First assessment of persistent organic pollutants in the Greater rhea (Rhea americana), a near-threatened flightless herbivorous bird of the Pampas grasslands
[en] Persistent Organic Pollutants (POPs) are still globally distributed and can exert different effects on ecosystems. Little is known about the occurrence of these contaminants in terrestrial birds from South America. In this study, POPs were assessed for the first time in a flightless herbivorous species from the Pampas grasslands, the Greater rhea (Rhea americana). Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs), were determined in 18 samples of feathers from free-ranging and captive individuals inhabiting four sites with different land use in central Argentina. Among the 16 POPs tested in those feathers, 6 PCBs (28, 52, 101, 138, 153 and 180) and 8 OCPs (α-HCH, β-HCH, γ-HCH, p,p'-DDE, p,p'-DDD, o,p'-DDT, p,p'-DDT and HCB) were quantified. No PBDEs were detected. Total concentration of POPs was higher in populations living in an intensive crop production area (Agriculture: 159 ng.g-1 and Farm: 97.53 ng.g-1) compared to the population in an urban area (Zoo: 45.86 ng/g) and an agroecosystem with extensive rearing of livestock (Cattle rearing: 36.77 ng.g-1). PCBs were the most abundant pollutants in all the populations studied. Lower chlorinated CB 52 and CB 101 were the principal PCB congeners detected, representing at least 70% of the total quantified. All populations studied showed a DDE + DDD / DDT ratio > 1, indicating a historical application of this insecticide. This study provides a new contribution to the scarce data on POP concentrations in South American bird species. Further investigations are needed to evaluate their potential effects on the health individuals and populations.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
Lèche, Alvina; Instituto de Diversidad y Ecología Animal (IDEA) - CONICET - Argentina
Gismondi, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Martella, Monica; Instituto de Diversidad y Ecología Animal (IDEA) - CONICET - Argentina
Navarro, Joaquin; Instituto de Diversidad y Ecología Animal (IDEA) - CONICET - Argentina
Language :
English
Title :
First assessment of persistent organic pollutants in the Greater rhea (Rhea americana), a near-threatened flightless herbivorous bird of the Pampas grasslands
Abbasi NA, Eulaers I, Jaspers VLB, Chaudhry MJI, Frantz A, Ambus PL, Covaci A, Malik RN (2016) Use of feathers to assess polychlorinated biphenyl and organochlorine pesticide exposure in top predatory bird species of Pakistan. Sci Total Environ 569-570:1408–1417. 10.1016/j.scitotenv.2016.06.224 DOI: 10.1016/j.scitotenv.2016.06.224
Alharbi OM, Basheer AA, Khattab RA, Ali I (2018) Health and environmental effects of persistent organic pollutants. J Mol Liq 263:442–453. 10.1016/j.molliq.2018.05.029 DOI: 10.1016/j.molliq.2018.05.029
Adrogué AQ, Miglioranza KS, Copello S, Favero M, Seco Pon JC (2019) Pelagic seabirds as biomonitors of persistent organic pollutants in the Southwestern Atlantic. Mar Pollut Bull 149:110516. 10.1016/j.marpolbul.2019.110516 DOI: 10.1016/j.marpolbul.2019.110516
Aver GF, Espín S, De Boni Dal Corno R, García-Fernández AJ, Petry MV (2020) Organochlorine pesticides in feathers of three raptor species in southern Brazil. Environ Sci Pollut Res 27:5971–5980. 10.1007/s11356-019-07370-6 DOI: 10.1007/s11356-019-07370-6
Ballesteros ML, Miglioranza KSB, Gonzalez M, Fillmann G, Wunderlin DA, Bistoni MA (2014) Multimatrix measurement of persistent organic pollutants in Mar Chiquita, a continental saline shallow lake. Sci Total Environ 490:73–80. 10.1016/j.scitotenv.2014.04.114 DOI: 10.1016/j.scitotenv.2014.04.114
