Pesticide Toxicity To Non Target Organisms Pesticide Toxicity To Parasitoids Exposure, Toxicity and Risk Assessment Meth

Chapter 2
Pesticide Toxicity to Parasitoids: Exposure,

Toxicity and Risk Assessment Methodologies
Abstract Parasitoids occur naturally as well as reared and released against target
pests, which is included as an important component in integrated pest management
(IPM) programme. Mostly parasitoids are host specific and they are exposed to
pesticides directly while spraying or through contaminated host insects or by con-
suming nectar of the crop plants treated with pesticides. Hence, it is essential to
assess the impact of pesticides on natural enemies like parasitoids. Mostly acute
toxicity bioassays are conducted using eggs, immature stages (cocoons/ mummies)
and adults to determine the median lethal concentrations to assess the effect of pes-
ticides. Ingestion toxicity assays are also being carried out since the adult parasit-
oids feeds on the nectar of the flowering plants. Apart from these bioassays, sublethal
studies are also important to assess the chronic effects of pesticides on the fecundity,
adult emergence, host foraging ability, longevity, generation time, sex ratio and
reproduction of parasitoids. In field conditions also, pesticide toxicity on parasitoids
are being assessed by examining their parasitization efficiency. Risk assessment of
insecticides for parasitoids were studied mostly using LC50 values of parasitoids and
the risk quotient was derived based on which the pesticide was categorized from
harmless to dangerous. Thus, the insecticide effective against target pests and selec-
tive to parasitoids can be identified and included in the IPM packages.
1 Importance of Insect Parasitoids
Insect parasitoids play a vital role in suppression of insect pests in agro ecosystem.
Parasitoids are nothing but insects that feed on another insect during different stages
of their life cycle resulting in death of the host organism and after completing its life
cycle it turns to be a free living organism, independent on host. In general, it is
believed by Entomologists that around 10 % insect species alone are known to sci-
ence and also 800,000 species of parasitoids are in existence (http://www.entomol-
ogy.wisc.edu/mbcn/fea506.html). Parasitoids occur in different insect orders;
however majority of them belongs to the orders, Diptera and Hymenoptera.
Hymenoptera (320,000 species) is one of the four hyper diverse insect groups, the
other three are Coleoptera (350,000 species), Lepidoptera (150,000 species) and
Diptera (120,000 species). The success of Hymenoptera is due to their body struc-
ture with small hindwings that are linked to the forewings by the hamuli, the
© Springer Science+Business Media Dordrecht 2016 99

J. Stanley, G. Preetha, Pesticide Toxicity to Non-target Organisms,
DOI 10.1007/978-94-017-7752-0_2
100 2 Pesticide Toxicity to Parasitoids: Exposure, Toxicity and Risk Assessment
haplodiploid sex determination and the parasitoid mode of life (Bonet 2009).
Parasitic wasps are found in the following 12 super families of Hymenoptera:
Orussoidea (70 species), Stephanoidea (100 species), Trigonalyoidea (100 species),
Megalyroidea (100 species), Evanioidea (1200 species), Ceraphronoidea (2000 spe-
cies), Proctotrupoidea (6000 species), Platygastroidea (10,000 species), Cynipoidea
(4000 species), Chalcidoidea (100,000 species), Ichneumonoidea (100,000 spe-
cies), Chrysidoidea (6348 species) and Vespoidea (11,124 species) (Aldrey and
Fontal-Cazalla 1999; Pennacchio and Strand 2006).
Lenteren (1986) stated that more than 80 % of the effective entomophagous
insects are parasitoids, and among the remaining percentage, 17 and 1 % were con-
tributed by predators and pathogens, respectively. He also estimated that 5000 spe-
cies are used in biological control and partial, substantial and complete control was
achieved by 100, 100 and 70 species, respectively. The most effective egg parasit-
oids in pest suppression belong to the families Scelionidae, Mymaridae and
Trichogrammatidae (Greathead 1986).
1.1 Insect Parasitoids
Insect parasitoids are about 64,000, 15,000 and 3400 described species belonging to
the orders Hymenoptera, Diptera and Coleoptera, respectively. The parasitoids are
also seen in the insect orders like Lepidoptera, Neuroptera and Trichoptera (Eggleton
and Belshaw 1992; Godfray 1994). The insect orders comprising parasitoids are
tabulated below.
Order Family Parasitoid Host

Hymenoptera Trichogrammatidae Trichogramma chilonis Lepidopterans
Braconidae Bracon hebetor Lepidopteran pests of stored
products
Ichneumonidae Itoplectis naranyae Lepidopterans
Aphelinidae Eretmocerus mundus Whitefly
Diptera Tachinidae Sturmiopsis inferens Sugar cane shoot borer
Coleoptera Carabidae Ground beetle, Lebia Colorado potato beetle pupae
grandis
Staphylinidae Rove beetle, Aleochara Cabbage maggot
bilineata
Rhipiphoridae Rhipidius sp. Cockroaches
Rhipiceridae Sandalus sp. Cicadas
Meloidae Blister beetle Egg cases of grasshopper
Strepsiptera Halictophagidae Twisted wing insects Bees, wasps, leafhoppers and
planthoppers
Neuroptera Mantispidae Mantid flies Egg sacs of spiders
1 Importance of Insect Parasitoids 101
Major Characteristics of Parasitoids

• Parasitoids are specialized in their choice of host
• They usually destroy their hosts during development
• Usually the parasitoids are smaller than the host
• The female alone searches for the host
• Parasitoid adults are free living while only the immature stages are parasitic
• Eggs or larvae are usually laid in, on, or near host
• Immatures itself almost kill host usually
• Parasitoids require only one host for their development
1.2 Mode of Development of Parasitoids
With respect to the host

(i)
(a) Endoparasitoid: Parasitoids that lives inside their host body and ulti-
mately kills it. e.g. Chelonus blackburni.
(b) Ectoparasitoid: Parasitoids that lives externally on the host body and kills
its host. e.g. Bracon brevicornis.
(ii) Number of immatures per individual host
(a) Solitary parasitoid: A single individual develops in a host. e.g. Chelonus
blackburni on potato tuber moth.
(b) Gregarious parasitoid: Several progeny parasitises a single host. e.g.
Copidosoma koehleri on potato tuber moth.
(iii) With respect to host stage
1. Egg parasitoid: The parasitoids that attack the egg stage of the host. e.g.
Trichogramma chilonis
2. Egg larval parasitoid: The parasitoid that lays the eggs in the eggs of host
insects and the parasitoid larvae develops in the host larva. e.g. Chelonus
blackburni
3. Egg pupal parasitoid: If the parasitoids lay its egg in the host eggs and
emerge our as adult from a host pupa, it is called as egg pupal parasitoid.
e.g. Fopius arisanus of tephritid fruit flies.
4. Larval parasitoid: The parasitoids that attack the larval stage of the host.
e.g. Apanteles spp.
5. Larval pupal parasitoid: Parasitoids lay eggs on the host larvae and come
out as adult from host pupae. e.g. Pleurotropis epilachnae
6. Pupal parasitoid: The parasitoids that attack the pupal stage of the host.
e.g. Brachymeria nephantidis
7. Adult parasitoids: Parasitoids of adult hosts. e.g. Blaesoziphae kellyi
8. Nymphal parasitoids: The parasitoids that attack the nymphal stage of the
host e.g. Epipyrops fuliginosa on nymphs of Idioscopus clypealis.
9. Nymphal adult parasitoids: The parasitoids that lay its eggs on host
nymphs but the parasitoid continues to develop and emerge from the dead
adult host. e.g. Epiricania melanoleuca parasitic on Pyrilla perpusilla.
(iv) With respect to effect of parasitization on host
1. Idiobionts: Those parasitoids in which the development of the host is pre-
vented upon parasitization (e.g. egg parasitoids)
2. Koinobionts: Those parasitoids in which the development of the host is
continued after parasitization (e.g. larval-pupal parasitoids).
(v) With respect to food web relationships
1. Primary parasitoid: Parasitism on a normal host.
2. Secondary parasitoid: The parasitoids develop on the primary parasitoid.
e.g. Opisina arenosella (pest) Bracon brevicornis (primary parasitoid) and
Pleurotropis sp. (secondary parasitoid).
3. Tertiary parasitoid: The parasitoid develops on a secondary parasitoid.
(vi) Number of hosts attacked
(a) Monophagous: Those parasitoids specific to one particular host. e.g. The
ichneumonid parasitoid, Mesolicus tenthredinis is specific for a saw fly.
(b) Oligophagous or Stenophagous: Parasitoids that develops only on closely
related hosts e.g. Exerterus amictoriius parasitizes saw fly of Diprion and
Neodiprion genera.
(c) Polyphagous: Parasitoids parasitizing multiple hosts, e.g. Tachnid fly,
Compsilura concinnata have about 20 hosts.
(vii) Number of host individuals essential for attack
(a) Heteroxenous: Require more than one host e.g. The tachinid, Ceromasla
auricaudata.
(b) Monoxenous: Those parasitoids that need only one host for its develop-
ment, e.g. Drino bohemica, a tachinid parasitoid of European spruce
sawfly.
(viii) Competition among the immature stages
1 . Intraspecific competition: Superparasitism
2. Interspecific competition: Multiple parasitism
1.3 Pest Suppression by Parasitoids
The abundance of natural enemies is an important criterion for short term pest con-
trol than species richness (Duelli and Obrist 2003). But for a long term pest control,
high diversity of natural enemy species is more important than abundance (Bengtsson
et al. 2003; Tilman 1996). Among the wide assemblage of parasitoids, selection of
effective parasitoid from its place of origin for introduction against a target pest is
one of the important strategies for successive pest suppression (Waage and Mills
1992).
The major step in classical biological control program is the selection of right
species of parasitoid for introduction. Most of those parasitoids are from the centre
of origin of the target pest and coevolved along with the pest. In a biocontrol pro-
gram, when the target pest is of exotic origin we prefer importation of natural ene-
mies. Such introductions may not establish in the new places or if so they may not
become pests. But still at certain cases due to the lack of natural enemies for sup-
pressing the pest population, the introduced insect may gain the pest status. When
an introduced insect become a pest, then natural enemies are also have to be
imported (Caltagirone 1981). The control of alfalfa weevil, Hypera postica was suc-
cessfully managed by importing its natural enemies (Bryan et al. 1993). The first
deliberate movement of parasitoids from one location to another was conducted by
C.V. Riley, who distributed parasitoids of the weevil Conotrachelus nenuphar
around the state of Missouri in 1870 (Doutt 1964). The first parasitoid successfully
moved and established from one continent to another, however, was Cotesia
(=Apanteles) glomeratus, which was shipped from England to the United States for
suppression of Pieris rapae by the U.S. Department of Agriculture in 1883 (Riley
1885, 1893).
Augmentation refers to mass culturing and release of natural enemies to increase
its population. Inoculative release is done for Encarsia formosa for the management
of whitefly, Trialeurodes vaporariorum (Hussey and Scopes 1985; Parrella 1990).
Release of Trichogramma is an excellent example of an augmentative method that
has been successful in many agricultural systems. Trichogramma is mass produced
and field released innundatively for decades in biological control programme (Li
1994). Conservation of natural enemies involves actions that preserve and increase
natural enemies by environmental manipulation.
1.4 Feeding Habits of Insect Parasitoids
Host feeding by parasitoid wasps has been regarded as a positive attribute in bio-
logical control point of view. Here, the host insects are get killed due to feeding
along with parasitism (Ueno 1998). The parasitoids feed on the fluids exudating
from the ovipositional wound of the host insect. In some cases, the hosts are killed
by host feeding rather than parasitisation (Heimpel and Collier 1996). Host feeding
resulted in the destruction of the host, or deteriorates its quality for egg laying
(Jervis and Kidd 1986). The indirect benefits may be more important than the imme-
diate cost to offspring. Host feeding is reported to increase the fecundity of the para-
sitoids (Heimpel and Collier 1996) may be supplying essential nutrients (Flanders
1953).
1.5 Major Insect Parasitoids
List of pests controlled by Trichogramma spp.

