Insecticide-induced hormesis and arthropod pest management

Pest Management Science

Volumn 70, Issue 5, 2014, Pages 690-697

  Guedes, Raul Narciso C ^a   Cutler, G Christopher ^b  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Biphasic concentration response; Hormoligosis; Insecticidal stress; Insecticide ecotoxicology; Pesticide mediated homeostatic regulation; Sublethal effects

Indexed keywords

ARTHROPODA;

INSECTICIDE;

ANIMAL; ARTHROPOD; DRUG EFFECTS; HORMESIS; INSECTICIDE RESISTANCE; PEST CONTROL;

ANIMALS; ARTHROPODS; HORMESIS; INSECTICIDE RESISTANCE; INSECTICIDES; PEST CONTROL;

EID: 84898620653     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3669     Document Type: Review

References (109)

1. Stumpf WE, The dose makes the medicine. Drug Discov Today 11:550-550 (2006).
2. Kendig EL, Le HH and Blecher SM, Defining hormesis: evaluation of a complex concentration response phenomenon. Int J Toxicol 29:235-246 (2010).
3. Jacobi J and Guterman N, Paracelsus: Selected Writings. Princeton University, Princeton, NJ (1995).
4. Schulz H, Uber Hefegifte. Pflug Arch Gesamte Physiol 42:517-541 (1888).
5. Hueppe F and Jordan EO, The Principles of Bacteriology. The Open Court, Chicago, IL (1899).
6. Calabrese EJ and Baldwin LA, The marginalization of hormesis. Hum Exp Toxicol 19:32-40 (2000).
7. Calabrese EJ, Hormesis: once marginalized, evidence now supports hormesis as the most fundamental dose response, in Hormesis: A Revolution in Biology, Toxicology and Medicine, ed. by Mattson MP and Calabrese EJ. Springer, New York, pp. 15-56 (2010).
8. Southam CM and Ehrlich J, Effects of extract of Western red-cedar heartwood on certain wood-decaying fungi in culture. Phytopathology 33:517-524 (1943).
9. Calabrese EJ and Baldwin LA, The dose determines the stimulation (and poison): development of a chemical hormesis database. Int J Toxicol 16:545-559 (1997).
10. Calabrese EJ and Baldwin LA, A quantitatively-based methodology for the evaluation of chemical hormesis. Hum Ecol Risk Assess 3:545-554 (1997).
11. Calabrese EJ and Baldwin LA, The frequency of U-shaped dose responses in the toxicological literature. Toxicol Sci 62:330-338 (2001).
12. Calabrese EJ and Baldwin LA, U-Shaped dose-response in biology, toxicology, and public health. Annu Rev Public Health 22:15-33 (2001).
13. Calabrese EJ and Blain R, The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview. Toxicol Appl Pharmacol 202:289-301 (2005).
14. Jager T, Barsi A and Ducrot V, Hormesis on life-history traits: is there such a thing as a free lunch? Ecotoxicology 22:263-270 (2013).
15. Cutler GC, Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11:154-177 (2013).
16. Costantini D, Metcalfe NB and Monaghan P, Ecological processes in a hormetic framework. Ecol Lett 13:1435-1447 (2010).
17. Luckey TD, Insecticide hormoligosis. J Econ Entomol 61:7-12 (1968).
18. Cohen E, Pesticide-mediated homeostatic modulation in arthropods. Pestic Biochem Physiol 85:21-27 (2006).
19. Guedes RNC, Magalhães LC and Cosme LV, Stimulatory sublethal response of a generalist predator to permethrin: hormesis, hormoligosis, or homeostatic regulation? J Econ Entomol 102:170-176 (2009).
20. Morse JG, Agricultural implications of pesticide-induced hormesis of insects and mites. Hum Exp Toxicol 17:266-269 (1998).
21. Capinera JL, Hormoligosis, in Encyclopedia of Entomology, Vol. 2 (D-K), ed. by Capinera JL. Springer, Heidelberg, pp. 1851-1852 (2008).
22. Belz RG, Cedergreen N and Duke SO, Herbicide hormesis - can it be useful in crop production? Weed Res 51:321-332 (2011).
23. Yu Y, Shen G, Zhu H and Lu Y, Imidacloprid-induced hormesis on the fecundity and juvenile hormone levels of the green peach aphid Myzuspersicae (Sulzer). Pestic Biochem Physiol 98:238-242 (2010).
24. Rozman KK and Doull J, Scientific foundation of hormesis. Part 2. Maturation, strengths, limitations and possible applications in toxicology, pharmacology, and epidemiology. Crit Rev Toxicol 33:451-462 (2003).
25. Thayer KA, Melnick R, Burns K, Davis D and Huff J, Fundamental flaws of hormesis for public health decisions. Environ Health Persp 113:1271-1276 (2005).
