Assessment of organochlorine pesticides and metals in ring-tailed lemurs (Lemur catta) at Beza Mahafaly special reserve, Madagascar

American Journal of Primatology

Volumn 71, Issue 12, 2009, Pages 998-1010

  Rainwater, Thomas R ^a   Sauther, Michelle L ^b   Rainwater, Katherine A E ^c   Mills, Rachel E ^c   Cuozzo, Frank P ^d   Baohong, Zhang ^a   McDaniel, Les N ^a   Abel, Michael T ^a   Marsland, Eric J ^a   Weber, Martha A ^e   Jacky, Ibrahim Antho Youssouf ^f   Platt, Steven G ^g   Cobb, George P ^a   Anderson, Todd A ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NORTH DAKOTA   (United States)

^e Department of Animal Health and Nutrition ^*  (United States)

^f Universitéde Toliara   (Madagascar)

^g SUL ROSS STATE UNIVERSITY   (United States)

Author keywords

Anthropogenic effects; Conservation; Metals; Organochlorine pesticides; Pollution; Primate; Toxicology

Indexed keywords

CHLORINATED HYDROCARBON; METAL; PESTICIDE;

BIOACCUMULATION; BODY SIZE; CONSERVATION MANAGEMENT; ECOTOXICOLOGY; ENDEMIC SPECIES; HABITAT LOSS; HUMAN ACTIVITY; METABOLITE; NATURE RESERVE; ORGANOCHLORINE; PERSISTENCE; POLLUTION EFFECT; POLLUTION EXPOSURE; PRIMATE; SURVIVAL; TOXICOLOGY; TRACE METAL;

ANIMAL; ARTICLE; BLOOD; ENVIRONMENTAL MONITORING; FEMALE; MADAGASCAR; MALE; METABOLISM; POLLUTANT; PROSIMIAN;

ANIMALS; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; FEMALE; HYDROCARBONS, CHLORINATED; LEMUR; MADAGASCAR; MALE; METALS; PESTICIDES;

BEZA MAHAFALY SPECIAL RESERVE; INDIAN OCEAN; INDIAN OCEAN ISLANDS; MADAGASCAR; TOLIARA;

LEMUR; LEMUR CATTA; LEMURIDAE; MAMMALIA; PRIMATES; STREPSIRHINI;

EID: 70350431478     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20742     Document Type: Article

References (80)