Parasitoids Pests References
Trichogramma Pine moth, citrus swallow tail Hirose (1986)
dendrolimi Spodptera litura Hamada (1992)
T. exiguum Helicoverpa zea Suh et al. (2000)
T. oleae, T. Olive moth, Prays oleae Blibech et al. (2015)
cacoeciae, T.
bourarachae
T. chilonis Tomato fruitworm, Helicoverpa Usman et al. (2012), Ballal and
armigera Singh (2003), and Puneeth and
Vijayan (2014)
Sugarcane early shoot borer, Chilo Sankar et al. (2014)
infuscatellus; top shoot borer,
Scirpophaga excerptalis
Sugarcane borers, S. excerptalis, C. Hussnain et al. (2007)
infuscatellus, Emmalocera
depresella, Acigona steniellus
Sugarcane stem borer, Muhammad et al. (2012) and
C. Infuscatellus Ahmad et al. (2012)
Cotton bollworms, H. armigera and Masood et al. (2011)
Earias insulana
T. pretiosum Cotton leafworm, Alabama Almeida (2001)
argillacea
H. armigera Ballal and Singh (2003)
Plutella xylostella Vasquez et al. (1997)
T. minutum Codling moth, Cydia pomonella; Pinto et al. (2002)
Oriental fruit moth, Grapholita
molesta
Chilotraea auricilia and Sesamia Saxena (1977)
inferens
T. evanescens P. xylostella Tabone et al. (2010)
Rice stem borer Sherif et al. (2005)
H. armigera Timus and Croitoru (2006) and
El-Wakeil (2007)
European corn borer, Ostrinia Tancik and Cagan (2004)
nubilalis
H. zea Atwa and Atwa (2014)
T. japonicum Scirpophaga incertulas Kim et al. (1986) and Varma
et al. (2013)
T. galloi Sugarcane borer, D. saccharalis Consoli et al. (2001)
Trichogramma spp. Sorghum stem borer, H. armigera Romeis et al. (1999)
Diamond backmoth, P. xylostella Tabone et al. (2002)
T. bactrae P. xylostella Vasquez et al. (1997)
Crop pests controlled by other insect parasitoids

Common
parasitoids Insect prey References
Anaphes iole Tarnished plant bug, Lygus lineolaris Williams III et al. (2003)
Anagrus Brown planthopper, Nilaparvata lugens Wang et al. (2008)
nilaparvatae
Eretmocerus Whitefly, Bemisia tabaci Sohrabi et al. (2014)
mundus
Eretmocerus Aleurothrixus floccosus Tello et al. (2013)
paulistus
Trissolcus Eurygaster integriceps Radjabi (1995) and
grandis Critchley (1998)
Encarsia Trialeurodes vaporariorum Lenteren et al. (1996)
formosa
Aphidius Aphids Prado et al. (2015)
colemani
Aphidius ervi Acyrthosiphon pisum He et al. (2005)
Diaeretiella Brevicoryne brassicae, Aphis craccivora, Saleh (2014)
rapae A. nerii
Tetrastichus Chilotrea infuscatellus Saxena (1977)
schoenobii S. incertulas Kim et al. (1986) and
Varma et al. (2013)
Tetrastichus Sugarcane early shoot borer, C. infuscatellus; Sankar et al. (2014)
howardi top shoot borer, S. excerptalis
Telenomus Scirpophaga nivella Saxena (1977)
dingus S. incertulas Varma et al. (2013)
Telenomus S. incertulas Kim et al. (1986)
rowani
Telenomus spp. C. infuscatellus, Proceras indicus, S. nivella Saxena (1977)
1.6 Biological Efficiency of Parasitoids in Field Conditions
The parasitoids are described as more valuable than predators since they are more
host specific, well adapted and require less food per individual. Parasitoids play a
major role in biological control and the food obtained from flowering plants can
have a positive impact on survival, searchability and rate of parasitism. The most
successful egg parasitoid, Trichogramma species was polyphagous attacking sev-
eral lepidopterans and many others (Thomson and Stinner 1989). Diaz et al. (2012)
suggested that Trichogramma atopovirilia and T. pretiosum might be potential para-
sitoids for the control of Spodoptera frugiperda and Copitarsia decolora, with para-
sitism percentage of 30–60 %, respectively. The studies of Ayvaz et al. (2008)
revealed that one release point as adequate to achieve sufficient parasitisation in
grape plants whereas multiple release points are needed for corn.
The egg parasitoid of Nezara viridula, Trissolcus basalis (Hymenoptera:
Platygastridae) attained greater impact on the hosts, even on multiparasitoid species
(Peri et al. 2014). Encarsia formosa is an effective parasitoid for the control of
greenhouse whiteflies and factors contributing for its success have been identified
by Hoddle et al. (1998). The E. formosa limits the whitefly population growth when
the intrinsic rate of increase is greater than the host’s intrinsic rate of increase. In
corn fields treated by Trichogramma egg parasitoid wasp, the range of egg parasit-
ism of corn stem borer, Ostrinia nubilalis was 10–28 % (Movahedi et al. 2014).
Trichogrammatoidea sp. nr. lutea and T. sp. nr. mwanzai showed higher parasit-
ism compared to several other strains in high-mid and mid-low altitudes, respec-
tively (Kalyebi et al. 2005). Egg parasitoids of vegetable ecosystem consist of
Trichogrammatids (Trichogramma, Trichogrammatoidea) parasitizing on
Lepidoptera, Scelionids (Telenomus, Trissolcus) on Lepidoptera and Heteroptera
and Mymarids on leafhopper and thrips. Trichogramma chilonis is a promising bio
control agent for used against a large number of lepidopteran pests (Krishnamoorthy
2012). Parasitism of European corn borer egg masses was greater in release plots
than in control plots by the egg parasitoid Trichogramma ostriniae (Hoffmann et al.
2006).
The releases of T. bourarachae, T. cordubensis and T. euproctidis have a greater
improvement in the management of lepidopterous pests of olive. Trichogramma
bourarachae was found to be capable in dispersal and foraging (Hegazi et al. 2007).
Studies on the efficacy of inundative releases of T. evanescens for the management
of Maruca vitrata revealed that parasitism increased by 53 and 43 % in release plots,
during dry and rainy season, respectively (Ulrichs and Mewis 2004). The field
release techniques and parasitisation of T. chilonis and T. evanescens on Sitotroga
cerealella, Corcyra cephalonica and Leucinodes orbonalis were also assessed. In
micro-plot technique, T. evanescens parasitized 75.5 and 38.83 % of host eggs by
adult release and paper strip method. In open field condition, T. chilonis parasitized
78.6 and 40.2 % of host eggs by adult release and paper strip method (Chowdhury
et al. 2016).
2 Exposure Routes of Pesticides to Parasitoids
The successful integration of biological control in pest management is based on the

impacts of pesticides on natural enemies (Croft 1990; Johnson and Tabashnik 1999).
The toxic effects of pesticides on natural enemies can be through direct (direct con-
tact with poison) or indirect (via host insect) means. The direct impacts are exhib-
ited as acute mortality or long-term sublethal effects (Johnson and Tabashnik 1999).
The threat due to pesticide exposure on natural enemies not only depends on the
group of pesticides, application methods or mode of action but also with respect to
the development of the parasitoid within the host and its stage. During pesticide
application, the adult parasitoids come into contact directly with the pesticide drop-
lets or they receive the toxin from the treated surfaces while searching hosts
(Longley and Jepson 1996). Parasitoids can be exposed to these residues while feed-
ing on nectar from flowers and contaminated honeydew secreated by toxicated
2 Exposure Routes of Pesticides to Parasitoids 107
insects (Longley and Stark 1996; Stapel et al. 1999). The young ones (immature
stages) may get exposed to pesticides during spray or indirectly through contami-
nated hosts on their development (Suss 1983; Hsiech and Allen 1986; Longley
1999).
2.1 Exposure via Direct Exposure to Spray Droplets
Pesticides on direct sprays may reduce survival of the adult parasitoids and or kill
the individuals while developing inside the hosts (Croft 1990). Spray treatment with
thiacloprid in the field did not show a notable impact on the biocontrol efficiency of
parasitoid fauna in the target crops (Schuld and Schmuck 2000). Fenitrothion, spi-
nosad and milbemectin caused 100 % mortality of Trissolcus nigripedius, an egg
parasitoid of pentatomid bug, Dolycoris baccarum within 24 h both by direct con-
tact and by indirect contact to residues. Thiamethoxam was found to be less suscep-
tible insecticide to the parasitoid, T. nigripedius via topical application or residual
exposure when compared to ingestion toxicity (Lim and Mahmoud 2008).
2.2 E
xposure via Uptake of Residues by Contact
with Contaminated Surfaces
Chlorpyrifos followed by imidacloprid had the highest toxicity to the wasp, A.