Barletta M, Lima ARA, Costa MF (2019) Distribution, sources and consequences of nutrients, persistent organic pollutants, metals and microplastics in South American estuaries. Sci Total Environ 651:1199–1218. 10.1016/j.scitotenv.2018.09.276 DOI: 10.1016/j.scitotenv.2018.09.276
Bazzano G, Giordano PF, Navarro JL, Martella MB (2014) Linking landscape data with population viability analysis for evaluating translocations as a conservation strategy for Greater Rhea (Rhea americana) in central Argentina. Ornitol Neotropical 25:25–34
Behrooz RD, Esmaili-Sari A, Ghasempouri SM, Bahramifar N, Covaci A (2009) Organochlorine pesticide and polychlorinated biphenyl residues in feathers of birds from different trophic levels of South-West Iran. Environ Int 35(2):285–290. 10.1016/j.envint.2008.07.001 DOI: 10.1016/j.envint.2008.07.001
Bellis LM, Martella MB, Navarro JL, Vignolo PE (2004) Home range of greater and lesser rhea in Argentina: relevance to conservation. Biodivers Conserv 13:2589–2598. 10.1007/s10531-004-1086-0 DOI: 10.1007/s10531-004-1086-0
BirdLife International (2020) Species factsheet: Rhea americana. Downloaded from http://www.birdlife.org on 27/08/2020
Blus LJ, Henny CJ, Krynitsky AJ (1985) The effects of heptachlor and lindane on birds, Columbia Basin, Oregon and Washington DC, 1976–1981. Sci Total Environ 46:73–81. 10.1016/0048-9697(85)90284-0 DOI: 10.1016/0048-9697(85)90284-0
Bustnes JO, Tveraa T, Varpe Ø, Henden JA, Skaare JU (2007) Reproductive performance and organochlorine pollutants in an Antarctic marine top predator: the south polar skua. Environ Int 33(7):911–918. 10.1016/j.envint.2007.04.010 DOI: 10.1016/j.envint.2007.04.010
Commendatore M, Yorio P, Scenna L, Ondarza PM, Suárez N, Marinao C, Miglioranza KS (2018) Persistent organic pollutants in sediments, intertidal crabs, and the threatened Olrog’s gull in a northern Patagonia salt marsh. Argentina Mar Pollut Bull 136:533–546. 10.1016/j.marpolbul.2018.09.010 DOI: 10.1016/j.marpolbul.2018.09.010
Dauwe T, Jaspers V, Covaci A, Schepens P, Eens M (2005) Feathers as a nondestructive biomonitor for persistent organic pollutants. Environ Toxicol Chem 24(2):442–449. 10.1897/03-596.1 DOI: 10.1897/03-596.1
Davies SJJF (2003) Rheas. In: Hutchins M (ed) Grzimek’s animal life encyclopedia, Second Edition, Volume 8: Birds I. Farmington Hills, Detroit, Gale, pp 69–73
Díaz-Zorita M, Duarte GA, Grove JH (2002) A review of no-till systems and soil management for sustainable crop production in the subhumid and semiarid Pampas of Argentina. Soil Tillage Res 65:1–18 DOI: 10.1016/S0167-1987(01)00274-4
Dietz R, Letcher RJ, Desforges JP, Eulaers I, Sonne C, Vikingsson G (2019) Current state of knowledge on biological effects from contaminants on arctic wildlife and fish. Sci Total Environ 696:133792. 10.1016/j.scitotenv.2019.133792 DOI: 10.1016/j.scitotenv.2019.133792
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2011) InfoStat. Statistical software. Retrieved from http://www.infostat.com.ar/
Espín S, Martínez-López E, María-Mójica P, García-Fernández AJ (2012) Razorbill (Alca torda) feathers as an alternative tool for evaluating exposure to organochlorine pesticides. Ecotoxicology. 21:183–190. 10.1007/s10646-011-0777-z DOI: 10.1007/s10646-011-0777-z
Espín S, García-Fernández AJ, Herzke D, Shore RF, Van Hattum B, Van den Brink NW (2016) Tracking pan-continental trends in environmental contamination using sentinel raptors - what types of samples should we use? Ecotoxicology. 25:777–801. 10.1007/s10646-016-1636-8 DOI: 10.1007/s10646-016-1636-8
