Contamination of Organochlorine Pesticides in Nest Soil, Egg, and Blood of the Snail-eating Turtle (Malayemys macrocephala) from the Chao Phraya River Basin, Thailand
Organochlorine pesticides (OCPs) are known to be
persistent and bioaccumulative toxicants that may cause reproductive
impairments in wildlife as well as human. The current study uses the
snail-eating turtle Malayemys macrocephala, a long-lived animal
commonly distribute in rice field habitat in central part of Thailand,
as a sentinel to monitor OCP contamination in environment. The
nest soil, complete clutch of eggs, and blood of the turtle were
collected from agricultural areas in the Chao Phraya River Basin,
Thailand during the nesting season of 2007-2008. The novel
methods for tissue extraction by an accelerated solvent extractor
(ASE, for egg) and liquid-liquid extraction (for blood) have been
developed. The nineteen OCP residues were analyzed by gas
chromatography with micro-electron captured detector (GC-μECD).
The validated methods have met requirements of the AOAC
standard. The results indicated that significant amounts of OCPs are
still contaminated in nest soil and eggs of the turtle even though the
OCPs had been banned in this area for many years. This suggested
the potential risk to health of wildlife as well as human in the area.
[1] A. S. Perry, I. Yamamato, I. Ishaaya and R. Perry, Insecticides in
Agriculture and Environment: Retrospects and Prospects, Berlin:
Springer, 1998.
[2] C. H. Walker, S. P. Hopkin, R. M. Sibly and D. B Peakall, Principles of
Ecotoxicology. 2nd ed, Boca Raton, FL: Taylor & Francis, 2001.
[3] W. P. Cunningham, M. A. Cunningham and S. B. Woodworth,
Environmental Science: A Global Concern, 9th ed., New York: McGraw-
Hill, 2007.
[4] K. Thirakhupt, D. Sitthicharoenchai, S. Keithmaleesatti and W.
Siriwong, "Organochlorine pesticides and their usages in Thailand: A
review," J. Sci. Res. Chulalongkorn Univ., vol. 31, pp. 1-15, 2006.
[5] T. Damstra, S. Barlow, A. Bergman, R. Kavlock, and G. Van Der Kraak,
Global Assessment of the State-of-the-Science of Endocrine Disruptors.
Geneva: International Programme on Chemical Safety, 2002.
[6] L. J. Guillette, T. S. Gross, G. R. Masson, J. M. Matter, H. F. Percival
and A. R. Woodward, "Developmental abnormalities of the gonad and
abnormal sex hormone concentrations in juvenile alligators from
contaminated and control lakes in Florida," Environ. Health Perspect.,
vol. 102, pp. 680-688, 1994.
[7] L. J. Guillette, D. B. Pickford, D. A. Crain, A. A. Rooney and H. F.
Percival, "Reduction in penis size and plasma testosterone
concentrations in juvenile alligators living in a contaminated
environment," Gen. Comp. Endocrinol., vol.101, pp. 32-42, 1996.
[8] W. A. Hopkins, "Use of tissue residues in reptile ecotoxicology: A call
for integration and experimentation" in Toxicology of Reptiles, S. C.
Gardner and E. Oberdörster, Eds. Boca Raton, FL: Taylor & Francis,
2006.
[9] J. M. Keller, J. R. Kucklick and P. D. McClellan-Green,
"Organochlorine contaminants in Loggerhead sea turtle blood:
extraction techniques and distribution among plasma and red blood
cells," Arch. Environ. Contam. Toxicol. vol. 46, pp. 254-264, 2004.
[10] J. J. Alava, J. M. Keller, J. R. Kucklick, J. Wyneken, L. Crowder and G.
I. Scott, "Loggerhead sea turtle (Caretta caretta) egg yolk
concentrations of persistent organic pollutants and lipid increase during
the last stage of embryonic development," Sci. Total Environ., vol. 367,
pp. 170-181, 2006.