nilaparvatae, while insect growth regulators (IGR) had the lowest toxicity through
acute contact toxicity tests (Wang et al. 2008). Reduction in the life time of parasit-
oid species viz., Hyposoter didymator and Chelonus inanitus was observed in the
insecticide treated individuals, irrespective of the route of uptake (residual, topical
and ingestion bioassays on adults), with the exception of C. inanitus adults treated
with imidacloprid (Medina et al. 2008). Two bioassay methods viz., contact of para-
sitoids with fresh and dried residues of the insecticides that were significantly toxic
in the bioassay I were conducted on Opius scabriventris, parasitoid of Liriomyza sp.
The results of bioassay I, among eight insecticides tested, cartap hydrochloride and
abamectin + mineral oil were harmful (Class 4) and deltamethrin was slightly harm-
ful (class 2). Only abamectin + mineral oil were harmful (Class 4) to O. scabriven-
tris in the second bioassay method (Araujo et al. 2015). Although certain
armoured-scale parasitoids may be secluded from residues of neonicotinoids
(Rosenheim and Hoy 1988b), these parasitoids may be exposed to toxic residues
while trying to emerge out of scale (Rill et al. 2008).
2.3 E
xposure via Oral Uptake from Contaminated Food
Sources
The hosts or prey species feed on their host plants and get the toxic products within
them and when the natural enemies feeding on the prey hosts they were exposed to
residues (Cardwell and Gu 2003). Natural enemies may get affected if the active
ingredients get distributed in the flower parts such as petals and sepals also (Hagen
1986). Natural enemies foraging on plant surfaces may be exposed to concentra-
tions of pesticides present in the guttation drops. They get contaminated even via
soil or growing medium (Girolami et al. 2009). Dichlorvos was the most toxic
insecticide, which generated 100 % mortality of Anagrus nilaparvatae 2 h after
treatment through oral toxicity tests. Isoprocarb, imidacloprid and thiamethoxam
were the most toxic insecticides and killed all wasps within 4 h (Wang et al. 2008).
Stapel et al. (2000) reported that the wasp, Microplitis croceipes when fed on extra
floral nectar of cotton treated with imidacloprid reduced foraging ability and lon-
gevity of the parasitoid. Fenitrothion was highly toxic to T. nigripedius when
ingested (Lim and Mahmoud 2008).
3 Effects of Pesticides on Parasitoids in Agroecosystem
The use of non-selective insecticides resulted in the decrease of natural enemies

which bring serious consequences in the pest population dynamics. The negative
effects of pesticides on organisms can be classified as acute and chronic. In the acute
intoxication, results will be concluded after an exposure with a single dose of insec-
ticidal treatment. The symptoms appear very fast for the products extremely or
highly toxic, some hours after the excessive exposure for a shorter period. It may be
mild, moderate or severe, based on the quantum of chemical absorbed (Walker et al.
1978). The sub acute intoxication occurs by moderate or small exposure to products
highly or moderately toxic. The chronic intoxication appears after months or years
and which may be due to moderate exposure to single or multiple toxic products
(Fernandes et al. 2010).
3.1 Acute Toxicity
3.1.1 Median Lethal Values
Acute toxicity tests are based on mortality and observed within shorter time
(Walthall and Stark 1997). The preliminary step in the assessment of toxicity of a
pesticide is determination of median lethal values (the dose that causes 50 % mortal-
ity of the test individuals) which can be expressed as LD50 (lethal dose 50) or LC50
3 Effects of Pesticides on Parasitoids in Agroecosystem 109
Median lethal concentrations of different insecticides to insect parasitoids

Median lethal
concentration
Pesticide Test organism Bioassay (LC50) References
Trichogramma spp.
Imidacloprid Trichogramma chilonis Contact 0.0027 mg a.i./L Preetha et al. (2009)
(adults)
T. ostriniae (adults) Contact 502.13 mg a.i./L Wang et al. (2012)
T. confusum (adults) Contact 752.62 mg a.i./L Wang et al. (2012)
T. cacoeciae (adults) Contact 6.25 ppm Saber (2011)
Thiamethoxam T. chilonis (adults) Contact 0.0014 mg a.i./L Preetha et al. (2009)
T. confusum (adults) Contact 0.24 mg a.i./L Wang et al. 2012
T. japonicum (adults) Contact 0.40 mg a.i./L Wang et al. (2012)
Chlorantraniliprole T. chilonis (adults) Contact 1.95 mg a.i./L Preetha et al. (2009)
Clothianidin T. chilonis (adults) Contact 0.0113 mg a.i./L Preetha et al. (2009)
Pymetrozine T. chilonis (adults) Contact 0.96 mg a.i./L Preetha et al. (2009)
Ethofenprox T. chilonis (adults) Contact 0.0045 mg a.i./L Preetha et al. (2009)
BPMC T. chilonis (adults) Contact 0.03 mg a.i./L Preetha et al. (2009)
Endosulfan T. chilonis (adults) Contact 1.85 mg a.i./L Preetha et al. (2009)
Acephate T. chilonis (adults) Contact 4.47 mg a.i./L Preetha et al. (2009)
Abamectin T. chilonis (adults) Contact 1.72 ppm Madhusudan (2015)
Chlorpyrifos T. chilonis (adults) Contact 11.34 ppm Madhusudan (2015)
Cypermethrin T. chilonis (adults) Contact 1.30 ppm Madhusudan (2015)
Indoxacarb T. chilonis (adults) Contact 176.09 ppm Madhusudan (2015)
Malathion T. chilonis (adults) Contact 1.05 ppm Madhusudan (2015)
Quinalphos T. chilonis (adults) Contact 271.47 ppm Madhusudan (2015)
Spinosad T. chilonis (adults) Contact 2.86 ppm Madhusudan (2015)
Triazophos T. chilonis (adults) Contact 1.29 ppm Madhusudan (2015)
Emamectin T. confusum (adults) Contact 21.76 mg a.i./L Wang et al. (2012)
benzoate
Fenpyroximate T. cacoeciae (adults) Contact 1949 ppm Saber (2011)
Nitenpyram T. confusum (adults) Contact 0.83 mg a.i./L Wang et al. (2012)
Anagrus nilaparvatae
Chlorpyrifos A. nilaparvatae (adults) Contact 0.002 mg a.i./L Wang et al. (2008)
Imidacloprid A. nilaparvatae (adults) Contact 0.021 mg a.i./L
Fipronil A. nilaparvatae (adults) Contact 0.180 mg a.i./L
Methamidophos A. nilaparvatae (adults) Contact 0.191 mg a.i./L
Thiamethoxam A. nilaparvatae (adults) Contact 0.520 mg a.i./L
Isoprocarb A. nilaparvatae (adults) Contact 1.071 mg a.i./L
Triazophos A. nilaparvatae (adults) Contact 1.253 mg a.i./L
Abamectin A. nilaparvatae (adults) Contact 8.499 mg a.i./L
Silafluofen A. nilaparvatae (adults) Contact 14.22 mg a.i./L
Dichlorvos A. nilaparvatae (adults) Contact 15.95 mg a.i./L
(continued)
Median lethal
concentration
Pesticide Test organism Bioassay (LC50) References
Cotesia plutellae
Rynaxypyr C. plutellae (adults) Contact 0.0004 % Halappa et al.
Indoxacarb C. plutellae (adults) Contact 0.0005 % (2012)
Flubendiamide C. plutellae (adults) Contact 0.0006 %
Emamectin C. plutellae (adults) Contact 0.0468 %
benzoate
Spinosad C. plutellae (adults) Contact 0.0475 %
Novaluron C. plutellae (adults) Contact 0.0621 %
Neochrysocharis okazakii
Imidacloprid N. okazakii (adults) Contact 0.0035 mg a.i./L Tran and Ueno
Pymetrozine N. okazakii (adults) Contact 8.7790 mg a.i./L (2012)
Lufenuron N. okazakii (adults) Contact 0.0508 mg a.i./L
Ethofenprox N. okazakii (adults) Contact 0.0085 mg a.i./L
Clothianidin N. okazakii (adults) Contact 0.0231 mg a.i./L
Habrobracon hebetor
Chlorpyrifos H. hebetor (larvae) Contact 3.69 ppm Mahdavi et al.
H. hebetor (adults) Contact 1.75 ppm (2015)
Spinosad H. hebetor (larvae) Contact 151.37 ppm
H. hebetor (adults) Contact 117.37 ppm
H. hebetor (adults – ♀) Residual 15.64 mg a.i./L Dastjerdi et al.
H. hebetor (adults – ♂) Residual 11.73 mg a.i./L (2008)
Profenofos H. hebetor (adults – ♀) Residual 12.44 mg a.i./L
H. hebetor (adults – ♂) Residual 6.91 mg a.i./L
Thiodicarb H. hebetor (adults – ♀) Residual 81.04 mg a.i./L
H. hebetor (adults – ♂) Residual 40.39 mg a.i./L
(lethal concentration 50). These median lethal values are useful in comparing the
toxicities of various chemical products. When the lethal values of a chemical were
found to be lower; it indicates greater toxicity.
3.1.2 Mortality in Laboratory Assays at Field Recommended Dose
3.1.2.1 Trichogramma spp.
Flubendiamide is found to be safe, indoxacarb and lufenuron are mildly toxic, while
spinosad and emamectin are highly toxic to the egg parasitoid, Trichogramma chi-
lonis (Sattar et al. 2011). Fenoxycarb was non-toxic or low toxic to T. evanescens
by not affecting the immature stages and not preventing adult emergence. On the
other hand, a significant reduction in adult emergence and parasitism was caused
by fenvalerate and thus highly toxic. Thiacloprid was slightly toxic (class 2) to
T. evanescens on direct exposure to chemical residues, while, fenvalerate was mod-

erately toxic and the mortality was found to be more than fenoxycarb and thiaclo-
prid tested as direct sprays on the host eggs or by indirect contact to residues in a
glass surface (Abdulhay and Rathi 2014). The parasitisation of T. chilonis was found
to get affected by spinosad (Saljoqi et al. 2012). The adult emergence and parasitiza-
tion of T. chilonis is found to be 90.67 and 85.32 %, respectively when exposed to
the field recommended dose of imidacloprid (25 g a.i./ha) (Preetha et al. 2010).
Imidacloprid, carbosulfan, methamidophos and thiodicarb were toxic to T. chilo-
nis at all concentrations by leaf dip bioassay method. The recommended and higher
doses of acetamiprid and thiamethoxam were found to be moderately harmful and
harmful, respectively whereas, the lower doses were found to be slightly harmful to
T. chilonis. Buprofezin was found to be harmless at all doses (Nasreen et al. 2004).
Imidacloprid was regarded as highly toxic to T. platneri (Brunner et al. 2001). The
least emergence of T. chilonis was observed on exposure to spinosad at all parasit-
ism situations. At 3 HAT (hour after treatment), maximum survival was recorded by
chlorantraniliprole (42 %) followed by lufenuron (36 %) and minimum survival was
observed in emamectin benzoate (18 %) and then by imidacloprid (22 %) (Hussain
et al. 2012).
Emamectin benzoate 1.9 EC affected the adult emergence and survival of T.
chilonis (Hussain et al. 2010). Abamectin was designated as harmful to T. pretiosum
(Carvalho et al. 2003) and it was also reported by Alexandre et al. (2006) as harm-
ful, slightly harmful and moderately harmful to T. pretiosum adults, larvae and
pupae, respectively. Deltamethrin (Decis® 100 mL/ha) and spinosad (Tracer®
20 mL/ha) were found to be moderately harmful and harmless to moderately harm-
ful, respectively to all Trichogramma species. All species of Trichogramma showed
differences in the adult emergence time and parasitism viability. Deltamethrin and
spinosad residues affected parasitism viability 31 and 24 days after the treatment for
almost all the species (Blibech et al. 2015).
Esfenvalerate and spinosad at 7.5 and 24 g/ha were categorized as class 4 (harm-
ful) and chlorfluazuron (10 g/ha), methoxyfenozide (19.2 g/ha), lactofen (165 g/ha),
fomesafen (250 g/ha), fluazifop (125 g/ha), glyphosate (960 g/ha), azoxistrobin +
ciproconazol (60 + 24 g/ha), azoxystrobin (50 g/ha) and myclobutanil (125 g/ha)
were grouped as harmless to all immature stages of T. pretiosum (Bueno et al.
2008). Imidacloprid and fenpyroximate at recommended doses caused 100 and
32 % mortality of T. cacoeciae adults (Saber 2011). Endosulfan and ethofenprox
were reported to be extremely toxic (class 4) to T. pretiosum and T. exiguum.
Triflumuron was identified as selective insecticide to the parasitoids in the eggs of
Ephestia kuehniella, Plutella xylostella and Spodoptera frugiperda (Goulart et al.
2012).
The LC50 values ranged from 1.29 to 2.57 for avermectins, 2.26–14.03 for pyre-
throids and 1.12–239.1 mg a.i./L for neonicotinoids and were found to be less toxic
to T. evanescens and insect growth regulators (IGRs) exhibited lowest toxicity with
the LC50 values of 3383–5650 mg a.i./L (Wang et al. 2014). Naled and chlorfenapyr
recorded 100 and 95 % adult mortality of T. nr. brassicae when directly applied and
exposed to residues within 24 h of treatment (Kapuge et al. 2003). Imidacloprid was
found to be most toxic to T. chilonis, at 30 min, 1, 2 and 6 h after treatment with
their lowest LC50 value of 0.07, 0.03, 0.075 and 0.00004 %, respectively followed by
cypermethrin. Chlorpyrifos and monocrotophos were least toxic to T. chilonis with
its higher LC50 value (Khulbe and Kumar 2015).
3.1.2.2 Anagyrus sp.
Fipronil and α-cypermethrin caused significant acute toxicity of vine mealybug

