. 2009 Sep 23;118(1):20–32. doi: 10.1289/ehp.0901164

Table 3.

Summary of the results for the effects of atrazine, through water column exposure, on fish and amphibian immunity.

Taxon, species	End point	Effect direction	Conc where effect was observed (μg/L)	Conc tested (μg/L)	Nonmonotonic dose response^a	Atrazine grade	Experiment type^b	Exposure duration	Reference
Salamander
A. tigrinum	No. of peripheral leukocytes	↓	16, 160	1.6, 16, 160	No	Tech	SR	Until metamorphosis	Forson and Storfer 2006b

Frog
R. pipiens	Splenocyte viability	ND	–	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2003, 2004 ^a
R. pipiens	No. of splenocytes	↓, if using appropriate one-tailed test	210	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2003, 2004 ^a
R. pipiens	No. of phagocytic splenocytes	↓ postinfection	210	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2003 ^a
R. pipiens	T cell proliferation	↓ in presence of mitogens	2.1, 21, 210	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2003, 2004 ^a
R. pipiens	T cell proliferation	↓ in absence of mitogens	2.1, 21, 210	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2003, 2004 ^a
R. pipiens	Absolute no. of phagocytic cells in spleen	↓	2.1, 21, 210	2.1, 21, 210	No	Tech	SR	21 days	Christin et al. 2004 ^a
R. pipiens	No. of thymic plaques	↑, indicating reduced immune capacity^b	0.1	0.1	NA	Tech	SR	Until metamorphosis	Hayes et al. 2006
R. pipiens	No. of hemolytic plaques representing antibody secreting B cells	↓	1, 10	1, 10	No	Not provided	SR	4 weeks	Houck and Sessions 2006
R. pipiens	No. of lymphocyte from spleen	ND	–	1, 10	Possibly	Not provided	SR	8 weeks	Houck and Sessions 2006
R. pipiens	No. of white blood cells	↓	0.01 to 10	0.01, 0.1, 1, 10	No	Tech	SR	8 days	Brodkin et al. 2007 ^c
R. pipiens	No. of highly phagocytic cells	↓	0.01 to 10	0.01, 0.1, 1, 10	No	Tech	SR	8 days	Brodkin et al. 2007 ^c
X. laevis	Splenocyte viability	ND	–	2.1, 21, 210, 2,100	No	Tech	SR	21 days	Christin et al. 2004 ^a
X. laevis	Splenocyte cellularity	↓	210, 2100	2.1, 21, 210, 2,100	No	Tech	SR	21 days	Christin et al. 2004 ^a
X. laevis	Relative no. of phagocytic cells in spleen	↑	21, 210, 2,100	2.1, 21, 210, 2,100	No	Tech	SR	21 days	Christin et al. 2004 ^a
X. laevis	Absolute no. of phagocytic cells in spleen	↓	210, 2,100	2.1, 21, 210, 2,100	No	Tech	SR	21 days	Christin et al. 2004 ^a
X. laevis	T cell proliferation	ND	–	2.1, 21, 210, 2,100	No data	Tech	SR	21 days	Christin et al. 2003 ^a
X. laevis	Downregulation of several genes involved in skin peptide defense	↓	400	400	NA	Tech	SR	Until metamorphosis	Langerveld et al. 2009
X. laevis	Downregulation of several genes involved in blood cell function	↓	400	400	NA	Tech	SR	Until metamorphosis	Langerveld et al. 2009
R. sylvatica	No. of eosinophil from circulating blood	↓	3, 30	3, 30	No	Tech	SR	4 weeks	Kiesecker 2002
R. pipiens	No. of melano-macrophages from liver	↓	< 1 Do not know maximum concentration	Unknown	No	Comm	FS	Unknown	Rohr et al. 2008c ^d
Rana paulustris	No. of melano-macrophages from liver	↓	117	117	NA	Tech	PE	4 weeks	Rohr et al. 2008c
R. paulustris	No. of eosinophil from liver	ND, trend toward decrease; p = 0.10	117	117	NA	Tech	PE	4 weeks	Rohr et al. 2008c
R. clamitans	No. of eosinophil from liver	↓	117	117	NA	Tech	PE	4 weeks	Rohr et al. 2008c
R. clamitans	No. of melano-macrophages from liver	ND	117	117	NA	Tech	PE	4 weeks	Rohr et al. 2008c