Fyfe RW, Risebrough RW, Monk JG, Jarman WM, Anderson DW, Kiff LF, Lincer J, Nisbet ICT II, Walton BJ (1988) DDE, productivity, and eggshell thickness relationships in the genus Falco. In: Cade TJ, Enderson JH, Thelander CG, White CM (eds) Peregrine falcon populations, their management and recovery. The Peregrine Fund, Boise, pp 319–335
Giordano PF, Bellis L, Navarro JL, Martella MB (2008) Abundance and spatial distribution of Greater Rhea (Rhea americana) in two sites on the pampas grasslands with different land use. Bird Conserv Int 18:63–70. 10.1017/S0959270908000075 DOI: 10.1017/S0959270908000075
Gold B, Brunk G (1982) Metabolism of 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane and 1,1-dichloro-2,2,-bis(p-chlorophenyl)ethane in the mouse. Chem Biol Interact 41:327–339. 10.1016/0009-2797(82)90109-0 DOI: 10.1016/0009-2797(82)90109-0
Gómara B, González MJ, Baos R, Hiraldo F, Abad E, Rivera J, Jiménez B (2008) Unexpected high PCB and total DDT levels in the breeding population of red kite (Milvus milvus) from Doñana National Park, south-western Spain. Environ Int 34:73–78. 10.1016/j.envint.2007.07.002 DOI: 10.1016/j.envint.2007.07.002
Greichus YA, Call DJ, Ammann BM, Greichus A, Shave H (1975) Physiological effects of polychlorinated biphenyls or a combination of DDT, DDD, and DDE in penned white pelicans. Arch Environ Contam Toxicol 3(3):330–343 DOI: 10.1007/BF02220745
Hauzenberger I, Perthen-Palmisalo B, Herrmann R (2004) Reports on substances scheduled for re-assessments under the UNECE POPs Protocol, Technical Review Report on Lindane, Austria. https://www.unece.org/fileadmin/DAM/env/lrtap/TaskForce/popsxg/2000-2003/lindane.pdf
IUCN 2016. BirdLife International. Rhea americana. The IUCN Red List of Threatened Species 2016: e.T22678073A92754472. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22678073A92754472.en Accessed 03 July 2020
Jacob J, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (Eds.) Avian biology: volume VI. Academic Press, pp. 199–324. https://doi.org/10.1016/B978-0-12-249406-2.50013-7
Jaspers VLB, Covaci A, Voorspoels S, Dauwe T, Eens M, Schepens P (2006) Brominated flame retardants and organochlorine pollutants in aquatic and terrestrial predatory birds of Belgium: levels, patterns, tissue distribution and condition factors. Environ Pollut 139:340–352. 10.1016/j.envpol.2005.05.008 DOI: 10.1016/j.envpol.2005.05.008
Jaspers VLB, Voorspoels S, Covaci A, Lepoint G, Eens M (2007) Evaluation of the usefulness of bird feathers as a nondestructive biomonitoring tool for organic pollutants: a comparative and meta-analytical approach. Environ Int 33:328–337. 10.1016/j.envint.2006.11.011 DOI: 10.1016/j.envint.2006.11.011
Jaspers VLB, Rodriguez FS, Boertmann D, Sonne C, Dietz R, Rasmussen LM, Eens M, Covaci A (2011) Body feathers as a potential new biomonitoring tool in raptors: a study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla). Environ Int 37:1349–1356. 10.1016/j.envint.2011.06.004 DOI: 10.1016/j.envint.2011.06.004
Jaspers VLB, Megson D, O’Sullivan G (2014) POPs in the terrestrial environment. In: O’Sullivan G, Sandau C (eds) Environmental Forensics for Persistent Organic Pollutants. Elsevier, pp 291–356. https://doi.org/10.1016/B978-0-444-59424-2.00007-4
Kodavanti PRS, Loganathan BG (2017) Organohalogen Pollutants and Human Health. In: Quah SR, Cockerham WC (eds) The International Encyclopedia of Public Health, vol 5, 2nd edn. Academic Press, Oxford, pp 359–366. 10.1016/B978-0-12-803678-5.00318-0 DOI: 10.1016/B978-0-12-803678-5.00318-0
Larsson P, Okla L, Woin P (1990) Atmospheric transport of persistent pollutants governs uptake by holarctic terrestrial biota. Environ Sci Technol 24:1599–1601 DOI: 10.1021/es00080a023