parasitoids, Anagyrus species near pseudococci and Coccidoxenoides perininutus
(Hymenoptera: Encyrtidae). Buprofezin and mancozeb were non toxic to parasit-
oids. The mortality of parasitoids emerging from mummies was found to be low
which is evident that mummy case serves as a barrier to pesticides (Mgocheki and
Addison 2009). Anagyrus pseudococci (a nectar-feeding wasp) when fed on imida-
cloprid treated buckwheat flowers, after 1 DAT (days after treatment), the survival
was found to be 38 % when compared to untreated flowers (98 %) and which
decreased to 0 and 57 % on treated and untreated flowers, respectively at 7 DAT
(Krischik et al. 2007).
3.1.2.3 Aphidius sp.
Cypermethrin showed a high survival percentage of aphid parasitoid, Aphidius cole-

mani when exposed 72 h after application whereas, chlorpyrifos was extremely
toxic to the parasitoid pupae and adults at all post-spraying introducing periods
(Irshaid and Hasan 2011). Lufenuron was harmless to Aphidius gifuensis through
contact and ingestion toxicity bioassays (Kobori and Amano 2004). The residues of
thiacloprid severely affected Aphidius rhopalosiphi adults whereas, pre-imaginal
stages remained unaffected (Schuld and Schmuck 2000).
3.1.2.4 Chelonus blackburni
Diafenthiuron is moderately harmful to the adults of C. blackburni tested by insec-

ticide coated scintillation vial bioassay causing 86.67 % mortality at the recom-
mended dose of 1.6 g/L. The 48 h LC50 of diafenthiuron was 0.89 g/L (Stanley et al.
2016). The recommended dose of imidacloprid (25 g a.i./ha) caused 56 % mortality
and thus moderately toxic to C. blackburni adults (Preetha et al. 2010). A minimum
adverse effect was found to cause by abamectin on C. blackburni adult emergence
(Sheebajasmine et al. 2008).
3.1.2.5 Bracon spp.
Imidacloprid was found to be toxic to the parasitoid Bracon hebetor, causing 70 %
mortality at 48 h after treatment (HAT) (Preetha et al. 2010). Imidacloprid and thia-
cloprid had least impact on Habrobracon hebetor and could be used along with the
parasitoid in integrated pest management programs (Mahdavi 2013).
3.1.2.6 Diadegma insulare
Tebufenozide and spinosad were non toxic to Diadegma insulare at 24 h and 30 min
after treatment, respectively. However, 100 % mortality was observed at 8 h after
treatment with spinosad (Hill and Foster 2000).
3.1.2.7 Diaeretiella rapae
Phosphomidon, dichlorvos and monocrotophos were harmful to D. rapae causing

100 % mortality followed by methamidophos which was moderately harmful caus-
ing 97 % mortality after 24 h of application in glass plate bioassay method. The adult
parasitoid emergence was reduced by about 9 and 7 %, when directly sprayed on D.
rapae pupae with Dimecron and Nogos, respectively. Monofos and Tamaron reduced
adult parasitoid emergence to 3 % compared to control (78 %) within 1 week of
treatment (Kakakhel et al. 1998). The residues of deltamethrin had lower toxic effect
on D. rapae which could limit populations of Myzus persicae (Desneux et al. 2005).
3.1.2.8 Cotesia plutellae
Indoxacarb (53 mg a.i./L), λ-cyhalothrin (28 mg a.i./L) and spinosad (53 mg a.i./L)
caused 100, 88.5 and 50 % mortalities of C. plutellae adults, respectively. Ten day
old residues of indoxacarb and λ-cyhalothrin caused 39 and 44 % mortality, respec-
tively and spinosad residues of 7 and 10 days old resulted in 24 and 0 % mortality of
C. plutellae adults, respectively (Haseeb et al. 2004).
3.1.2.9 Other Parasitoids
Chlorpyrifos was the most toxic insecticide to four parasitoid species viz., Aphytis
melinus, Eretmocerus eremicus, Encarsia formosa and Gonatocerus ashmeadi
based on LC50 values and among the four test parasitoids, A. melinus was the most
susceptible (Prabhaker et al. 2007). Organophosphate and carbamate insecticides
were highly toxic to apple leaf roller parasitoids, Colpoclypeus florus and
Trichogramma platneri (Hymenoptera: Eulophidae) in topical applications but
foliar residues of some products were non toxic after 7 days. Among the newer
molecules, imidacloprid and abamectin were classified as highly toxic to both para-
sitoids on topical application but were non toxic as 1 day old residues (Brunner et al.
2001). Azadirachtin residues were non toxic to stink bug parasitoid, Trichopoda
pennipes whereas, spinosad was as highly toxic to this parasitoid (Tillman 2008).
When A. nilaparvatae fed with honey contaminated with imidacloprid, the parasit-
ism rates were significantly lower than control (9.58 %) (Liu et al. 2010). Spinetoram,
imidacloprid+cyfluthrin, abamectin and tolfenpyrad caused 100 % mortality in 72 h
of a hymenopteran parasitoid of potato, Tamarixia triozae or tomato psyllid,
Bactericera cockerelli (Hemiptera: Trizoidae) in glass surface residue bioassay
whereas, spinetoram was extremely toxic to T. triozae adults as 15 days old residues
caused 100 % mortality in leaf residue bioassay. Chlorantraniliprole, fenpyroxi-
mate, pymetrozine, spiromesifen and spirotetramat had less adverse effect on T.
triozae adults, tested through glass surface or leaf-residue bioassays. Spinetoram,
abamectin and imidacloprid + cyfluthrin caused 100 % mortality in adults of T.
triozae when taken by ingestion. Tolfenpyrad caused 75.0 % mortality in 12 h,
whereas pymetrozine showed moderate effects on the survival of adults (Liu et al.
2012). Among various treatments, novaluron followed by spinetoram exhibited
lowest parasitoid diversity index (Hemandez et al. 2011).
Aphytis melinus, was not reportedly affected by spirotetramat applied to the host
(California red scale, Aonidiella aurantii) when the parasitoid was in the egg or
larval stage, while the adults on exposure to leaves with residues showed 2 weeks of
moderate reductions in survival (Garcera et al. 2013). Endosulfan, monocrotophos,
profenofos and dimethoate caused 100 % mortality within 1 h in mealybug parasit-
oids, Aenasius bambawalei and A. advena and this was found to be more than
untreated check. Imidacloprid resulted in 100 % mortality of both the sexes of the
parasitoids after 3 h (Nalini and Manickavasagam 2011). Acetamiprid and emamec-
tin benzoate showed less reduction percentages to the parasitoid, Aphytis lepidosa-
phes (Hymenoptera: Aphelinidae) on citrus (Dewer et al. 2012). Organophosphates
proved to be more toxic than pyrethroids or carbamates (Longley 1999). The maxi-
mum recommended field concentration and half the dose of amitraz were found to
be harmful and one-fourth dose was moderately harmful to Encarsia formosa
(Chitgar and Ghadamyari 2012). Abamectin was reported to reduce the survivabil-
ity of larvae and pupae of Hemiptarsenus varicornis and Diglyphus isaea (leafminer
parasitoids) (Bjorksten and Robinson 2005).
3.2 Chronic Toxicity
Apart from lethal toxicity, pesticides may also cause sub lethal toxicity on test indi-
viduals that survived on exposure to the toxic residues. These effects are not much
considered while conducting acute toxicity bioassays (Laskowski 2001). Hence, we
also evaluate chronic exposure studies to assess their toxicity. The mortality of
treated pupae, longevity of emerged adults, fecundity, egg hatchability, per cent
pupation, per cent adult emergence and sex ratio of offspring of T. chilonis were
adversely affected due to exposure to chlorantraniliprole. Duration of life cycle of