[11] C. A. Bishop, P. Ng, K. E. Pettit, S. W. Kennedy, J. J. Stegeman, R. J.
Norstrom and R. J. Brooks, "Environmental contamination and
developmental abnormalities in eggs and hatchlings of the common
snapping turtle (Chelydra serpentina serpentina) from the Great Lakes-
St. Lawrence River (1989 - 1991)," Environ. Pollut., vol. 101, pp. 143-
156, 1998.
[12] S. R. de Solla, K. J. Fernie and S. Ashpole, "Snapping turtles (Chelydra
serpentina) as bioindicators in Canadian Areas of concern in the Great
Lakes Basin II. Changes in hatching success and hatchling deformities in
relation to persistent organic pollutants," Environ. Pollut., vol. 153, pp.
529-536, 2008.
[13] C. A. Bishop, D. R. S. Lean, R. J. Brooks, J. H. Carey and P. Ng,
"Chlorinated hydrocarbons in early life stages of the common snapping
turtle (Chelydra serpentina serpentina) from a coastal wetland on Lake
Ontario," Environ. Toxicol. Chem., vol. 14, pp. 421-426, 1995.
[14] W. Siriwong, "Organochlorine pesticide residues in aquatic ecosystem
and health risk assessment of local agricultural community," Ph.D.
dissertation, Graduate School, Chulalongkorn Univ., Bangkok, Thailand,
2006.
[15] S. Keithmaleesatti, K. Thirakhupt, A. Pradatsudarasar, P.
Varanusupakul, N Kitana, and M. Robson, "Concentration of
organochlorine in egg yolk and reproductive success of Egretta garzetta
(Linnaeus, 1758) at Wat Tan-en Non-hunting Area, Phra Nakhorn Si
Ayuthaya Province, Thailand," Ecotox. Environ. Safe., vol. 68, pp. 79-
83, 2007.
[16] N. Srinarumol, "Population biology of the Malayan snail-eating turtle
Malayemys subtrijuga (Schlegel and Muller, 1844)," M.S. thesis, Dept.
Biology, Fac. Sci., Chulalongkorn Univ., Bangkok, Thailand, 1995.
[17] T. R. Brophy, "Geographic variation and systematics in the South-east
Asia turtle of the genus Malayemys (Testudines: Bataguridae),"
Hamadryad, vol. 29, pp. 63-79, 2004.
[18] F. Bonin, B. Devaux and A. Dupré, Turtles of the World, 1st ed.,
Baltimore, MD: The Johns Hopkins University Press, 2006.
[19] W. Siriwong, K. Thirakhupt, D. Sitticharoenchai and M. Robson,
"Accumulation of organochlorine pesticide residues in aquatic plants," J.
Sci. Res. Chulalongkorn Univ., vol. 32, pp.7-14, 2007.
[20] R. D. Pridmore, S. F. Thrush, V. J. Cummings and J. E. Hewitt, "Effect
of the organochlorine pesticide technical chlordane on intertidal
macrofauna," Mar. Pollut. Bull., vol. 24, pp. 98-102, 1992.
[21] B. Pan, W. X. Liu, Z. Shi, J. Cao, W. R. Shen, B. P. Qing, R. Sun and S.
Tao, "Sample purification for analysis of organochlorine pesticides in
sediment and fish muscle," J. Environ. Sci. Health, vol. 39, pp. 353-365,
2004.
[22] C. M. Lino, C. B. F. Azzolini, D. S. V. Nunes, J. M. R. Silva and M. I.
N. Silveira, "Methods for the determination of organochlorine pesticide
residues in human serum," J. Chromatogr. B, vol. 716, pp. 147-152,
1998.
[23] P. Chulintorn, Ministry of Agriculture and Cooperatives, Bangkok,
Thailand, private communication, November 2006.
[24] T. Poolpak, P. Pokethitiyook, M. Kruatrachue, U. Arjarasirikoon and N.
Thanwaniwat, "Residue analysis of organochlorine pesticides in the Mae
Klong river of Central Thailand," J. Hazard Mater, vol. 156, pp. 230-
239, 2008.
