust for any potential confounding effect of other variables because neither age category nor sex or isotope levels were significantly associated with markers of oxidative damage. Our study points to genotoxic effects as one potential sublethal consequence of ranging in proximity of agricultural fields owing to exposure to pesticides or other unidentified sources of stress. Given our phylogenetic proximity, this information is relevant for the conservation of this species which is endangered and also sentinel for human health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data could be communicated upon demands to the corresponding author.
References
Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaie A (2004). Pesticides and oxidative stress: a review. Medical Science Monitor: Int Med J Exp Clin Res 10(6): RA141–147. http://www.ncbi.nlm.nih.gov/pubmed/15173684 Accessed 10 Jan 2023
Amusa C, Rothman J, Odongo S, Matovu H, Ssebugere P, Baranga D, Sillanpää M (2021) The endangered African Great Ape: pesticide residues in soil and plants consumed by Mountain Gorillas (Gorilla beringei) in Bwindi Impenetrable National Park, East Africa. Sci Total Environ 758:143692. https://doi.org/10.1016/J.SCITOTENV.2020.143692
Belles A, Tapie N, Pardon P, Budzinski H (2014) Development of the performance reference compound approach for the calibration of “polar organic chemical integrative sampler” (POCIS). Anal Bioanal Chem 406(4):1131–1140. https://doi.org/10.1007/S00216-013-7297-Z/FIGURES/6
Berho C, Claude B, Coisy E, Togola A, Bayoudh S, Morin P, Amalric L (2017) Laboratory calibration of a POCIS-like sampler based on molecularly imprinted polymers for glyphosate and AMPA sampling in water. Anal Bioanal Chem 409(8):2029–2035. https://doi.org/10.1007/S00216-016-0150-4/METRICS
Bortolamiol S, Cohen M, Potts K, Pennec F, Rwaburindore P, Kasenene J, Seguya A, Vignaud Q, Krief S (2014) Suitable habitats for endangered frugivorous mammals: small-scale comparison, regeneration forest and chimpanzee density in Kibale National Park. Uganda PLOS ONE 9(7):e102177. https://doi.org/10.1371/JOURNAL.PONE.0102177
Bush ER, Whytock RC, Bahaa-El-din L, Bourgeois S, Bunnefeld N, Cardoso AW, Dikangadissi JT, Dimbonda P, Dimoto E, Ndong JE, Jeffery KJ, Lehmann D, Makaga L, Momboua B, Momont LRW, Tutin CEG, White LJT, Whittaker A, Abernethy K (2020) Long-term collapse in fruit availability threatens Central African forest megafauna. Science 370(6521):1219–1222. https://doi.org/10.1126/SCIENCE.ABC7791/SUPPL_FILE/ABC7791_BUSH_SM.PDF
Carlitz EHD, Miller R, Kirschbaum C, Gao W, Hänni DC, Van Schaik CP (2016) Measuring hair cortisol concentrations to assess the effect of anthropogenic impacts on wild chimpanzees (Pan troglodytes). PLoS ONE 11(4):e0151870. https://doi.org/10.1371/JOURNAL.PONE.0151870
Chapman CA, Lambert JE (2000) Habitat alteration and the conservation of African primates: case study of Kibale National Park. Uganda Am J Primatol 50(3):169–185. https://doi.org/10.1002/(SICI)1098-2345(200003)50:3%3c169::AID-AJP1%3e3.0.CO;2-P
Chapman CA, Chapman LJ, Struhsaker TT, Zanne AE, Clark CJ, Poulsen JR (2005) A long-term evaluation of fruiting phenology: importance of climate change. J Trop Ecol 21(1):31–45. https://doi.org/10.1017/S0266467404001993
Chiyo PI, Cochrane EP, Naughton L, Basuta GI (2005) Temporal patterns of crop raiding by elephants: a response to changes in forage quality or crop availability? Afr J Ecol 43(1):48–55. https://doi.org/10.1111/J.1365-2028.2004.00544.X
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(8):890–900. https://doi.org/10.1002/AJP.22417
Costantini D (2015) Land-use changes and agriculture in the tropics: pesticides as an overlooked threat to wildlife. Biodivers Conserv 24(7):1837–1839. https://doi.org/10.1007/S10531-015-0878-8/METRICS