26. Mushak P, Hormesis and its place in nonmonotonic dose-response relationships: some scientific reality checks. Environ Health Persp 115:500-506 (2007).
27. Rattan SIS, Hormesis in aging. Ageing Res Rev 7:63-78 (2008).
28. Mattson MP, Calabrese EJ, Hormesis: what it is and why it matters, in Hormesis: A Revolution in Biology, Toxicology and Medicine, ed. by Mattson MP and Calabrese EJ. Springer, New York, pp. 1-14 (2010).
29. Vaiserman AM, Hormesis, adaptive epigenetic reorganization, and implications for human health and longevity. Dose-Response 8:16-21 (2010).
30. Stebbing ARD, A theory of growth hormesis. BELLE Newsl 6:1-11 (1997).
31. Forbes VE, Is hormesis an evolutionary expectation? Funct Ecol 14:12-24 (2000).
32. Stebbing ARD, Hormesis: Interpreting the β-curve using control theory. J Appl Toxicol 20:93-101 (2000).
33. Stebbing ARD, Maia hypothesis - growth control and toxicology. Hum Ecol Risk Assess 6:301-311 (2000).
34. Calabrese EJ, Evidence that hormesis represents an 'overcompensation' response to a disruption in homeostasis. Ecotoxicol Environ Safe 42:135-137 (1999).
35. Sibly RM and Calow P, Physiological Ecology of Animals - An Evolutionary Approach. Blackwell, Oxford (1986).
36. Weltje L, vom Saal FS and Oehlmann J, Reproductive stimulation by low doses of xenoestrogens contrasts with the view of hormesis as an adaptive response. Hum Exp Toxicol 24:431-437 (2005).
37. Milsum JH, Biological Control Systems Analysis. McGraw-Hill, New York (1966).
38. Calabrese EJ and Baldwin LA, Defining hormesis. Hum Exp Toxicol 21:91-97 (2002).
39. Calow P, Physiological costs of combating chemical toxicants: ecological implications. Comp Biochem Physiol C 100:3-6 (1991).
40. Daniel SH and Smith RH, Functional anatomy of the egg pore in Callosobruchusmaculates: a trade-off between gas-exchange and protective functions? Physiol Entomol 19:30-38 (1994).
41. Calow P and Forbes VE, How do physiological responses to stress translate into ecological and evolutionary processes? Comp Biochem Physiol A 120:11-16 (1998).
42. Chown SL and Gaston K, Exploring links between physiology and ecology at macro-scales: the role of respiratory metabolism in insects. Biol Res 74:87-120 (1999).
43. Coustau C, Chevillon C and ffrench-Constant RH, Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15:378-383 (2000).
44. Guedes RNC, Oliveira EE, Guedes NMP, Ribeiro B and Serrão JE, Cost and mitigation of insecticide resistance in the maize weevil. Physiol Entomol 31:30-38 (2006).
45. Ayyanath MM, Cutler GC, Scott-Dupree CD and Sibley PK, Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. Plos One 8:e74532 (2013).
46. Jager T, Crommentuijn T, Van Gestel CAM and Kooijman SALM, Simultaneous modeling of multiple endpoints in life-cycle toxicity tests. Environ Sci Technol 38:2894-2900 (2004).
47. Vilca Mallqui KS, Vieira JL, Guedes RNC and Gontijo LM, Azadirachtin-mediated shift in fecundity-longevity trade-off in the Mexican bean beetle Zabrotessubfasciatus. J Econ Entomol (in press).
48. Flatt T and Kawecki TJ, Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophilamelanogaster. Evolution 61:1980-1991 (2007).
49. Guedes NMP, Tolledo J, Corrêa AS and Guedes RNC, Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophiluszeamais. J Appl Entomol 134:142-148 (2010).
50. Cordeiro EMG, de Moura ILT, Fadini MAM and Guedes RNC, Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Olygonychusilicis? Chemosphere 93:1111-1116 (2013).
51. Parsons PA, Radiation hormesis: an evolutionary expectation and the evidence. Appl Rad Isotopes 41:857-860 (1990).
52. Parsons PA, The hormetic zone: an ecological and evolutionary perspective based upon habitat characteristics and fitness selection. Q Rev Biol 76:459-467 (2001).
53. Stark M, Hormesis, adaptation, and the sandpile model. Crit Rev Toxicol 38:641-644 (2008).
54. Mattson MP, The fundamental role of hormesis in evolution, in Hormesis: A Revolution in Biology, Toxicology and Medicine, ed. by Mattson MP and Calabrese EJ. Springer, New York, pp. 57-68 (2010).
55. Desneux N, Decourtye A and Delpuech J-M, The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81-106 (2007).