[25] S. Keithmaleesatti, W. Siriwong, P. Varanusupakul, and N. Kitana,
"Organochlorine pesticide residues in egg of the snail-eating turtle
(Malayemys macrocephala) from the lower Chao Phraya River basin,
Thailand," presented at the 7th Int. Symp. Biological Monitoring in
Occupational and Environmental Health, Beijing, China, September 10-
12, 2007.
[26] T. H. Wu, J. E. Canas, T. R. Rainwater, S. G. Platt, S. T. McMurry and
T. A. Anderson, "Organochlorine contaminants in complete clutches of
Morelet-s crocodile (Crocodylus moreletii) eggs from Belize." Environ.
Pollut., vol. 144, pp. 151-157, 2006.
[27] S. J. Ormerod and S. J. Tyler, "Environmental pollutants in the eggs of
Welsh dippers Cinclus cinclus: a potential monitor of organochlorine
and mercury contamination in upland rivers," Bird Study, vol. 37, pp.
171-176, 1990.
[28] R. H. Rauschenberger, M. S. Sep├╝lveda, J. J. Wiebe, N. J. Szabo and T.
S. Gross, "Predicting maternal body burdens of organochlorine
pesticides from eggs and evidence of maternal transfer in Alligator
mississippiensis," Environ. Toxicol. Chem., vol. 23, pp. 2906-2915,
2004.
[29] R. H. Rauschenberger, J. J. Wiebe, J. E. Buckland, J. T. Smith, M. S.
Sepulveda and T. S. Gross, "Achieving environmentally relevant
organochlorine pesticide concentrations in eggs through maternal
exposure in Alligator mississsippiensis." Mar. Environ. Res., vol. 58, pp.
851-856, 2004.
[30] J. E. Canas and T. A. Anderson, "Organochlorine contaminants in eggs:
the influence of contaminated nest material," Chemosphere, vol. 47, pp.
585-589, 2002.
[31] S. R. de Solla, C. A. Bishop, G. Van Der Kraak and R. J. Brooks,
"Impact of organochlorine contamination on levels of sex hormones and
external morphology of common snapping turtles (Chelydra serpentina
serpentina) in Ontario, Canada," Environ. Health Perspect., vol. 106,
pp. 253-260, 1998.
[32] K. Bang, B. M. Jensen, C. Lydersen and J. C. Skaare, "Organochlorine
burdens in blood of ringed and bearded seals from north-western
Svalbard," Chemosphere, vol. 44, pp. 193-203, 2001.
[33] J. O. Bustnes, J. C. Skaare, K. E. Erikstad, V. Bakken and F. Mehlum,
"Whole blood concentration of organochlorine as a dose metric for
studies of the glaucocs gull (Larus hyperboreus)," Environ. Toxicol.
Chem., vol. 20, pp. 1046-1052, 2001.
[34] J. M. Keller, J. R. Kucklick, C. A. Harms, and P. D. McClellan-Green,
"Organochlorine contaminants in sea turtles: correlations between whole
blood and fat," Environ. Toxicol. Chem. vol. 23, pp. 726-38, 2004.
[35] The Association of Official Agricultural Chemists (AOAC) Peer
Verified Methods Program, Manual on Policies and Procedures.
Arlington, VA: AOAC, 1993.
[36] C. A. Bishop, G. P. Brown, R. J. Brooks, D. R. S. Lean, and J. H. Carey,
"Organochlorine contaminant concentrations in eggs and their
relationship to body size and clutch characteristics of the female
common snapping turtle (Chelydra serpentina serpentina) in Lake
Ontario, Canada," Arch. Environ. Contam. Toxicol. vol. 27, pp. 82-87,
1994.
[1] A. S. Perry, I. Yamamato, I. Ishaaya and R. Perry, Insecticides in
Agriculture and Environment: Retrospects and Prospects, Berlin:
Springer, 1998.