Couturier C, Bortolamiol S, Ortmann S, Okimat JP, Asalu E, Krief S (2022) All-you-can-eat: influence of proximity to maize gardens on the wild diet and the forest activities of the Sebitoli chimpanzee community in Kibale National Park. Animals 12(7):806. https://doi.org/10.3390/ani12070806
Deniro MJ, Epstein S (1981a) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Deniro MJ, Epstein S (1981b) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
Estrada A (2013) Socioeconomic contexts of primate conservation: population, poverty, global economic demands, and sustainable land use. Am J Primatol 75(1):30–45. https://doi.org/10.1002/AJP.22080
Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Fiore A, Di Anne-Isola Nekaris K, Nijman V, Heymann EW, Lambert JE, Rovero F, Barelli C, Setchell JM, Gillespie TR, Mittermeier RA, Arregoitia LV, de Guinea M, Gouveia S, Dobrovolski R,… Li B (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3(1), e1600946. https://doi.org/10.1126/SCIADV.1600946
Girard-Buttoz C, Higham JP, Heistermann M, Wedegärtner S, Maestripieri D, Engelhardt A (2011) Urinary C-peptide measurement as a marker of nutritional status in macaques. PLoS ONE 6(3):18042. https://doi.org/10.1371/JOURNAL.PONE.0018042
González NT, Otali E, Machanda Z, Muller MN, Wrangham R, Thompson ME (2020) Urinary markers of oxidative stress respond to infection and late-life in wild chimpanzees. PLoS ONE 15(9):e0238066. https://doi.org/10.1371/JOURNAL.PONE.0238066
Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine. Free Radicals Biol Med. https://doi.org/10.1093/ACPROF:OSO/9780198717478.001.0001
Higham JP, Girard-Buttoz C, Engelhardt A, Heistermann M (2011) Urinary C-peptide of insulin as a non-invasive marker of nutritional status: some practicalities. PLoS ONE 6(7):e22398. https://doi.org/10.1371/JOURNAL.PONE.0022398
Hockings K, Humley T (2009) Best practice guidelines for the prevention and mitigation of conflict between humans and great apes. Best Pract Guidelines Prev Mitig Conflict between Humans Great Apes. https://doi.org/10.2305/IUCN.CH.2009.SSC-OP.37.EN
Hockings KJ, Humle T, Anderson JR, Biro D, Sousa C, Ohashi G, Matsuzawa T (2007) Chimpanzees Share Forbidden Fruit. PLOS ONE 2(9):e886. https://doi.org/10.1371/JOURNAL.PONE.0000886
Hyeroba D, Apell P, Otali E (2011) Managing a speared alpha male chimpanzee. The Veterinary Record 169(25):658. https://doi.org/10.1136/VR.D4680
IUCN (2023) IUCN Red List of Threatened Species. https://www.iucnredlist.org/ Accessed 10 Jan 2023
Krief S, Hladik CM, Haxaire C (2005) Ethnomedicinal and bioactive properties of plants ingested by wild chimpanzees in Uganda. J Ethnopharmacol 101(1–3):1–15. https://doi.org/10.1016/J.JEP.2005.03.024
Krief S, Cibot M, Bortolamiol S, Seguya A, Krief JM, Masi S (2014a) Wild chimpanzees on the edge: nocturnal activities in croplands. PLoS ONE 9(10):e109925. https://doi.org/10.1371/JOURNAL.PONE.0109925
Krief S, Krief JM, Seguya A, Couly G, Levi G (2014b) Facial dysplasia in wild chimpanzees. J Med Primatol 43(4):280–283. https://doi.org/10.1111/JMP.12129
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. https://doi.org/10.1016/J.SCITOTENV.2017.04.113
Krief S, Watts DP, Mitani JC, Krief JM, Cibot M, Bortolamiol S, Seguya AG, Couly G (2018) Two cases of cleft lip and other congenital anomalies in wild chimpanzees living in Kibale National Park. Uganda. https://doi.org/10.1597/14-188,52(6),743-750.10.1597/14-188
Krief S, Iglesias-González A, Appenzeller BMR, Okimat JP, Fini JB, Demeneix B, Vaslin-Reimann S, Lardy-Fontan S, Guma N, Spirhanzlova P (2020) 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(22):27914–27925. https://doi.org/10.1007/S11356-020-09098-0/METRICS
Krief S, Iglesias-González A, Appenzeller BMR, Rachid L, Beltrame M, Asalu E, Okimat JP, Kane-Maguire N, Spirhanzlova P (2022) Chimpanzee exposure to pollution revealed by human biomonitoring approaches. Ecotoxicol Environ Saf 233:113341. https://doi.org/10.1016/J.ECOENV.2022.113341