the offsprings was not adversely affected by insecticidal treatments (Mallick and
Mandal 2014).
3.3 Persistent Toxicity
Abamectin and pymetrozine are classified as short lived (Class A) as their persis-
tence is <5 days and imidacloprid as slightly persistent (Class B) with persistence
between 5 and 15 days against adult of a thelytokous parasitoid, Lysiphlebus
fabarum (Hymenoptera: Aphidiidae) of Aphis fabae (Sabahi et al. 2009). Cartap
hydrochloride 75 % SG was found to be moderately persistent (16–30 days), chlor-
fenapyr 10 % F and emamectin benzoate 1 % EC as slightly persistent (5–10 days)
against female wasps of C. plutellae using leaf disc bioassay. The synthetic pyre-
throd, permethrin was found to be short lived with toxicity for only less than 5 days
(Haseeb and Amano 2002). Emamectin benzoate and spinosad were moderately
persistent (16–30 days; Class C), indoxacarb was slightly persistent (5–15 days;
Class B) and lufenuron and flubendiamide were short lived (<5 days; Class A)
against T. chilonis adults (Sattar et al. 2011). The pupae of T. bourarachae on expo-
sure to residues on olive leaves caused reduction in the parasitism viability of 35.5 %
and 25.5 % for deltamethrin and spinosad treatment, respectively after 31 days
(Blibech et al. 2015).
Fresh residues of flonicamid, flubendiamide and spirotetramat were harmless to
Aphidius ervi and Chelonus inanitus. Residual toxicity of metaflumizone was mod-
erately persistent and persistent to C. inanitus and A. ervi, respectively. However,
deltamethrin was slightly persistent and persistent, respectively for A. ervi and C.
inanitus (Medina et al. 2012). The persistent toxicity of endosulfan, monocroto-
phos, cypermethrin and dimethoate on per cent parasitization and emergence of T.
brasiliensis lasted for 9, 9, 5 and 3 days after treatment, respectively (Amandeep
et al. 2012). Dimethoate, phosalone and dichlorvos at 0.05, 0.07 and 0.10 %, respec-
tively were found to be less toxic to adults of Anicetus ceylonensis. Dichlorvos
(0.10 %), methyl demeton (0.05 %) and endosulfan (0.07 %) showed least persis-
tence whereas fenvalerate at 0.01 % and monocrotophos at 0.05 % had higher per-
sistent toxicity to the adult parasitoids (Mani and Krishnamoorthy 1997). The 1-day
residues of lambda-cyhalothrin caused a significant population reduction of
Eretmocerus mundus and found to be harmful from 7 days after introduction (DAI)
until the last evaluation at 38 DAI which was graded as moderately harmful
(Bengochea et al. 2012).
3.4 Sublethal Toxicity
Sublethal toxicity is an important strategy effective against the continuous use of

conventional insecticides which may have lethal and sublethal effects on natural
enemies. Effects of insecticides on natural enemies are mostly determined based on
the results of the acute toxicity bioassays (Desneux et al. 2007). In the field condi-
tions, parasitoids are exposed to a high concentration of pesticide at the time of
application and then the concentration get decreased as the pesticides get degraded.
So, the rates equivalent to the LC50 are usually tested against parasitoids. Insecticides
affect the efficacy of potential natural enemies by interfering with their biological
traits viz., fertility, fecundity, emergence, developmental rates, longevity and also
by modifying behavioural traits. Several authors reported the reduction in the effi-
cacy of parasitoids (Cross et al. 1999; Sterk et al. 1999; Brunner et al. 2001; Kapuge
et al. 2003).
Sublethal effects of insecticides cause the parasitoids to be less effective in para-
sitizing the hosts in field conditions. So, sublethal effects should also be done as
these can be expressed several days after treatment in addition to acute mortalities
(Tipping and Burbutis 1983). The long term sublethal effects normally happen after
24 h of pesticide exposure. Insecticides at sublethal doses can have positive or nega-
tive impact on beneficials (Croft 1977; Elzen 1989; Messing and Croft 1990; Wright
and Verkerk 1995). The positive effects include increased fecundity (Fleschner and
Scriven 1957; Attallah and Newsom 1966), enhanced parasitoid efficiency (Irving
and Wyatt 1973), increase in movement or searching (Dempster 1968; Critchley
1972) and reduction in developmental periods (Adams 1960; Lawrence et al. 1973).
The sublethal effects of various insecticides on different parasitoids are detailed
below.
3.4.1 Fecundity
Bastos et al. (2006) showed that the fecundity of T. pretiosum is highly reduced by
pyrethroids irrespective of the host species, Sitotroga cerealella and Ephestia kue-
hniella. Fecundity of T. pretiosum was found to get reduced by the exposure of
betacyfluthrin and esfenvalerate. The fecundity of parasitoids was found to get
affected by these pyrethroids even for two subsequent generations. The higher con-
centrations of deltamethrin resulted in >50 % reduction in potential fecundity
(Meilin et al. 2012).
3.4.2 Adult Emergence
Fenitrothion and deltamethrin had a significantly reduced the adult emergence of

egg parasitoids, Trissolcus grandis. They also reduced the emergence rates of egg
parasitoid by 18.0 and 34.4 %, respectively on comparison with untreated check
(Saber et al. 2005). Lambda cyhalothrin, thiodicarb, profenofos, cypermethrin, spi-

nosad adversely affected the emergence of Trichogramma from Helicoverpa zea
eggs when exposed as larval, prepupal, or pupal stages. Spinosad and profenofos
were the most toxic products to T. exiguum adult females and then by lambda cyha-
lothrin, cypermethrin and thiodicarb (Suh et al. 2000). Dimethoate reduced the
emergence of D. rapae adults from treated mummies. The Mean number of off-
spring per female ranged between 49.3 and 93.3 for primicarb and pymetrozine,
respectively (Kheradmand et al. 2012). Dimethoate and chlorpyrifos were reported
to cause a reduction in the emergence of parasitoids, Tamarixia radiata (Beloti et al.
2015). Encarsia formosa exposed to pyriproxyfen at various concentrations exhib-
ited different sublethal effects (Liu and Stansly 1997). The Eretmocerus tejanus
pupae treated with buprofezin showed shorter life span of emerging adults than
those treated with water, endosulfan and thiodicarb (Jones et al. 1998).
3.4.3 Host Foraging Ability and Longevity
Reduced foraging ability and longevity was reported in Microplitis croceipes when
fed upon extrafloral nectar from insecticide treated cotton plants (Stapel et al. 2000).
It was also found that the foraging ability of parasitoids was severely affected for
2 days in imidacloprid and 18 days in aldicarb treatment. Elzen (1989) reported that
cotton plants sprayed with fenvalerate-chlordimeform mixture resulted in decrease
in flight activity (indicator of foraging efficiency) of the parasitoid females, M. cro-
ceipes. The odours from some insecticide treated plants may cause avoidance
behaviour in parasitoids and thus affects the effectiveness as biological control
agents.
The survivors of the parasitoid, Aphytis melinus on exposure to carbaryl, exhib-
ited no significant sublethal effects whereas, to organophosphates resulted in
reduced longevity by 73–85 %. A temporary reduction in progeny production was
also found due to OP exposure (Rosenheim and Hoy 1988a). Spinosad caused
100 % mortality of T. chilonis adults within 15 min. of exposure (Saljoqi et al.
2012). The adult longevity of Telenomus busseolae was reported to be affected by
deltamethrin (Bayram et al. 2010), Aphidius ervi (Desneux et al. 2006b) and
Habrobracom hebetor (Sarmadi et al. 2010). The endoparasitoid, Hyposoter didy-
mator when exposed to diflubenzuron decreased female longevity and reduced the
parasitization rate (Schneider et al. 2004). Longevity of Eretmocerus tejanus that
emerged after applications of buprofezin and azinphos-methyl are slightly shorter
(3.32 and 3.09 days) when compared to control (4.25 days) (Jones et al. 1998).
3.4.4 Mobility and Orientation
A significant sublethal effects (arrestment response and walking behavior) of delta-

methrin was found on Trissolcus basalis to a contact kairomone from Nezara virid-
ula (Salerno et al. 2002). The orientation behaviour of A. ervi and D. rapae toward
plants infested with aphids is not altered on exposure of parasitoid to deltamethrin

(Desneux et al. 2006a, b). The walking behaviour of T. chilonis was observed for
3 min, first in absence and then in presence of spinosad (0.005 % and 0.001 %) and
observed that lower distance (16.22 cm) was covered by the parasitoid when treated
with 0.005 % concentration, while it travelled 25.4 cm when treated with 0.001 %
showing that the higher concentrations affect parasitoid behaviour and search abil-
ity (Saljoqi et al. 2012).
3.4.5 Communication
Deltamethrin at sublethal dose exposed to only males induced an increase of the

arrestment of T. brassicae males by the sex pheromone and deltamethrin enhanced
the response of non insecticide-treated males when the treated females emits the
pheromone (Delpuech et al. 1999).
3.4.6 Behaviour
Tebufenozide and gamma-cyhalothrin affected the parasitism of the F0 generation of

Tamarixia radiata, but the effect was not found in next generations (Beloti et al.
2015). When Anagyrus pseudococci fed on buckwheat flowers treated with imida-
cloprid (soil application) altered the behaviour and reduction in the survivorship of
the parasitoid (Krischik et al. 2007).
3.4.7 Generation Time and Sex Ratio of Parasitoids
Hexaflumuron, profenofos and spinosad was found to reduce the generation time of
H. hebetor and also affected its sex ratio (Dastjerdi et al. 2009). Development of
both males and females of parasitoid, Cotesia marginiventris on cotton was delayed
(<1 day) by λ-cyhalothrin, dicrotophos and emamectin benzoate. The lowest sur-
vival was observed in the emamectin benzoate and λ-cyhalothrin treatments
(Ruberson and Roberts 2005). Chlorpyrifos shifted the sex ratio of the parasitoid,
Aphytis melinus offspring toward more males (Rosenheim and Hoy 1988a).
Abamectin irrespective of developmental stage and the exposed parasitoid gen-
eration affected emergence and sex ratio of Trichogramma pretiosum. Abamectin,
lufenuron and primicarb exposed at egg-larval stage had an influence on the adult
female parasitoids by affecting their longevity (Carvalho et al. 2003). The develop-
mental time of Apanteles galleriae reared on cypermethrin treated larvae of Achroia
grisella was increased by more than 50 % when compared to Apanteles galleriae
reared on untreated hosts (Ergin et al. 2007). Fenoxycarb increased larval duration
of Pseudoperichaeta nigrolineata irrespective of doses (Grenier and Plantevin
1990).
3.4.8 Life Table Parameters
Pymetrozine reduced parasitoid’s life table parameters in comparison to the control

and caused 27 % mortality in adult stage (Kheradmand et al. 2012). Saber (2011)
stated that fenpyroximate was compatible with parasitoid, T. cacoeciae; whereas
imidacloprid exhibited toxic effects on parasitoid adults.
3.4.9 Offspring Production
An insect growth regulator, diflubenzuron completely blocks the production of