[2] C. H. Walker, S. P. Hopkin, R. M. Sibly and D. B Peakall, Principles of
Ecotoxicology. 2nd ed, Boca Raton, FL: Taylor & Francis, 2001.
[3] W. P. Cunningham, M. A. Cunningham and S. B. Woodworth,
Environmental Science: A Global Concern, 9th ed., New York: McGraw-
Hill, 2007.
[4] K. Thirakhupt, D. Sitthicharoenchai, S. Keithmaleesatti and W.
Siriwong, "Organochlorine pesticides and their usages in Thailand: A
review," J. Sci. Res. Chulalongkorn Univ., vol. 31, pp. 1-15, 2006.
[5] T. Damstra, S. Barlow, A. Bergman, R. Kavlock, and G. Van Der Kraak,
Global Assessment of the State-of-the-Science of Endocrine Disruptors.
Geneva: International Programme on Chemical Safety, 2002.
[6] L. J. Guillette, T. S. Gross, G. R. Masson, J. M. Matter, H. F. Percival
and A. R. Woodward, "Developmental abnormalities of the gonad and
abnormal sex hormone concentrations in juvenile alligators from
contaminated and control lakes in Florida," Environ. Health Perspect.,
vol. 102, pp. 680-688, 1994.
[7] L. J. Guillette, D. B. Pickford, D. A. Crain, A. A. Rooney and H. F.
Percival, "Reduction in penis size and plasma testosterone
concentrations in juvenile alligators living in a contaminated
environment," Gen. Comp. Endocrinol., vol.101, pp. 32-42, 1996.
[8] W. A. Hopkins, "Use of tissue residues in reptile ecotoxicology: A call
for integration and experimentation" in Toxicology of Reptiles, S. C.
Gardner and E. Oberdörster, Eds. Boca Raton, FL: Taylor & Francis,
2006.
[9] J. M. Keller, J. R. Kucklick and P. D. McClellan-Green,
"Organochlorine contaminants in Loggerhead sea turtle blood:
extraction techniques and distribution among plasma and red blood
cells," Arch. Environ. Contam. Toxicol. vol. 46, pp. 254-264, 2004.
[10] J. J. Alava, J. M. Keller, J. R. Kucklick, J. Wyneken, L. Crowder and G.
I. Scott, "Loggerhead sea turtle (Caretta caretta) egg yolk
concentrations of persistent organic pollutants and lipid increase during
the last stage of embryonic development," Sci. Total Environ., vol. 367,
pp. 170-181, 2006.
[11] C. A. Bishop, P. Ng, K. E. Pettit, S. W. Kennedy, J. J. Stegeman, R. J.
Norstrom and R. J. Brooks, "Environmental contamination and
developmental abnormalities in eggs and hatchlings of the common
snapping turtle (Chelydra serpentina serpentina) from the Great Lakes-
St. Lawrence River (1989 - 1991)," Environ. Pollut., vol. 101, pp. 143-
156, 1998.
[12] S. R. de Solla, K. J. Fernie and S. Ashpole, "Snapping turtles (Chelydra
serpentina) as bioindicators in Canadian Areas of concern in the Great
Lakes Basin II. Changes in hatching success and hatchling deformities in
relation to persistent organic pollutants," Environ. Pollut., vol. 153, pp.
529-536, 2008.
[13] C. A. Bishop, D. R. S. Lean, R. J. Brooks, J. H. Carey and P. Ng,
"Chlorinated hydrocarbons in early life stages of the common snapping
turtle (Chelydra serpentina serpentina) from a coastal wetland on Lake
Ontario," Environ. Toxicol. Chem., vol. 14, pp. 421-426, 1995.
[14] W. Siriwong, "Organochlorine pesticide residues in aquatic ecosystem
and health risk assessment of local agricultural community," Ph.D.
dissertation, Graduate School, Chulalongkorn Univ., Bangkok, Thailand,
2006.
[15] S. Keithmaleesatti, K. Thirakhupt, A. Pradatsudarasar, P.