Ledda C, Cannizzaro E, Cinà D, Filetti V, Vitale E, Paravizzini G, Di Naso C, Iavicoli I, Rapisarda V (2021) Oxidative stress and DNA damage in agricultural workers after exposure to pesticides. J Occup Med Toxicol 16(1):1–7. https://doi.org/10.1186/S12995-020-00290-Z/FIGURES/1
Martinez-Moral MP, Kannan K (2019) How stable is oxidative stress level? An observational study of intra- and inter-individual variability in urinary oxidative stress biomarkers of DNA, proteins, and lipids in healthy individuals. Environ Int 123:382–389. https://doi.org/10.1016/J.ENVINT.2018.12.009
Masi S, Chauffour S, Bain O, Todd A, Guillot J, Krief S (2012) Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS ONE 7(12):e49805. https://doi.org/10.1371/JOURNAL.PONE.0049805
Matthiessen P, Wheeler JR, Weltje L (2017) A Review of the Evidence for Endocrine Disrupting Effects of Current-Use Chemicals on Wildlife Populations 48(3),195-216.10(1080/10408444),pp.1397099
McLennan MR, Ganzhorn JU (2017) Nutritional characteristics of wild and cultivated foods for chimpanzees (Pan troglodytes) in agricultural landscapes. Int J Primatol 38(2):122–150. https://doi.org/10.1007/S10764-016-9940-Y/TABLES/4
Mendenhall CD, Karp DS, Meyer CFJ, Hadly EA, Daily GC (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509(7499):213–217
Mitani JC, Watts DP (2005) Correlates of territorial boundary patrol behaviour in wild chimpanzees. Anim Behav 70(5):1079–1086. https://doi.org/10.1016/J.ANBEHAV.2005.02.012
Naughton-Treves L, Treves A, Chapman C, Wrangham R (1998) Temporal patterns of crop-raiding by primates: linking food availability in croplands and adjacent forest. J Appl Ecol 35(4):596–606. https://doi.org/10.1046/J.1365-2664.1998.3540596.X
Ordaz-Németh I, Sop T, Amarasekaran B, Bachmann M, Boesch C, Brncic T, Caillaud D, Campbell G, Carvalho J, Chancellor R, Davenport TRB, Dowd D, Eno-Nku M, Ganas-Swaray J, Granier N, Greengrass E, Heinicke S, Herbinger I, Inkamba-Nkulu C, Kühl HS (2021) Range-wide indicators of African great ape density distribution. American Journal of Primatology 83(12):23338. https://doi.org/10.1002/AJP.23338
Schoeninger MJ, Moore J, Sept JM (1999) Subsistence strategies of two “savanna” chimpanzee populations: the stable isotope evidence. Am J Primatol 49:297–314. https://doi.org/10.1002/(SICI)1098-2345(199912)49:4
Spirhanzlova P, Fini JB, 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. Environmental Pollution (Barking, Essex : 1987)251, 460–468. https://doi.org/10.1016/J.ENVPOL.2019.05.006
Sponheimer M, Loudon JE, Codron D, Howells ME, Pruetz JD, Codron J, de Ruiter DJ, Lee-Thorp JA (2006) Do “savanna” chimpanzees consume C4 resources? J Hum Evol 51(2):128–133. https://doi.org/10.1016/J.JHEVOL.2006.02.002
Struhsaker TT (1997) Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. Ecol Afr Rain Forest: Logging Kibale Conflict between Conserv Exploitation 52(1):87–87. https://doi.org/10.1007/BF02861299/METRICS
Thompson ME, Wrangham RW (2006) Comparison of sex differences in gregariousness in fission-fusion species. Primates of Western Uganda, 209–226, New York, NY: Springer New York. https://doi.org/10.1007/978-0-387-33505-6_12
Thompson ME, Muller MN, Wrangham RW, Lwanga JS, Potts KB (2009) Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55(2):299–305
Thompson DA, Lehmler HJ, Kolpin DW, Hladik ML, Vargo JD, Schilling KE, Lefevre GH, Peeples TL, Poch MC, Laduca LE, Cwiertny DM, Field RW (2020) A critical review on the potential impacts of neonicotinoid insecticide use: current knowledge of environmental fate, toxicity, and implications for human health. Environ Sci Process Impacts 22(6):1315–1346. https://doi.org/10.1039/C9EM00586B
Van Der Schalie WH, Gardner HS, Bantle JA, De Rosa CT, Finch RA, Reif JS, Reuter RH, Backer LC, Burger J, Folmar LC, Stokes WS (1999) Animals as sentinels of human health hazards of environmental chemicals. Environ Health Perspect 107(4):309–315. https://doi.org/10.1289/EHP.99107309