1. Abel MT, Presley SM, Rainwater TR, Austin GP, Cox SB, McDaniel LN, Marsland EJ, Leftwich BD, Kendall RJ, Cobb GP. 2007. Spatial and temporal evaluation of metal concentrations in soils and sediments from New Orleans, LA following hurricanes Katrina and Rita. Environ Toxicol Chem 26:2108-2114.
2. Addison RF, Brodie PF. 1977. Organochlorine residues in maternal blubber, milk, and pup blubber from grey seals (Halichoerus grypus) from Sable Island, Nova Scotia. J Fish Res Board Can 34:937-941.
3. Addison RF, Brodie PF. 1987. Transfer of organochlorine residues from blubber through the circulatory system in milk in the lactating grey seal, Halichoerus grypus. Can J Fish Aquat Sci 44:782-786.
4. ATSDR. 2002. Toxicological profile for DDT, DDE, and DDD. Agency for Toxic Substances and Disease Registry, U.S. Public Health Service, Atlanta, ATSDR. 403p.
5. Bernhoft A, Wiig O, Skaare JU. 1997. Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environ Pollut 95:159-175.
6. Beyer WN, Heinz GH, Redmon-Norwwod AW, editors. 1996. Environmental contaminants in wildlife: interpreting tissue concentrations. Boca Raton: CRC Press. 494p.
7. Borrell A, Bloch D, Desportes G. 1995. Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands. Environ Pollut 88:283-292.
8. Burger J, Marquez M, Gochfeld M. 1994. Heavy metals in hair of opossum from Palo Verde, Costa Rica. Arch Environ Contam Toxicol 27:472-476.
9. Burger J, Murray S, Gaines KF, Novak JM, Punshon T, Dixon C, Gochfeld M. 2006. Element levels in snakes in South Carolina: differences between a control site and exposed site on the Savannah River Site. Environ Monit Assess 112:35-52.
10. Castillo LE, de la Cruz E, Ruepert C. 1997. Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environ Toxicol Chem 16:41-51.
11. Cobb GP, Abel MT, Rainwater TR, Austin GP, Cox SB, Kendall RJ, Marsland EJ, Anderson TA, Leftwich BD, Zak JC, Presley SM. 2006. Metal distributions in New Orleans following Hurricanes Katrina and Rita: a continuation study. Environ Sci Technol 40:4571-4577.
12. Collins C, Fryer M, Grosso A. 2006. Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45-52.
13. Cuozzo FP, Sauther ML. 2004. Tooth loss, survival, and resource use in wild ring-tailed lemurs (Lemur catta): implications for inferring conspecific care in fossil hominids. J Hum Evol 46:625-633.
14. Cuozzo FP, Sauther ML. 2006a. Temporal change in tooth size among ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve, Madagascar: effects of an environmental fluctuation. In: Jolly A, Sussman RW, Koyama N, Rasmimanana H, editors. Ring-tailed lemur biology. New York: Springer. p 343-366.
15. Cuozzo FP, Sauther ML. 2006b. Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history. J Hum Evol 51:490-505.
16. Cuozzo FP, Sauther ML, Yamashita N, Lawler RR, Brockman DK, Godfrey LR, Gould L, Youssouf IAJ, Lent C, Ratsirarson J, Richard AF, Scott JR, Sussman RW, Villers LM, Weber MA, Willis G. 2008. A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar. Am J Primatol 70:363-371.
17. Curtis CF. 2002. Restoration of malaria control in the Madagascar highlands by DDT spraying. Am J Trop Med Hyg 66:1.
18. Custer TW, Custer CM, Hines RK, Sparks DW. 2000. Trace elements, organochlorines, polycyclic aromatic hydrocarbons, dioxins, and furans in lesser scaup wintering on the Indiana Harbor Canal. Environ Pollut 110:469-482.
19. Daly GL, Lei YD, Teixeira C, Muir DCG, Castillo LE, Wania F. 2007. Accumulation of current-use pesticides in neotropical montane forests. Environ Sci Technol 41:1118-1123.
20. Davis RS, Peterson RKD, Macedo PA. 2007. An ecological risk assessment for insecticides used in adult mosquito management. Integr Environ Assess Manag 3:373-382.