Varanusupakul, N Kitana, and M. Robson, "Concentration of
organochlorine in egg yolk and reproductive success of Egretta garzetta
(Linnaeus, 1758) at Wat Tan-en Non-hunting Area, Phra Nakhorn Si
Ayuthaya Province, Thailand," Ecotox. Environ. Safe., vol. 68, pp. 79-
83, 2007.
[16] N. Srinarumol, "Population biology of the Malayan snail-eating turtle
Malayemys subtrijuga (Schlegel and Muller, 1844)," M.S. thesis, Dept.
Biology, Fac. Sci., Chulalongkorn Univ., Bangkok, Thailand, 1995.
[17] T. R. Brophy, "Geographic variation and systematics in the South-east
Asia turtle of the genus Malayemys (Testudines: Bataguridae),"
Hamadryad, vol. 29, pp. 63-79, 2004.
[18] F. Bonin, B. Devaux and A. Dupré, Turtles of the World, 1st ed.,
Baltimore, MD: The Johns Hopkins University Press, 2006.
[19] W. Siriwong, K. Thirakhupt, D. Sitticharoenchai and M. Robson,
"Accumulation of organochlorine pesticide residues in aquatic plants," J.
Sci. Res. Chulalongkorn Univ., vol. 32, pp.7-14, 2007.
[20] R. D. Pridmore, S. F. Thrush, V. J. Cummings and J. E. Hewitt, "Effect
of the organochlorine pesticide technical chlordane on intertidal
macrofauna," Mar. Pollut. Bull., vol. 24, pp. 98-102, 1992.
[21] B. Pan, W. X. Liu, Z. Shi, J. Cao, W. R. Shen, B. P. Qing, R. Sun and S.
Tao, "Sample purification for analysis of organochlorine pesticides in
sediment and fish muscle," J. Environ. Sci. Health, vol. 39, pp. 353-365,
2004.
[22] C. M. Lino, C. B. F. Azzolini, D. S. V. Nunes, J. M. R. Silva and M. I.
N. Silveira, "Methods for the determination of organochlorine pesticide
residues in human serum," J. Chromatogr. B, vol. 716, pp. 147-152,
1998.
[23] P. Chulintorn, Ministry of Agriculture and Cooperatives, Bangkok,
Thailand, private communication, November 2006.
[24] T. Poolpak, P. Pokethitiyook, M. Kruatrachue, U. Arjarasirikoon and N.
Thanwaniwat, "Residue analysis of organochlorine pesticides in the Mae
Klong river of Central Thailand," J. Hazard Mater, vol. 156, pp. 230-
239, 2008.
[25] S. Keithmaleesatti, W. Siriwong, P. Varanusupakul, and N. Kitana,
"Organochlorine pesticide residues in egg of the snail-eating turtle
(Malayemys macrocephala) from the lower Chao Phraya River basin,
Thailand," presented at the 7th Int. Symp. Biological Monitoring in
Occupational and Environmental Health, Beijing, China, September 10-
12, 2007.
[26] T. H. Wu, J. E. Canas, T. R. Rainwater, S. G. Platt, S. T. McMurry and
T. A. Anderson, "Organochlorine contaminants in complete clutches of
Morelet-s crocodile (Crocodylus moreletii) eggs from Belize." Environ.
Pollut., vol. 144, pp. 151-157, 2006.
[27] S. J. Ormerod and S. J. Tyler, "Environmental pollutants in the eggs of
Welsh dippers Cinclus cinclus: a potential monitor of organochlorine
and mercury contamination in upland rivers," Bird Study, vol. 37, pp.
171-176, 1990.
[28] R. H. Rauschenberger, M. S. Sep├╝lveda, J. J. Wiebe, N. J. Szabo and T.
S. Gross, "Predicting maternal body burdens of organochlorine
pesticides from eggs and evidence of maternal transfer in Alligator
mississippiensis," Environ. Toxicol. Chem., vol. 23, pp. 2906-2915,
2004.