Fish
C. auratus	No. of superoxide radical from macrophages of spleen and kidney	↑ 4 and 8 weeks; indicator of oxidative stress	42	42	NA	Tech	SR	12 weeks	Fatima et al. 2007 ^a
C. auratus	Plasma lysozyme activity	↑ at 8 and 12 weeks, argued as a reduction in resistance to infection	42	42	NA	Tech	SR	12 weeks	Fatima et al. 2007 ^a
C. auratus	Antibody titers against Aeromonas hydrophila	↓	42	42	NA	Tech	SR	12 weeks	Fatima et al. 2007 ^a
C. auratus	Antioxidant enzyme in spleen (superoxide dismutase)	↓ at 4, 8, and 12 weeks	42	42	NA	Tech	SR	12 weeks	Fatima et al. 2007 ^a
Galaxias maculatus	Leucocrit	↓	3, 50	0.9, 3, 10, 50	Possibly	Tech	SR	10 days	Davies et al. 1994
O. mykiss	Proliferative ability of circulating T lymphocytes (ConA)	↓	> 5,000	1,000–10,000	Possibly	Tech	PE	2 days	Rymuszka et al. 2007
O. mykiss	Proliferative ability of circulating B lymphocytes (LPS)	↓	> 5,000	1,000–10,000	Possibly	Tech	PE	2 days	Rymuszka et al. 2007
O. mykiss	Respiratory burst activity of circulating phagocytes	↓	> 2,500	1,000–10,000	Possibly	Tech	PE	2 days	Rymuszka et al. 2007
Liza ramada and Liza aurata	Macrophage quality	↓ (cells degenerated)	25–280	Unknown	Unknown	Unknown	Unknown	Unknown	Biagianti-Risbourg 1990 ^e
L. ramada and L. aurata	Melanomacrophage centers in liver	↑	25–280	Unknown	Unknown	Unknown	Unknown	Unknown	Biagianti-Risbourg 1990 ^e
Salmonidae (species not specified)	White blood cells	↓	100–1,000	Unknown	Unknown	Unknown	Unknown	Unknown	Walsh and Ribelin 1975 ^e
Salmonidae (species not specified)	Lymphoid organ quality	↓ (evidence of atrophy)	100–1,000	Unknown	Unknown	Unknown	Unknown	Unknown	Walsh and Ribelin 1975 ^e
Salvelinus namaycush, Oncorhynchus kisutch	Spleen weight	↓/no effect	1,500–13,500	Unknown	Unknown	Unknown	Unknown	Unknown	Zeeman and Brindley 1981
S. namaycush, O. kisutch	No. of lymphocytes	↓/no effect	1,500–13,500	Unknown	Unknown	Unknown	Unknown	Unknown	Zeeman and Brindley 1981

Abbreviations: ↓, decreased; ↑, increased; Comm, commercial; Conc, concentration; FS, field survey; NA, not applicable (used when there were too few concentrations to evaluate nonmonotonicity); ND, not detected; PE, pulse experiment; SR, static renewal experiment, Tech, technical. Excluded studies are listed in Supplemental Material, Table S1 (doi:10.1289/ehp.0901164.S1).

Atrazine was a component of a mixture of pesticides tested, and thus the experiment did not isolate the effects of atrazine.

Atrazine alone and every mixture containing atrazine increased thymic plaques.

Immune response stimulated by thioglycollate.

No quantified factors correlated with atrazine could parsimoniously explain patterns in infection.

As reported by Dunier and Swicki 1993; could not obtain original works.