56. Ripper WE, Effect of pesticides on balance of arthropod populations. Annu Rev Entomol 1:403-438 (1956).
57. Knutson H, Modifications in fecundity and lifespan of Drosophilamelanogaster Meigen following sublethal exposure to an insecticide. Ann Entomol Soc Am 48:35-39 (1955).
58. Afifi SED and Knutson H, Reproductive potential, longevity, and weight of house flies which survived one insecticidal treatment. J Econ Entomol 49:310-313 (1966).
59. Kilpatrick JW, Schoof JH, Fly production in treated ad untreated privies. Public Health Rep 71:787-796 (1956).
60. Ouye MT and Knutson H, Reproductive potential, longevity, and weight of house flies following treatments of larvae with malathion. J Econ Entomol 50:490-493 (1957).
61. Hunter PE, Cutkomp LK and Kolkaila AM, Reproduction in DDT- and diazinon-treated house flies. J Econ Entomol 11:579-582 (1958).
62. Kuenen DJ, Influence of sublethal doses of DDT upon the multiplication rate of Sitophilusgranaries (Coleoptera: Curculionidae). Entomol Exp Appl 1:147-152 (1958).
63. Saini RS and Cutkomp LK, The effects of DDT and sublethal doses of dicofol on reproduction of the two-spotted spider mite. J Econ Entomol 59:249-253 (1966).
64. Dittrich V, Streibert P and Bathe PA, An old case reopened: mite stimulation by insecticide residues. Environ Entomol 3:534-540 (1974).
65. Fleschner CA and Scriven GT, Effect of soil-type and DDT on ovipositional response of Chrysopacalifornica (Coq.). J Econ Entomol 50:221-222 (1957).
66. Atallah YH and Newson LL, Ecological and nutritional studies on Coleomegillamaculate De Geer (Coleoptera: Coccinelidae). III. The effects of DDT, toxaphene, and endrin on the reproductive and survival potentials. J Econ Entomol 59:1181-1187 (1966).
67. Grosch DS and Vacovic LR, Chlorinated hydrocarbon insecticides are not mutagenic in Braconhebetor tests. J Econ Entomol 60:1177-1179 (1967).
68. Farlow RA and Pitre HN, Bioactivity of the post emergent herbicides acifluorfen and bentazon on Geocorispunctipes (Say) (Hemiptera: Lygaeidae). J Econ Entomol 76:200-203 (1983).
69. Yokoyama VY and Pritchard J, Effect of pesticides on mortality, fecundity and egg viability of Geocorispallens (Hemiptera: Lygaedae). J Econ Entomol 77:876-879 (1984).
70. Magalhães LC, Guedes RNC, Oliveira EE and Tuelher ES, Development and reproduction of the predator Podisusdistinctus (Stal) (Heteroptera: Pentatomidae). Neotrop Entomol 31:445-448 (2002).
71. Zanuncio TV, Serrão JE, Zanuncio JC and Guedes RNC, Permethrin-induced hormesis on the predator Supputiuscincticeps (Stal, 1860) (Heteroptera: Pentomidae). Crop Prot 22:941-947 (2003).
72. Croft BA, Arthropod Biological Control Agents and Pesticides. Wiley, New York (1990).
73. Gil LI and Gill SS, Insect Control: Biological and Synthetic Agents. Academic Press, London (2010).
74. Szczepaniec A and Raupp MJ, Effects of imidacloprid on spider mite (Acari: Tetranychidae) abundance and associated injury to boxwoods. Arboric Urban For 38:37-39 (2012).
75. Szczepaniec A and Raupp MJ, Direct and indirect effects of imidacloprid on fecundity and abundance of Eutetranychusbuxi (Acari: Tetranychidae) on boxwoods. Exp Appl Acarol 59:307-318 (2013).
76. Casida JE and Durkin KA, Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99-117 (2013).
77. Duke SO, Cedergreen N, Velini D and Belz RG, Hormesis: is it an important factor in herbicide use and allelopathy? Outlooks Pest Manag 17:29-33 (2006).
78. Cedergreen N, Streibig JC, Kudsk P, Mathiassen SK and Duke SO, The occurrence of hormesis in plants and algae. Dose-Response 5:150-162 (2007).
79. Cooper J and Dobson H, The benefits of pesticides to mankind and the environment. Crop Prot 26:1337-1348 (2007).
80. Edwards-Jones G, Do benefits accrue to 'pest control' or 'pesticides'?: a comment on Cooper and Dobson. Crop Prot 27:965-967 (2008).
81. Matsumura F, Contemporary issues on pesticide safety. J Pestic Sci 29:299-303 (2004).
82. Matthews GA, Attitudes and behaviours regarding use of crop protection products - a survey of more than 8500 smallholders in 26 countries. Crop Prot 27:834-846 (2007).