Lèche A, Bazzano G, Hansen C, Navarro JL, Marin RH, Martella MB (2014) Stress in wild Greater Rhea populations Rhea americana: effects of agricultural activities on seasonal excreted glucocorticoid metabolite levels. J Ornithol 155:919–926. 10.1007/s10336-014-1074-4 DOI: 10.1007/s10336-014-1074-4
Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C, Verreault J, Vijayan MM, Gabrielsen GW (2010) Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 408(15):2995–3043. 10.1016/j.scitotenv.2009.10.038 DOI: 10.1016/j.scitotenv.2009.10.038
Lohmann R, Breivik K, Dachs J, Muir D (2007) Global fate of POPs: current and future research directions. Environ Pollut 150:150–165. 10.1016/j.envpol.2007.06.051 DOI: 10.1016/j.envpol.2007.06.051
Luek JL, Dickhut RM, Cochran MA, Falconer RL, Kylin H (2017) Persistent organic pollutants in the Atlantic and southern oceans and oceanic atmosphere. Sci Total Environ 583:64–71. 10.1016/j.scitotenv.2016.12.189 DOI: 10.1016/j.scitotenv.2016.12.189
Martella MB, Navarro JL, Gonnet JM, Monge SA (1996) Diet of greater Rheas in an agroecosystem of central Argentina. J Wildl Manag 60:586–592 DOI: 10.2307/3802076
Martella M, Navarro J (2006) Proyecto Ñandú. Manejo de Rhea americana y R. pennata en la Argentina. In: Bolkovic, M.L., Ramadori, D.E. (Eds.) Manejo de Fauna en Argentina: Proyectos de Uso Sustentable. Dirección de Fauna Silvestre—Secretaría de Ambiente y Desarrollo Sustentable, Buenos Aires, Argentina, pp. 39–50
Martínez-López E, Espín S, Barbar F, Lambertucci SA, Gómez-Ramírez P, García- Fernández AJ (2015) Contaminants in the southern tip of South America: analysis of organochlorine compounds in feathers of avian scavengers from Argentinean Patagonia. Ecotoxicol Environ Saf 115:83–92. 10.1016/j.ecoenv.2015.02.011
Miglioranza KS, Gonzalez M, Ondarza PM, Shimabukuro VM, Isla FI, Fillmann G, Aizpún JE, Moreno VJ (2013) Assessment of Argentinean Patagonia pollution: PBDEs, OCPs and PCBs in different matrices from the Río Negro basin. Sci Total Environ 452:275–285. 10.1016/j.scitotenv.2013.02.055 DOI: 10.1016/j.scitotenv.2013.02.055
Ministerio de Justicia y Derechos Humanos (2002) http://servicios.infoleg.gob.ar/ infoleg Internet/anexos/75000-79999/79677/norma.htm
Monclús L, Rubè B-C, De La Puente J, Lacorte S, Lopez-Bejar M (2018a) Influence of persistent organic pollutants on the endocrine stress response in free-living and captive red kites (Milvus milvus). Environ Pollut 242(Part A):329–337. 10.1016/j.envpol.2018.06.086 DOI: 10.1016/j.envpol.2018.06.086
Monclús L, Lopez-Bejar M, De la Puente J, Covaci A, Jaspers VL (2018b) First evaluation of the use of down feathers for monitoring persistent organic pollutants and organophosphate ester flame retardants: a pilot study using nestlings of the endangered cinereous vulture (Aegypius monachus). Environ Pollut 238:413–420. 10.1016/j.envpol.2018.03.065 DOI: 10.1016/j.envpol.2018.03.065
Naso B, Perrone D, Ferrante MC, Zaccaroni A, Lucisan A (2003) Persistent organochlorine pollutants in liver of birds of different trophic levels from coast area of Campania. Italy Arch Environ Contam Toxicol 45:407–414. 10.1007/S00244-003-2201-Z DOI: 10.1007/S00244-003-2201-Z
Navarro JL, Martella MB (2008) The relevance of captive breeding to conservation of native ratites in Argentina: an overview. Aust J Exp Agric 48(10):1302–1307. 10.1071/EA08155 DOI: 10.1071/EA08155
Navarro JL, Martella MB (2011) Ratite conservation: linking captive release and welfare. In: Glatz P, Lunam C, Malecki I (eds) The welfare of farmed ratites. Springer, New York, pp 237–258. 10.1007/978-3-642-19297-5_11 DOI: 10.1007/978-3-642-19297-5_11