21. Dip R, Hegglin D, Deplazes P, Dafflon O, Koch H, Naegeli H. 2003. Age-and sex-dependent distribution of persistent organochlorine pollutants in urban foxes. Environ Health Perspect 111:1608-1612.
22. Duinker JC, Hillebrand MTJ. 1979. Mobilization of organo-chlorines from female lipid tissue and transplacental transfer to fetus in a harbour porpoise (Phocoena phocoena) in a contaminated area. Bull Environ Contam Toxicol 23:728-732.
23. Dutton CJ, Junge RE, Louis EE. 2003. Biomedical evaluation of free-ranging ring-tailed lemurs (Lemur catta) in Tsimanampetsotsa Strict Nature Reserve, Madagascar. J Zoo Wildl Med 34:16-24.
24. Eisler R. 1985. Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. Report 85 (1.12), U.S. Fish and Wildlife Service, Washington. 30p.
25. Eisler R. 1988. Lead hazards to fish, wildlife, and invertebrates: a synoptic review. Report 85 (1.14). U.S. Fish and Wildlife Service, Washington. 94p.
26. El Khalil H, El Hamiani O, Bitton G, Ouazzani N, Boularbah A. 2008. Heavy metal contamination from mining sites in South Morocco: monitoring metal content and toxicity of soil runoff and groundwater. Environ Monit Assess 136: 147-160.
27. Finkelstein ME, Gwiazda RH, Smith DR. 2003. Lead poisoning of seabirds: environmental risks from leaded paint at a decommissioned military base. Environ Sci Technol 37:3256-3260.
28. Gardner CJ, Fanning E, Thomas H, Kidney D. 2009. The lemur diversity of the Fiherenana-Manombo Complex, southwest Madagascar. Mad Conserv Develop 4:38-43.
29. Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT. 2000. The global decline of reptiles, déjà vu amphibians. Bioscience 50:653-666.
30. Goodman SM, Rakotoarisoa SV, Wilmé L. 2006. The distribution and biogeography of the Ringtailed Lemur (Lemur catta) in Madagascar. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H, editors. Ring-tailed lemur biology. New York: Springer. p 3-15.
31. Greig DJ, Ylitalo GM, Hall AJ, Fauquier DA, Gulland FMD. 2007. Transplacental transfer of organochlorines in California sea lions (Zalophus californianus). Environ Toxicol Chem 26:37-44.
32. Hariono B, Ng J, Sutton RH. 1993. Lead concentrations in tissues of fruit bats (Pteropus sp.) in urban and non-urban locations. Wildl Res 20:315-320.
33. Junge RE, Louis EE. 2005. Biomedical evaluation of two sympatric lemur species (Propithecus verreauxi deckeni and Eulemur fulvus rufus) in Tsiombokibo classified forest, Madagascar. J Zoo Wildl Med 36:581-589.
34. Kershaw TG, Clarkson TW, Dhahir PH. 1980. The relationship between blood levels and dose of methylmercury in man. Arch Environ Health 35:28-36.
35. Kilbourn AM, Karesh WB, Wolfe ND, Bosi EJ, Cook RA, Andau M. 2003. Health evaluation of free-ranging and semicaptive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. J Wildl Dis 39:73-83.
36. Klemens JA, Wieland ML, Flanagin VJ, Frick JA, Harper RG. 2003. A cross-taxa survey of organochlorine pesticide contamination in a Costa Rican wildland. Environ Pollut 122: 245-251.
37. Koeman JH, Den Boer WMJ, Feith AF, de Iongh HH, Spliethoff PC. 1978. Three years' observation on side effects of helicopter applications of insecticides used to exterminate Glossina species in Nigeria. Environ Pollut 15:31-59.
38. Lacher TE, Goldstein MI. 1997. Tropical ecotoxicology: status and needs. Environ Toxicol Chem 16:100-111.
39. Lahaye V, Bustamante P, Dabin W, Churlaud C, Caurant F. 2007. Trace element levels in foetus-mother pairs of short- beaked common dolphins (Delphinus delphis) stranded along the French coasts. Environ Int 33:1021-1028.
40. Lowry II PP, Randriatafika F, Rabenantoandro J. 2008. Conservation status of vascular plant species from the QMM/Rio Tinto mining area at Mandena, Tolagnaro (Fort Dauphin) region, southeast Madagascar. Mad Conserv Develop 3:55-63.
41. Luo XW, Foo SC, Ong HY. 1997. Serum DDT and DDE levels in Singapore general population. Sci Total Environ 208:97-104.