Voigt CC, Kelm DH (2006) Host preference of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. J Mammal 87:1–6
Wang X, Anadón A, Wu Q, Qiao F, Ares I, Martínez-Larrañaga MR, Yuan Z, Martínez MA (2018). Mechanism of neonicotinoid toxicity: impact on oxidative stress and metabolism. 58: 471–507 https://doi.org/10.1146/ANNUREV-PHARMTOX-010617-052429
Watts DP, Mitani JC (2001). Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138(3):299–327. https://www.jstor.org/stable/4535825 Accessed 10 Jan 2023
Williams JM, Pusey AE, Carlis JV, Farm BP, Goodall J (2002) Female competition and male territorial behaviour influence female chimpanzees’ ranging patterns. Anim Behav 63(2):347–360. https://doi.org/10.1006/ANBE.2001.1916
Williamson EA, Macfie EJ (2014) Guidelines for best practice in great ape tourism. Primate Tourism 292–310, Cambridge University Press: Cambridge University Press. https://doi.org/10.1017/CBO9781139087407.022
Acknowledgements
We are grateful to the Uganda Wildlife Authority, Uganda National Council for Science and Technology for permission to conduct research at Sebitoli in Kibale NP, Uganda. We are grateful to Jean-Michel Krief, co-director of Great Ape Conservation Project, the managers and the field assistants of the Sebitoli Chimpanzee Project for their contribution to the long-term research: Harold Rugonge, Deogratius Kiomuhangi, Emmanuel Balinda, Joseph Alinaitwe, Ibrahim Nyakana, Wilson Muzahura, Edward Kalyegira, Nelson Tugume, Robert Asiimwe, Robert Nyakahuma, and Daniela Birungi. We are very grateful to Sophie Vaslin-Reiman, Sophie Lardy-Fontan, and the LNE for their collaboration to the water chemical analysis. We also thank Gaël Guillou from the Plateforme Analyses Isotopiques of the LIENSs laboratory for running stable isotope analyses. Thanks are due to the CPER (Contrat de Projet Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for funding the IRMS of LIENSs laboratory.
Funding
Field trip, data collection and analysis, station maintenance, and team support for the long-term research conducted in Sebitoli were granted by the Projet pour la Conservation des Grands Singes, Fondation pour la Nature et l’Homme, Fondation Prince Albert II de Monaco, and Fonds Français pour l’Environnement Mondial. The research related to oxidative stress was funded by the Centre National de la Recherche Scientifique AAP MITI 2020–2021 Ecologie de la santé to DC.
Author information
Authors and Affiliations
Contributions
Conception and design of the study were performed by Shelly Masi, David Costantini, Sabrina Krief, Petra Spirhanzlova, and Chloé Couturier. Coordination for the data acquisition, administration, and authorization were done by Eric Okwir and Edward Asalu. Data and sample collection were performed by Sabrina Krief and Chloé Couturier. Experiments and analyses were performed by David Costantini and Paco Bustamante. Interpretation of data and draft of the manuscript were done by Sabrina Krief, David Costantini, and Shelly Masi. Chloé Couturier, Eric Okwir, and Paco Bustamante reviewed, commented, and edited on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
Sebitoli chimpanzees are monitored without employing invasive methods and without any interactions with SCP team. SCP adhered and followed the guidelines of the Uganda Wildlife Authority (UWA). The SCP research is conducted in the context of the Memorandum of Understanding MNHN/UWA/Makerere University SJ 445–12.
Consent to participate
NA.
Consent for publication
NA.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Krief, S., Spirhanzlova, P., Masi, S. et al. High urinary oxidative DNA damage in wild chimpanzees ranging in proximity of agricultural fields in Sebitoli area, Uganda. Environ Sci Pollut Res 30, 110600–110611 (2023). https://doi.org/10.1007/s11356-023-30187-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-30187-3