Navarro JL, Lèche A, Della Costa NS, Vera Cortez M, Marin RH, Martella MB (2018) State of the art knowledge in adrenocortical and behavioral responses to environmental challenges in a threatened South American ratite: implications to in situ and ex situ conservation. Gen Comp Endocrinol 273:52–60. 10.1016/j.ygcen.2018.04.012 DOI: 10.1016/j.ygcen.2018.04.012
Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986. 10.1016/j.envint.2009.02.006 DOI: 10.1016/j.envint.2009.02.006
Ottinger MA, Carro T, Bohannon M, Baltos L, Marcell AM, McKernan M, Dean K, Lavoie E, Abdelnabi M (2013) Assessing effects of environmental chemicals on neuroendocrine systems: potential mechanisms and functional outcomes. Gen Comp Endocrinol 190:194–202. 10.1016/j.ygcen.2013.06.004 DOI: 10.1016/j.ygcen.2013.06.004
Reyna PB, Ballesteros ML, Albá ML, Bertrand L, González M, Miglioranza KSB, Tatián M, Hued AC (2019) A multilevel response approach reveals the Asian clam Corbicula largillierti as a mirror of aquatic pollution. Sci Total Environ 692:175–187. 10.1016/j.scitotenv.2019.07.194 DOI: 10.1016/j.scitotenv.2019.07.194
Rutkowska M, Płotka-Wasylka J, Lubinska-Szczygeł M, Różańska A, Możejko-Ciesielska J, Namieśnik J (2018) Birds’ feathers – suitable samples for determination of environmental pollutants. Trends Anal Chem 109:97–115. 10.1016/j.trac.2018.09.022 DOI: 10.1016/j.trac.2018.09.022
Schettgen T, Alt A, Esser A, Kraus T (2015) Current data on the background burden to the persistent organochlorine pollutants HCB, p,p′-DDE as well as PCB 138, PCB 153 and PCB 180 in plasma of the general population in Germany. Int J Hyg Environ Health 218:380–385. 10.1016/j.ijheh.2015.02.006 DOI: 10.1016/j.ijheh.2015.02.006
Sonne C, Siebert U, Gonnsen K, Desforges J-P, Eulaers I, Dietz R (2020) Health effects from contaminant exposure in Baltic Sea birds and marine mammals: a review. Environ Int 139:1–9. 10.1016/j.envint.2020.105725 DOI: 10.1016/j.envint.2020.105725
Tartu S, Angelier F, Herzke D, Moe B, Bech C, Gabrielsen GW (2014) The stress of being contaminated? Adrenocortical function and reproduction in relation to persistent organic pollutants in female black legged kittiwakes. Sci Total Environ 476–477:553–560. 10.1016/j.scitotenv.2014.01.060 DOI: 10.1016/j.scitotenv.2014.01.060
Vallack HW, Bakker DJ, Brandt I, Broström-Lundén E, Brouwer A, Bull KR, Gough C, Guardans R, Holoubek I, Jansson B, Koch R, Kuylenstierna J, Lecloux A, Mackay D, McCutcheon P, Mocarelli P, Taalman RDF (1998) Controlling persistent organic pollutants–what next? Environ Toxicol Pharmacol 6(3):143–175. 10.1016/S1382-6689(98)00036-2 DOI: 10.1016/S1382-6689(98)00036-2
Viglizzo EF, Frank FC, Carreño L (2005) Situación ambiental en las ecoregiones pampa y campos y malezales. In: Acerbi M, Corcuera J, Brown A, Martínez Ortiz U (eds) Situación ambiental Argentina. Fundación Vida Silvestre Argentina, Buenos Aires, pp 261–269
Voorspoels S, Covaci A, Maervoet J, Schepens P (2002) Relationship between age and levels of organochlorine contaminants in human serum of a Belgian population. Bull Environ Contam Toxicol 69:22–29. 10.1007/s00128-002-0004-y DOI: 10.1007/s00128-002-0004-y
Vorkamp K, Rigét FF (2014) A review of new and current-use contaminants in the Arctic environment: evidence of long-range transport and indications of bioaccumulation. Chemosphere. 111:379–395. 10.1016/j.chemosphere.2014.04.019 DOI: 10.1016/j.chemosphere.2014.04.019
Wania F, Mackay D (1996) Tracking the distribution of persistent organic pollutants. Environ Sci Technol 30(9):390A–396A. 10.1021/es962399q DOI: 10.1021/es962399q