42. McIlroy JC. 1981. The sensitivity of Australian animals to 1080 Poison I. intraspecific variation and factors affecting acute toxicity. Aust Wildl Res 8:369-383.
43. Michel K, Ludwig B. 2005. Bioavailability and biogeochemistry of metals in the terrestrial environment. In: Sigel A, Sigel H, Sigel RKO, editors. Metal ions in biological systems, volume 44: biogeochemistry, availability, and transport of metals in the environment. London: Informa Health Care. p 75-96.
44. Miller DS, Sauther ML, Hunter-Ishikawa M, Fish K, Culbertson H, Cuozzo FP, Campbell TW, Andrews GA, Chavey PS, Nachreiner R, Rumbeiha W, Stacewicz-Sapuntzakis M, Lappin MR. 2007. Biomedical evaluation of free-ranging ring-tailed lemurs (Lemur catta) in three habitats at Beza Mahafaly Special Reserve, Madagascar. J Zoo Wildl Med 38:201-216.
45. Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajaobelina S, Tatersall I, Myers D. 2006. Lemurs of Madagascar, 2nd ed. Conservation International: Washington DC. 520p.
46. Miranda KC, Metcalfe CD, Metcalfe TL, Muelbert MMC, Robaldo RB, Martinez PE, Colares EP, Bianchini A. 2009. Lactational transfer of PCBs and chlorinated pesticides in pups of southern elephant seals (Mirounga leonina) from Antarctica. Chemosphere 75:610-616.
47. Mora MA, Laack LL, Lee MC, Sericano J, Presley R, Gardinali PR, Gamble LR, Roberston S, Frank D. 2000. Environmental contaminants in blood, hair, and tissues of ocelots from the lower Rio Grande Valley, Texas, 1986-1997. Environ Monit Assess 64:477-492.
48. Murray DL. 1994. Cultivating Crisis: The human cost of pesticides in Latin America. Austin: University of Texas Press. 177p.
49. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.
50. Ogola JS, Mitullah WV, Omulo MA. 2002. Impact of gold mining on the environment and human health: a case study in the Migori Gold Belt, Kenya. Environ Geochem Health 24:141-158.
51. O'Hara TM, Carroll G, Barboza P, Mueller K, Blake J, Woshner V, Willetto C. 2001. Mineral and heavy metal status as related to a mortality event and poor recruitment in a moose population in Alaska. J Wildl Dis 37:509-522.
52. Peveling R, Rafanomezantsoa JJ, Razafinirina R, Tovonkery R, Zafimaniry G. 1999. Environmental impact of the locust control agents fenitrothion, fenitrothion-esfenvalerate and triflumuron on terrestrial arthropods in Madagascar. Crop Prot 18:659-676.
53. Peveling R, McWilliam AN, Nagel P, Rasolomanana H, Raholijaona, Rakotomianina L, Ravoninjatovo A, Dewhurst CF, Gibson G, Rafanomezana S, Tingle CCD. 2003. Impact of locust control on harvester termites and endemic vertebrate predators in Madagascar. J Appl Ecol 40:729-741.
54. Pfleeger TG, Fong A, Hayes R, Ratsch H, Wickliff C. 1996. Field evaluation of the EPA (Kenaga) nomogram, a method for estimating wildlife exposure to pesticide residues on plants. Environ Toxicol Chem 15:535-543.
55. Ramirez M, Massolo S, Frache R, Correa JA. 2005. Metal speciation and environmental impact on sandy beaches due to El Salvador copper mine, Chile. Mar Pollut Bull 50:62-72.
56. Roberts DR, Vanzie E, Bangs MJ, Grieco JP, Lenares H, Hshieh P, Rejmankova E, Manguin S, Andre RG, Polanco J. 2002. Role of residual spraying for malaria control in Belize. J Vector Ecol 27:63-69.
57. Romi R, Razaiarimanga C, Raharimanga R, Rakotondraibe EM, Ranaivo LH, Pietra V, Raveloson A, Majori G. 2002. Impact of the malaria control campaign (1993-1998) in the highlands of Madagascar: parasitological and entomological data. Am J Trop Med Hyg 66:2-6.
58. Santos X, Pastor D, Llorente GA, Albaige's J. 1999. Organo- chlorine levels in viperine snake Natrix maura carcasses from the Ebro Delta (NE Spain): sexual and size-related differences. Chemosphere 39:2641-2650.
59. Sauther ML. 1998. The interplay of phenology and reproduction in ring-tailed lemurs; implications for ring-tailed lemur conservation. Folia Primatol 69:309-320.