83. Pickett AD, A critique on insect chemical control methods. Can Entomol 81:67-76 (1949).
84. Metcalf RL, Changing role of insecticides in crop protection. Annu Rev Entomol 25:219-256 (1980).
85. Hardin MR, Benrey B, Colt M, Lamp W, Roderick GK and Barbosa P, Arthropod pest resurgence: an overview of potential mechanisms. Crop Prot 14:3-18 (1995).
86. Doutt RL, Smith RF, The pesticide syndrome - diagnosis and suggested prophylaxis, in Biological Control, ed. by Huffaker CB. Plenum, New York, pp. 3-15 (1971).
87. Pedigo LP, Entomology and Pest Management. MacMillam, New York (1989).
88. DeBach P, Rosen D, Biological Control by Natural Enemies. Cambridge University Press, New York (1991).
89. Georghiou GP, The evolution of resistance to pesticides. Annu Rev Entomol 3:133-168 (1972).
90. Battsten LB, Holyoke Jr. CW, Leeper JR and Raffa KF, Insecticide resistance: challenge to pest management and basic research. Science 231:1255-1260 (1986).
91. Whalon ME, Mota-Sanchez D, Hollingworth RM, Global Pesticide Resistance in Arthropods. CABI, Wallingford, UK (2008).
92. Hemingway J, Vontas J, Poupardin R, Raman J, Lines J, Schwabe C etal, Country-level operational implementations of the Global Plan for Insecticide Resistance Management. Proc Natl Acad Sci USA 110:9397-9402 (2013).
93. Oakeshott JG, Farnsworth CA, East PD, Scott C, Ha Y, Wu Y, etal, How many genetic options for evolving insecticide resistance in heliothine and spodopteran pests? Pest Manag Sci 69:889-896 (2013).
94. Sota N, Motoyama N, Fujisaki K and Nakasuji F, Possible amplification of insecticide hormoligosis from resistance in the diamondback moth, Plutellaxylostella (Lepidoptera: Yponomeutidae). Appl Entomol Zool 33: 435-440 (1998).
95. Veloso RVS, Proteômica Diferencial em Populações de Sitophiluszeamais (Motschulsky, Coleoptera: Curculionidae) mediante expressão do fenômeno hormese. DS Dissertation, Univ. Fed. Viçosa, Brazil (2012).
96. Terriere LC, Induction of detoxification enzymes in insects. Annu Rev Entomol 29:71-88 (1984).
97. Yu SJ, Host plant induction of microsomal monooxygenases in relation to organophosphate activation in fall armyworm larvae. Fl Entomol 69:579-587 (1984).
98. Mukherjee SN, Rawal SK, Ghumare SS and Sharma RN, Hormetic concentrations of azadirachtin and isoesterase profiles in Triboliumcastaneum (Herbst) (Coleoptera: Tenebrionidae). Experientia 49:557-560 (1993).
99. Vaiserman AM, Hormesis and epigenetics: is there a link? Ageing Res Rev 10:413-421 (2011).
100. Chelliah S and Heinrichs EA. 1980. Factors affecting insecticide-induced resurgence of the brown planthopper, Nilaparvatalugens, on rice. Environ Entomol 9:773-777.
101. Lowery DT and Sears MK. 1986. Stimulation of reproduction of the green peach aphid (Homoptera: Aphididae) by azinphosmethyl applied to potato. J Econ Entomol 79:1530-1533.
102. Morse JG and Zareh N. 1991. Pesticide-induced hormoligosis of citrus thrips (Thysanoptera: Thripidae) fecundity. J Econ Entomol 84:1169-1174.
103. Belz RG, Cedergreen N and Sørensen H, Hormesis in mixtures - can it be predicted? Sci Total Environ 404:77-87 (2008).
104. Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP and Raupp MJ, Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PLoS ONE 6, e20018 (2011).
105. Paperiello CJ, Risk assessment and risk management implications of hormesis. J Appl Toxicol 20:147-148 (2000).
106. Feinendegen LE, Evidence for beneficial low level radiation effects and radiation hormesis. Br J Radiol 78:3-7 (2005).
107. Sarup P and Loeschcke V, Life extension and the position of the hormetic zone depends on sex and genetic background in Drosophilamelanogaster. Biogerontology 12:109-117 (2011).
108. López-Martínez G and Hahn DA, Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irraditation and enhances male sexual performance in the Caribbean fruit fly, Anastrephasuspense. J Exp Biol 215:2150-2161 (2012).
109. Piiroinen S, Lyytinen A and Lindström L, Stress for invasion success? Temperature stress of preceding generations modifies the response to insecticide stress in an invasive pest insect. Evol Appl 6:313-323 (2013).