Colpoclypeus florus offspring thereby causing severe sublethal effects (Brunner
et al. 2001). Methoxyfenozide had small effect on the number of progeny of
Arrhenophagus chionaspidis whereas, clothianidin, acetamiprid and emamectin
benzoate treated progenies never reach the pupal or adult stage (Yoshioka and
Takeda 2006). Chlorpyrifos, carbaryl and thiamethoxam lowered the number of
Tiphia vernalis reaching to cocoon stage and carbaryl and chlorpyrifos also reduced
the number of Popillia japonica larvae parasitized (Oliver et al. 2005).
3.5 Field Toxicity
In field trials, methoxyfenozide showed no impacts on Trichogramma adult emer-

gence from treated parasitized eggs, whereas indoxacarb exhibited <8 % emergence
(Kapuge et al. 2003). Diafenthiuron is relatively less toxic to Trichogramma sp.
(www.bioresources.com/pretisoumchemicals). Acetamiprid and emamectin benzo-
ate showed less reduction percentages to the parasitoid, Aphytis lepidosaphes
(Hymenoptera: Aphelinidae) on citrus (Dewer et al. 2012). Parasitism of aphids by
Aphidius sp. and of pod borers by Argyrophylax sp. (tachinid flies), Phanerotoma
leucobasis and Braunsia kriegeri (braconid) and Pristomerus sp. (ichneumonid)
were significantly reduced by insecticides viz., cypermethrin and dimethoate
(Munyuli et al. 2009). Spinosad at labelled rate was moderately to highly toxic to
Aphelinus mali whereas, other compounds and spinosad at lower dose had no detri-
mental effects. Carbaryl had the greatest residual toxicity to A. mali causing 85 %
mortality at 21 DAP (days after application) and declining to 40 % by 28 days
(Rogers et al. 2011).
The residues of insecticides such as fipronil, spinosad, cyfluthrin etc. were most
deleterious to Anaphes iole (95 %) (Williams III et al. 2003). The effect of abamec-
tin on C. plutellae revealed that abamectin at 9, 11 and 13 g/ha was relatively safer
to the parasitoid populations (Sheebajasmine et al. 2008). Thiacloprid was classified
as a slightly dangerous insecticide to Lysiphlebus fabarum in immature stages
(Purhematy et al. 2013). Under field conditions, fenvalerate 5 EC and chlorpyrifos
48 EC were categorized as moderately harmful (80–99 %), while, flufenoxuron 10
EC was categorized as slightly harmful (30–79 %) according to the IOBC ranking
to Trichogramma evanescens (Mohamed 2015).
4 Methods to Assess Pesticide Toxicity to Parasitoids
Bioassays will be used based on the mode in which the test insect was harmed by
the chemicals. The pesticide selectivity to natural enemies can be estimated through
toxicity bioassays and the methods for assessing the toxicity of insecticides to para-
sitoids are detailed hereunder.
4.1 Acute Contact Toxicity Bioassays
4.1.1 Bioassays with Parasitized Eggs
4.1.1.1 Egg Card Bioassay: Dip Method (Hussain et al. 2010)
In this method, five egg cards containing 40 parasitized host (Sitotroga cerealella)
eggs were dipped in the respective insecticidal treatment for 1 s on 1, 2, 4, 5 and
7 day after oviposition during egg, larval, pre-pupal, early pupal and pupal stage
after ovi-position. The treated egg cards were dried and transferred to small plastic
Petri dish and maintained in the laboratory until parasitoid emergence.
In another experiment by Bueno et al. (2008), the host (Anagasta kuehniella)
eggs (approximately 250 nos) in 1 cm2 card board squares were placed on vials and
newly emerged parasitoids (T. pretiosum) were introduced into the egg card con-
taining vials for 24 h. Later these parasitized egg cards were removed and trans-
ferred to another vials and treated with insecticides at 72 h (eggs), 144 h (larvae) and
192 h (pupae) by dip method and dried for an hour to eliminate excess moisture.
Then the card were transferred to transparent polythene bags and observed for the
emergence of parasitoids from the corresponding treatments.
4.1.1.2 Egg Card Bioassay: Spray Method (Preetha et al. 2010)
The parasitized egg cards (16 × 32 cm) were sprayed using atomizer with insecti-
cides of respective treatments and water was used in the control (Fig. 2.1). After
shade drying for 10 min, three 7 × 2 cm cards, representing three replications were
cut and kept in test tubes. The parasitoids emerged/cm2 area at 24 and 48 h after
treatment (HAT) were recorded. Per cent emergence was calculated as per the for-
mula given below
No. of wasps emerged

Percent emergence = × 100
Total no. of eggs in 1 cm 2

4 Methods to Assess Pesticide Toxicity to Parasitoids 121
Fig. 2.1 Toxicity on emergence and parasitization -egg card bioassay
Fresh eggs were provided to these parasitoids at 6:1 ratio. After 24 and 48 h of
provision of eggs, the parasitized eggs were counted and percent parasitisation
recorded. The eggs appearing black and plumpy were denoted as parasitized eggs.
No. of parasitized eggs

Parasitization (%) = ×100
Total no. of Corcyra eggs
4.1.1.3 Oviposition Preference Test (Saljoqi et al. 2012)
In this bioassay method, the desired insecticidal concentrations were sprayed on the
host eggs (Sitotroga cereallela) and glued on cards each of around 50–100 eggs and
placed on vials containing freshly emerged virgin females of parasitoids (T. chilo-
nis) with individual virgin male and allowed for mating for a day and the females
were left as such till death. Observations were recorded on the number of eggs being
parasitized, number of adults emerged from the parasitized eggs and adult
longevity.
4.1.1.4 Direct Spray on Host Eggs (Abdulhay and Rathi 2014)
In this method, parasitized E. cautella eggs (30 nos) were placed in a Petri dish
containing filter paper (5.5 cm dia.) and sprayed with the respective field recom-
mended insecticidal dose. Filter papers and eggs were shade dried for 1 h and then
30 eggs from each insecticidal treatment and control (water alone) were transferred
individually into plastic vials. Honey solution (50 %) was streaked on the vials and
observations recorded daily on the emergence or death of the adult parasitoids (T.
evanescens). Three parameters viz., parasitisation, parasitoid emergence and the
reduction in capacity of parasitism were evaluated. After 14 days of initial parasit-
ism, a final evaluation was made on the emergence and the reduction in parasitism
capacity was calculated using the formula:
PR = 1 − ( P / p ) × 100 

Where,
PR – Per cent reduction in parasitism
P – average value for each parasitism for insecticide
p – average parasitism rate for the control treatment
4.1.2 Bioassays with Parasitoid Pupae
4.1.2.1 Topical Bioassays (Mgocheki and Addison 2009)
Twenty mummies with parasitoid were selected and placed on sticky tape which
was placed on glass plates. The recommended field concentration of insecticides
were sprayed on the mummies using Potter’s spray tower and the sticky tapes were
allowed to dry for an hour and then sprinkled with fine soil to prevent emerging
parasitoids to come in contact with the residues and also from getting stuck on the
adhesive. The tape was kept in ventilated Petri dish and observed for emergence of
the parasitoids daily and the emerged parasitoids were transferred to ventilated vials
and provided with 50 % honey: water solution.
4.1.2.2 Pesticides Sprayed on Parasitoid Cocoon (Ruberson and Roberts

2005)
In this method, fresh parasitoid cocoons (Cotesia marginiventris cocoons of <12 h

old) were sprayed with the respective insecticidal concentration, air dried and
placed individually in tissue culture tubes and observed daily twice for adult emer-
gence. The emerged adults were paired within the insecticidal treatments and each
pair was placed in a plastic Petri dish streaked with honey as feed. Fifty 24–48 h old
host caterpillar (beet armyworm) were introduced into each Petri dish every day for
the female parasitoid to oviposit them and the previous day released caterpillars
were removed and transferred to diet and kept until parasitoid emergence or pupa-
tion of caterpillar. Assessment was made on wasp fecundity and the ability of the
parasitoids to locate and attack hosts.
4.1.3 Bioassays with Parasitoid Adults
4.1.3.1 Potter’s Spray Tower (Brunner et al. 2001)
In this method, 1–2 (Colpoclypeus florus) and 2–4 day old (Trichogramma platneri)
adult females of parasitoids were used for the tests. Five test insects selected at ran-
dom were anaesthetized with CO2 and placed on filter paper. Test pesticide was
sprayed topically using Potter’s spray tower to the test parasitoids and were trans-
ferred immediately to small Petri dish. Nutrient and moisture sources were given
and mortality was recorded at 48 h after treatment.
4.1.3.2 Preval Sprayer (Tillman 2008)
In this method, the adult insects (T. pennipes) were cooled down in the refrigerator
for 1–2 min. The anesthetized adults were kept in Petri dish and applied topically
with insecticidal solution using Preval sprayer. Then the treated insects were trans-
ferred to clean Petri dish and sugar solution was given as feed. Mortality was
recorded at 1, 24 and 48 h after treatment.
4.1.3.3 Using Exposure Chamber (Mgocheki and Addison 2009)
Exposure chamber is made of two glass plates treated with pesticides (10 × 10 cm)
fitted to a Munger cell (10 × 10 × 2 cm) with six holes (0.8 cm dia.) through the side
of the walls for ventilation. The pesticidal doses were applied to glass plates using
Potter’s spray tower and were air dried. The Munger cells were assembled with
treated glass surfaces facing inwards and the holes covered with fine gauze. The
parasitoids 20 one day old (Coccidoxenoides perminutus) and 1–2 days old
(Anagyrus sp. near pseudococci) were introduced into each cell through the hole left
uncovered and was plugged with cotton wool soaked in 50 % honey-water solution,
as food source. Observations were recorded at 6, 12, 18 and 24 h after
introduction.
4.1.3.4 Using Modified Exposure Chamber (Longley and Jepson 1997a)
Exposure chambers (modified from Mead-Briggs 1992) consisted of two insecti-

cide treated glass plates fitted to a section of plastic drain pipe (10.5 cm dia. and
2.5 cm ht), with five holes (1 cm dia.) for ventilation and covered with fine gauze
leaving one hole as uncovered and through which the parasitoids were released and
plugged with 1:1 honey: water solution soaked cotton wool.
In this bioassay, the glass plates were not sprayed but covered with leaves from
untreated host plants i.e., winter wheat (Tottman and Broad 1987). Leaves with their
adaxial surfaces uppermost were fixed to the glass using adhesive tapes. Different
concentrations of test pesticide solutions were prepared. Treatments were imposed