[29] R. H. Rauschenberger, J. J. Wiebe, J. E. Buckland, J. T. Smith, M. S.
Sepulveda and T. S. Gross, "Achieving environmentally relevant
organochlorine pesticide concentrations in eggs through maternal
exposure in Alligator mississsippiensis." Mar. Environ. Res., vol. 58, pp.
851-856, 2004.
[30] J. E. Canas and T. A. Anderson, "Organochlorine contaminants in eggs:
the influence of contaminated nest material," Chemosphere, vol. 47, pp.
585-589, 2002.
[31] S. R. de Solla, C. A. Bishop, G. Van Der Kraak and R. J. Brooks,
"Impact of organochlorine contamination on levels of sex hormones and
external morphology of common snapping turtles (Chelydra serpentina
serpentina) in Ontario, Canada," Environ. Health Perspect., vol. 106,
pp. 253-260, 1998.
[32] K. Bang, B. M. Jensen, C. Lydersen and J. C. Skaare, "Organochlorine
burdens in blood of ringed and bearded seals from north-western
Svalbard," Chemosphere, vol. 44, pp. 193-203, 2001.
[33] J. O. Bustnes, J. C. Skaare, K. E. Erikstad, V. Bakken and F. Mehlum,
"Whole blood concentration of organochlorine as a dose metric for
studies of the glaucocs gull (Larus hyperboreus)," Environ. Toxicol.
Chem., vol. 20, pp. 1046-1052, 2001.
[34] J. M. Keller, J. R. Kucklick, C. A. Harms, and P. D. McClellan-Green,
"Organochlorine contaminants in sea turtles: correlations between whole
blood and fat," Environ. Toxicol. Chem. vol. 23, pp. 726-38, 2004.
[35] The Association of Official Agricultural Chemists (AOAC) Peer
Verified Methods Program, Manual on Policies and Procedures.
Arlington, VA: AOAC, 1993.
[36] C. A. Bishop, G. P. Brown, R. J. Brooks, D. R. S. Lean, and J. H. Carey,
"Organochlorine contaminant concentrations in eggs and their
relationship to body size and clutch characteristics of the female
common snapping turtle (Chelydra serpentina serpentina) in Lake
Ontario, Canada," Arch. Environ. Contam. Toxicol. vol. 27, pp. 82-87,
1994.
@article{"International Journal of Biological, Life and Agricultural Sciences:61171", author = "Sarun Keithmaleesatti and Pakorn Varanusupakul and Wattasit Siriwong and Kumthorn Thirakhupt and Mark Robson and Noppadon Kitana", title = "Contamination of Organochlorine Pesticides in Nest Soil, Egg, and Blood of the Snail-eating Turtle (Malayemys macrocephala) from the Chao Phraya River Basin, Thailand", abstract = "Organochlorine pesticides (OCPs) are known to be
persistent and bioaccumulative toxicants that may cause reproductive
impairments in wildlife as well as human. The current study uses the
snail-eating turtle Malayemys macrocephala, a long-lived animal
commonly distribute in rice field habitat in central part of Thailand,
as a sentinel to monitor OCP contamination in environment. The
nest soil, complete clutch of eggs, and blood of the turtle were
collected from agricultural areas in the Chao Phraya River Basin,
Thailand during the nesting season of 2007-2008. The novel
methods for tissue extraction by an accelerated solvent extractor
(ASE, for egg) and liquid-liquid extraction (for blood) have been
developed. The nineteen OCP residues were analyzed by gas
chromatography with micro-electron captured detector (GC-μECD).
The validated methods have met requirements of the AOAC
standard. The results indicated that significant amounts of OCPs are
still contaminated in nest soil and eggs of the turtle even though the
OCPs had been banned in this area for many years. This suggested
the potential risk to health of wildlife as well as human in the area.", keywords = "Gas chromatography, persistent organic pollutants,rice field, sentinel species.", volume = "3", number = "4", pages = "205-6", }