60. Sauther ML, Sussman RW, Gould L. 1999. The socioecology of the ringtailed lemur: thirty-five years of study. Evol Anthropol 8:120-132.
61. Sauther ML, Sussman RW, Cuozzo FP. 2002. Dental and general health in a population of wild ring-tailed lemurs: a life history approach. Am J Phys Anthropol 117:122-132.
62. Sauther ML, Fish K, Cuozzo F, Miller DS, Hunter-Ishikawa M, Culbertson H. 2006. Patterns of health, disease and behavior among wild ring-tailed lemurs, Lemur catta: effects of habitat and sex. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H, editors. Ring-tailed lemur biology. New York: Springer. p 313-331.
63. Schmitt CJ, Hinck JE, Blazer VS, Denslow ND, Dethloff GM, Bartish TM, Coyle JJ, Tillitt DE. 2005. Environmental contaminants and biomarker responses in fish from the Rio Grande and its U.S. tributaries: spatial and temporal trends. Sci Total Environ 350:161-193.
64. Shen L, Wania F, Lei YD, Teixeira C, Muir DCG, Bidleman TF. 2005. Atmospheric distribution and long-range transport behavior of organochlorine pesticides in North America. Environ Sci Technol 39:409-420.
65. Shore RF, Rattner BA, editors. 2001. Ecotoxicology of wild mammals. New York: John Wiley and Sons. 730p.
66. Sims RC, Overcash MR. 1983. Fate of polynuclear aromatic compounds (PNAs) in soil-plant systems. Residue Rev 88:1-68.
67. Smith PN, Cobb GP, Godard-Codding C, Hoff D, McMurry ST, Rainwater TR, Reynolds KD. 2007. Contaminant exposure in terrestrial vertebrates. Environ Pollut 150:41-64.
68. Sondgeroth K, Blitvich B, Blair C, Terwee J, Junge R, Sauther M, Vandewoude S. 2007. Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ringtailed lemurs in southwestern Madagascar. J Wildl Dis 43:40-47.
69. Sussman RW. 1991. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am J Phys Anthropol 84:43-58.
70. Turusov V, Rakitsky V, Tomatis L. 2002. Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110:125-128.
71. U.S. Environmental Protection Agency. 1998. Guidance for data quality assessment. Practical methods for data analysis. EPA/6000/R-96/084. Available at: http://www.epa.gov/swerust1/cat/epaqag9.pdf.
72. Waichman AV, Rombke J, Ribeiro MOA, Nina NCS. 2002. Use and fate of pesticides in the Amazon state, Brazil-risk to human health and the environment. Environ Sci Pollut Res 9:423-428.
73. Wandiga SO. 2001. Use and distribution of organochlorine pesticides. The future in Africa. Pure Appl Chem 73:1147-1155.
74. Weis IM, Muir DCG. 1997. Geographical variation of persistent organochlorine concentrations in blubber of ringed seal (Phoca hispida) from the Canadian arctic: univariate and multivariate approaches. Environ Pollut 96:321-333.
75. Whitelaw D, Sauther ML, Loudon JE, Cuozzo F. 2005. Anthropogenic change in and around Beza-Mahafaly Reserve: methodology and results. Am J Phys Anthropol Suppl 40:222.
76. Wiktelius S, Edwards CA. 1997. Organochlorine insecticide residues in African fauna: 1971-1995. Rev Environ Contam Toxicol 151:1-37.
77. Wolfe MF, Schwarzbach S, Sulaiman RA. 1998. Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146-160.
78. Yamashita N. 2002. Diets of two lemur species in different microhabitats in Beza Mahafaly Special Reserve, Madagascar. Int J Primatol 23:1025-1051.
79. Yoshikane M, Kay WR, Shibata Y, Inoue M, Yanai T, Kamata R, Edmonds JS, Morita M. 2006. Very high concentrations of DDE and toxaphene residues in crocodiles from the Ord River, Western Australia: an investigation into possible endocrine disruption. J Environ Monit 8:649-661.
80. Zhang BH, Pan XP, Smith JN, Anderson TA, Cobb GP. 2007. Extraction and determination of trace amounts of energetic compounds in blood by gas chromatography with electron capture detection (GC/ECD). Talanta 72:612-619.