using Potter’s spray tower and were shade dried for 1 h. The chambers were then
assembled and ten parasitoids (five male and five female) were carefully introduced
to each chamber. A 2 cm wide strip of nontransparent tape was sticked all over the
edges of the glass plate to keep the parasitoids in the illuminated area. Parasitoid
responses were assessed at different intervals upto 24 h after exposure.
In another bioassay, a glass plate (12 × 12 cm) and a glass dish (6 cm dia.) were
sprayed with the field concentration of insecticide. Spray on both glass plate and
dish is to give maximum exposure of parasitoids to pesticide residues. After drying,
the two components were kept together and were sealed by which humidified air
were introduced using hypodermic needles. Individual female Aphidius rhopalosi-
phi were placed inside the exposure chambers for 2, 3, 5, 10, 15, 30 and 45 min and
control chamber for min only. Fifteen test insects were used for each treatment.
After the treatment time, parasitoids were transferred to Petri dish and honey solu-
tion soaked cotton was given as feed. Observations were recorded on the parasitoids
response immediately, 1 h and 24 h after exposure over the following 4 days.
4.1.3.5 Using Exposure Cages (Mahdavi 2013)
The experimental setup has a frame and two glass plates as ceiling and floor. Both
the sides of frame was drilled with five ventilation holes (5 mm in dia.), covered
with black netting. The water tube and food for the wasps are placed on the two
openings in the fourth side of the frame. The glass plates were sprayed with 3 mL
of the field recommended concentrations of test pesticides using a Potter’s spray
tower. The plates were allowed to dry completely for 1 h and ten CO2 anesthetized
young female adults (<24 h old) kept in each exposure cages and the ceiling was
fixed. Honey was placed on a small strip of paper and provided as food for wasps.
The number of dead and alive wasps in each cage was counted at 12, 24, 36 and 48 h
after the treatment.
4.1.3.6 Using Experimental Cages (Sohrabi et al. 2014)
Young adult parasitoids (<24 h old) were exposed to the field-recommended con-
centration of insecticide for assessing the parasitoid functional response. The host
(cucumber) leaves were dipped for 10 s into insecticidal concentrations and into
distilled water for control. After drying for an hour, the treated leaves were placed
in the experimental cage. The experimental cages consisted of round plastic con-
tainers (5.2 cm ht, 4 cm dia.) with four lateral screened holes (1 cm dia.) for ventila-
tion. Leaf discs (4 cm dia.) from treated leaves were placed with their adaxial side
on a layer of 1 % agar. About, 40–50 pairs of young adult parasitoids (Eretmocerus
mundus) were exposed to treated leaves. After 48 h, from the alive females, six
were randomly selected and placed individually to clip cages (4 cm dia.) on fresh,
undipped leaves with different prey densities of 2, 4, 8, 16, 32 and 64 B. tabaci
(second instar nymphs). Wasps were removed after 24 h. Observations were
recorded on the number of parasitized whitefly nymphs with the aid of a stereo-
scopic microscope.
4.1.3.7 Cage Bioassay (Carmo et al. 2010)
The egg masses (150 eggs) of Spodoptera frugiperda parasitized by Telenomus

remus were transferred to glass vials which contains honey droplets on its inner
wall. Then the glass vials were sealed with plastic film and at parasitoid emergence,
glass plates (13 × 13 cm) were sprayed with the respective test chemical and with
distilled water in case of control, ensuring a deposit of 1.25 mg/cm2. After drying,
the plates were set as per Hassan (1992). The parasitoids were exposed to the glass
plates by fitting the vials with parasitoids to the cages. After 24 h, cards with S.
frugiperda egg (400 eggs) were placed inside along with honey feed. A second card
was kept inside the cages 24 h after the first card and then by the third card. Percent
parasitism and parasitoid emergence were assessed.
4.1.3.8 Using Bioassay Chamber (Williams III et al. 2003)
A bioassay chamber was made using a transparent flexible tube of about 2.5 cm dia.
and 3.5 cm long which have holes covered with organdy cloths for ventilation. Two
scintillation vial caps (2.3 cm dia.), containing agar and a leaf disc treated with
insecticides were kept inside the tubing. The abaxial side of the leaf disc formed the
chambers ceiling, while the adaxial side of another leaf disc formed the floor. After
sealing the chambers with dialysis membrane, 25 parasitoids (mixed gender) were
released, inserted the feeding tube and approximately 25 μL of honey solution
added. After a 48 h of exposure, wasps in each chamber were assessed for mortality
using a microscope.
4.1.3.9 Nonchoice and Residual Tests Bioassay (Tello et al. 2013)
In this method, the internal glass surfaces of vials were swabbed with cotton con-
taining insecticide. The vials were allowed to dry for specific periods such as 1, 48
and 96 h and 10–30 adults of parasitoids (Eretmocerus paulistus) were introduced.
The insects were exposed for 12 h and mortality was recorded.
4.1.3.10 T
oxicity Bioassay with Fresh Residues
(Gonzalez-Zamora et al. 2013)
In this method, pesticides were applied to tops and bottoms of Petri dishes with a
Potter’s spray tower which was calibrated to leave 1.5 mg of solution/cm2. Pesticides
were left to dry for an hour, and then six to eight adult females of parasitoid (Aphytis
melinus) that were 24–48 h old were introduced into each Petri dish and honey was
provided as feed. Parasitoid mortality on each Petri dish was evaluated after 24 h.
4.1.3.11 T
oxicity Bioassay with 7-day Old Residues
(Gonzalez-Zamora et al. 2013)
This method is in continuation with the previous bioassay with fresh residues. When
the mortality was 100 % then the insecticide was classified as harmful and when the
mortality was <100 %, they are less harmful. After the insecticides were sprayed on
Petri dishes were kept upside open and covered using filter paper. The experimental
set up was kept at room temperature for 7 days to allow residues to age and evapo-
rate. After this period, six to eight parasitoids (A. melinus) females (24–48 h old)
were introduced in each Petri dish. Honey was given as food. Adult mortality was
evaluated after 24 h.
4.1.3.12 Dry Film Residue Bioassay (Preetha et al. 2009)
Different insecticidal concentrations were prepared in acetone: water (80:20) and

0.5 ml of the respective concentration was coated on glass scintillation vials of
15 mL capacity and dried. The control vials were treated with acetone: water.
Twenty adult wasps just emerging and moving from the parasitized egg cards (T.
chilonis) were allowed in the vial and covered. A muslin cloth was used to cover the
vial and secured with rubber bands. The wasps were removed after 4 h and trans-
ferred to clean test tubes. Observations on mortality was recorded at 24 and 48 h
after treatment.
4.1.3.13 Filter Paper Bioassay (Rogers et al. 2011)
This bioassay procedure consists of a filter paper disc placed into the lid of a Petri
dish with 0.5 mL of pesticide solution applied on the paper and allowed to dry for
20–25 min and water was used for the control. Approximately 30 adult parasitoids
(Aphelinus mali) were collected and used for a replication and then quickly covered
with bottom of the Petri dish and sealed. Mortality was recorded after 16 h.
4.1.3.14 Dipped Surface Residue Bioassay (Hussain et al. 2010)
This bioassay method consists of ventilated glass bioassay chambers (15 cm long
and 4 cm dia.). Filter paper (15 × 10 cm) was dipped in the respective insecticidal
treatments, air dried and put into the glass bioassays chamber. Approximately, 20
newly emerged parasitoid adults (T. chilonis) were released in each bioassay cham-
ber lined with treated filter paper and mortality was recorded after 4 and 24 h.
4.1.3.15 Leaf Disc Bioassay Using Glass Jars (Hill and Foster 2000)
In this bioassay method, leaf discs (8.75 cm in dia.) were taken from uninfested
cabbage plants and were immersed individually in the respective insecticidal con-
centration for 3 s and air dried for 2 h. Control leaves were treated with water.
Treated leaf discs were lined inside the glass jar and ten randomly selected, newly
emerged adult parasitoids (Diadegma insulare) were released into each jar and cov-
ered with nylon netting secured by an elastic band. A 50 % honey solution was
streaked on the net as food source for the parasitoids. Mortality of parasitoids was
recorded at 30 min, 8 and 24 h. In this method leaves are used as substrate in which
pesticides are applied and exposed to parasitoids rather than inert glass surface.
Substrate plays a vital role in determining the contact toxicity of pesticides (Croft
1990; Wright and Verkerk 1995).
4.1.3.16 L
eaf Disc Bioassay in Petri Dish with Agar Beds
(Prabhaker et al. 2007)
In this Petri dish bioassay technique, agar medium was prepared and spread on a
Petri dish to maintain moisture for test leaves (citrus for Gonatocerus ashmeadi and
A. melinus or cotton for Eretmocerus eremicus and Encarsia formosa) for up to
7 days. Freshly excised leaf discs of test plants were dipped in respective insecti-
cidal concentration for 30 s. Treated leaf discs were shade dried for an hour and
placed on the agar beds in the Petri dish. Then 15 respective test insects were
released in each Petri dish. A thin strip of honey was given as feed for the test
insects by smearing on the inner side of the Petri dish lid. Mortality of insects was
recorded at 24 and 48 h for general insecticides and 96 h for the insect growth regu-
lators like buprofezin and pyriproxyfen since there may be delay in mortality
impacts.
4.1.3.17 L
eaf Disc Bioassay Using Disposable Petri Dish
(Aydogdu and Guner 2012)
In this method, the leaves (almond/apple/plum/cherry) were treated with insecti-

cides in 1 mL of application dose, dried and then placed in a disposable Petri plate
(60 mm dia.). Then four alive Itoplectis maculator adults obtained from Archips
rosana larvae were released into the Petri plate and 50 % honey solution soaked cot-
ton was used as food source. Mortality rates were recorded at 1, 2, 4, 8, 12, 16, 20
and 24 h after treatment.
4.1.3.18 Residual Toxicity Bioassay Using Petri Dish (Tillman 2008)
In residual toxicity tests, the insecticidal concentrations were sprayed on the top and
bottom of a Petri dish (100 × 15 mm) using a sprayer and dried for 1 h. After drying,
the test insects (Trichopoda pennipes) were released singly in the Petri dishes. The
test insects were transferred to uncontaminated dishes after the exposure period and
fed with sugar solution. Mortality was recorded at 1, 24 and 48 h after treatment.
In another method given by Abdulhay and Rathi (2014), the lid and bottom of
glass Petri dish (1 cm in depth and 10 cm in dia.) were sprayed with 1 mL of field
recommended concentrations of respective insecticides and water in case of control.
The treated Petri dishes were dried for 2 h and then 20–30 unsexed parasitoid adults
(24–48 h old) were introduced into each Petri dish for 24 h. The mortality was
recorded at 2, 4, 6 and 24 h after treatment.
4.2 Acute Ingestion Toxicity Bioassays
4.2.1 Insecticide Honey Mixture in Glass Cover Slip (Wang et al. 2008)
In this method, plastic Petri dish (3 cm ht and 4.8 cm dia.) drilled with three holes
of 1 cm dia., one at the base and two on the sides and covered with mesh (0.1 mm)
for ventilation was used. Each insecticidal formulation was made to the required
concentration with 10 % honey solution. The honey water mixture alone was used
as control. Droplets of insecticide honey mixture solution was kept in microscopic
glass cover slips and kept in Petri dish as food for the parasitoids. Four droplets
(1 mL each) of were kept on the coverslip as food. Female wasps (Anagrus nilapar-
vatae) of about ten numbers were introduced to each Petri dish. Mortality was
recorded after 1, 2, 4 and 8 h.
4.2.2 Insecticide Sugar Mixture in Feeding Wells (Tillman 2008)
The respective insecticidal concentration was mixed with sugar solution and kept in
feeding wells in Petri dishes and the adult test insects (T. pennipes) that had been
starved for 24 h prior to the assay were placed singly into these feeding wells and
were allowed to feed once. After the insects have taken the treated food, they were
transferred individually into Petri dishes. The time taken for an insect to die after
feeding was recorded if applicable. Mortality was recorded at 24 and 48 h after
treatment.
4.3 Persistent Toxicity
4.3.1 Field-Aged Residues Tested in Laboratory (Rogers et al. 2011)
In this method, the trees (apple) were sprayed with the respective insecticide using
a Knapsack sprayer. The leaves of a similar size from the treatments were collected
on day ‘0’ immediately after the spray deposits had dried and on additional days
after spraying. The leaves from an untreated tree were used for control. The leaves
were collected from the treated trees and the experiment was continued until there
was little toxicity. Thirty test insects (A. mali) adults were exposed to the treated leaf
with residues within a Petri dish for 24 h, after which the insects were assessed for
mortality.
4.3.2 Residual Toxicity Bioassay (Wang et al. 2008)
In this bioassay method, three pots per treatment containing rice plants were sprayed
with insecticides. Treated plants were allowed to dry and leaves were removed from
the respective treatment and a leaf blade of approximate size of 7.0 × 1.0 cm cut out.
Test tubes were taken and 1 % agar medium was poured and allow to get solidify.
About two leaf blades were kept on the agar bed to keep the leaf blade turgid. Ten
adult parasitoids (A. nilaparvatae) were introduced into each tube. Mortality was
recorded after 8 h. The residual toxicity of the insecticides to the adult parasitoids
was periodically assessed on 0, 1, 3 and 7 days after treatment.
4.3.3 Bioassay Using Aged Residue in Petri Dish (Roubos et al. 2014)
In this method, insecticidal treatments were applied to the inner surface of Petri dish
(4.7 cm dia.) bottoms by using a Potter’s precision spray tower. Petri dishes were
allowed to get dry and test insects were introduced. For aged residue experiments,
the Petri dishes were treated and aged in a greenhouse for 0, 3, 7 and 14 days after
treatment. After residues aged for the appropriate period of time, ten adult insects
(mixture of females and males of Aphidius colemani) were introduced into each
Petri dish. Honey solution was smeared on the inner surface of lid along with a cot-
ton wig for water. Mortality of test insect were observed at 24, 48 and 72 h exposure
time.
4.3.4 Clip Cage Bioassay (Longley and Jepson 1997b)
In this bioassay method, the live female parasitoids belonging to Aphidius genus
were kept individually in ventilated clip cages (2 × 1.75 cm) for 24 h before conduct-
ing experiments and are fed with 50 % honey solution. After application of
deltamethrin on wheat leaves and dried for 1 h, ten clip cages, each containing a
single live Aphidius female were placed on randomly selected flag leaves and simi-
larly placed for the control treatment also. Mortality of parasitoids was recorded
after 24 h and the same procedure was repeated on third and fifth day after
application.
4.4 Sublethal Bioassay
4.4.1 Behavioural Test (Desneux et al. 2004)
In this method, the female parasitoids of D. rapae and Aphidius matricariae were
exposed to insecticides for 24 h via glass residual bioassay method. The survivors
of the parasitoids after 24 h were collected and placed individually in Petri dishes
and used for behavioural studies. The parasitoid females were placed individually
on an aphid patch (M. persicae) and observations were recorded using a micro-
scope. Various observations such as antennal contact, antennal examination, sting-
ing attempt and stinging were recorded. The frequency and duration of walking on
and out of aphid patch, grooming and time spent immobile are also noted. The fre-
quencies of these behaviours were recorded using the Observer software. The
observations were recorded on 3–4 females/species/dose till the parasitoid flew
away or left the patch for 60 s.
4.4.2 A
ssessment of Sublethal Effects via Ingestion Toxicity (Wang et al.
2008)
The wasps (A. nilaparvatae) surviving from the ingestion toxicity bioassay method
were removed and transferred to uncontaminated tubes and fed with honey solution.
Equal males for mating were introduced into the tube containing females for an
hour and five females were selected for assessing the sublethal effects like longev-
ity, fecundity and emergence. A single female wasp was allowed to get into a tube
containing a rice stem with approx. 40–50 brown planthopper (BPH) eggs. The
longevity of the wasp was recorded every 12 h. The host eggs and feed were replaced
daily. Observations were recorded on the total number of parasitized eggs and the
rate of emergence.
4.4.3 S
tandard Leslie Matrix Model for Population Growth (Banks et al.
2011)
This model is used to find out the possibility of predicting the impact of pesticides
on a guild of parasitoids by assessing one representative species. A standard Leslie
matrix model (Leslie 1945) was used to represent the population growth through
time. It includes four life stages for four different parasitoid species.
The population growth may be described by the matrix equation 1:
 X1( t + 1)   0 0 0 f 4   x1( t ) 
 X2 ( t + 1)  a1 0 0 0   X2 ( t )
X ( t + 1) =   =  =  = AX ( t )
 X3 ( t + 1)   0 a 2 0 0   X3 ( t ) 
     
 X 4 ( t + 1)  0 0 a3 a 4  X 4 ( t )

xi – the number of individuals in each of the four life stages; i = (1, 2, 3, 4), The
population expressed as a vector X = [x1, x2, x3, x4] T.
ai – the rate survivability to the next stage (0<ai<, i = 1, 2, 3 and 0 ≤ a4 ≤ 1)
f4 – Rate of reproduction of adult.
If the dominant eigenvalue (λ) of the transition matrix (A) > 1 = population will
grow (Caswell 2001; Cushing 1998).
The expression derived relating the dominant eigenvalue to the net reproductive
rate of the population, R0 is the number of progenies produced by an insect in its
lifetime (Banks et al. 2010).
This rate is given by:
f4 a1 a 2 a 3
R0 =
1 − a4
( )
= f4 a1 a 2 a 3 1 + a 4 + a 4 2 + a 4 3 + …

R0 > 1 = growing population.
R0 < 1 = population going to extinction (Dyer et al. 2008).
4.4.4 S
imulation Model to Estimate the Impact of Pesticide Exposure
on Parasitoids (Stark and Bamfo 2002)
In this method, the crucifer leaves each containing batches of 50 mummified

Brevicoryne brassicae were kept on a moistened paper towel in Petri dishes. The
field dose and three different concentrations of field dose (one-half, one-fourth and
one-eighth) were applied using Potter’s spray tower in addition to water for control.
The data was recorded for 2 weeks on the emergence of parasitoid, D. rapae. The
experiment was replicated thrice on different day with different generations of para-
sitoid. To estimate the effects of insecticide exposure on the parasitoid populations,
a simulation model was developed (Leslie 1945; Caswell 1989; Carey 1993).
The primary matrix of the model – the life history characteristics of a parasitoid,
a starting vector, n(t) – information on age distribution of the population multiplied
against the primary matrix resulting in a secondary vector, n(t + 1). Again multiplied
against the matrix, thus could project the growth of population by the time step of
the matrix. The simulation was run twice, once with a starting vector consisting
adults and again with the stable age distribution.
4.4.5 Functional Response Bioassay (Rezaei et al. 2014)
The parasitoids were exposed to sub lethal insecticidal concentration (LC25) employ-
ing glass vial residue bioassay method. Seven parasitoids treated with insecticides
and distilled water was introduced individually to transparent cylindrical containers
(7.5 cm dia.; 8 cm length) containing 4–5 leaf stage canola seedlings infested by
third instar nymphs of Lipaphis erysimi at different densities (2, 4, 6, 8, 16, 32, and
64) having ten replicates each. The parasitoids were removed after 24 h and the
aphids were maintained for about 10 days in order to count the mummies.
To determine the type of functional response,
Na
=
(
exp P0 + P0 N 0 + P0 N 0 2 + P0 N 0 3 )
N 0 1 + exp ( P0 + P0 N 0 + P2 N0 2 + P3 N03 )

(Juliano 2001).
Where,
Na – No. of parasitized hosts
N0 – Initial host density
P0,P1,P2,P3 – Intercept, linear, quadratic and cubic
Type of functional response was determined by examining the sign of P1 and P2.
A negative and positive linear parameter (P1) indicates type II and III, respectively
(Juliano 2001).
To compare the search rates (a) and the handling time (Th) of the parasitoid on
host, the Rogers’ type II random parasitism equation (Rogers 1972) can be fitted.

{ }
N a = N 0 1 − exp  −a ( T − ThN 0 )

Where,
T – Total time (24 h)
a – Attack rate (h − 1)
Th – Time of handling
Pairwise comparisons were made using indicator variable method (Juliano 2001)

{ 
( )( (
N a = N 0 1 − exp  − a + Da ( j) T − Th + DTh( j) ))) Na }
Where,
j – Indicator variable
Da and DTh – the difference between ‘a’ and ‘Th’ parameters in different treat-
ments (Juliano 2001; Allahyari et al. 2004)
4.4.6 T
oxicity Assessment on Immature Parasitoids (Mummies) (Longley
and Jepson 1997a)
Newly emerged female A. rhopalosiphi (mated) were released into the cages con-
taining second instar Sitobion avenae for parasitization for a period of 24 h. The
parasitized aphids were allowed on the barley seedlings for 10 days for mummifica-
tion. Then the leaf sections containing mummies were cut and glued to glass plates.
The mummies used for the experiment was 80 and replicated eight times and treated
with recommended dose and half of recommended dose of insecticides and water
for control. Then the plates were allowed to dry for 1 h and then covered with a lid
of fine mesh gauze and maintained at controlled conditions. Emerging parasitoids
were fed with honey.
The parasitoids emerging were noted and transferred to an untreated chamber
and fed with food and assessed for longevity. For assessing the fecundity, ten sur-
viving females from control and treatment were transferred to potted barley seed-
lings. About 40 S. avenae were introduced on the plants and kept inside the cylinders
of clear acetate sheeting. The plant chambers were maintained at controlled envi-
ronment with constant illumination for 24 h and then the parasitoids were removed.
Observations were recorded on the mummified aphids (Nos) after 12 days. Levene
test was used for testing the homogeneity of variance (Day and Quinn 1989). The
fecundity data was analysed using a two-sample t test.
4.4.7 Egg Card Dip Bioassay (Carvalho et al. 2003)
The newly emerged T. pretiosum females (15 adults) were individualized in glass
tubes and provided with blue paper cards containing UV killed Anagasta kuehniella
eggs for 24 h. The paper cards with eggs were maintained at controlled environment
for the development of T. pretiosum. Eggs of A. kuehniella containing T. pretiosum
at egg larval, pre pupal and pupal with 24, 96 and 192 h after parasitism respectively
were treated by dipping them in the respective insecticidal solution for 5 s and after
elimination of excess moisture, paper cards were individualized in glass tubes. Then
15 newly emerged females were selected at random from treated F1 generation eggs
from each treatment, individualized in glass tubes and provided with non-treated
and inviabilized eggs of A. kuehniella for 48 h for assessing the pesticide impacts in
the next generation. The following parameters were evaluated.
1 . The number of eggs parasitized by F1 generation insects
2. Emergence of parasitoid in F1 and F2 generations
3. The parasitoid sex ratio in the egg-larval, prepupal and pupal stages
4. The F1 female longevity.
A paper card containing about 125 parasitized host eggs constitute the experi-
mental unit. The comparisons between treatments were analysed by Scott and
Knott’s groupment analysis test at 5 % probability (Scott and Knott 1974).
4.4.8 A
ssessment of Longevity, Progeny Production, Size and Sex Ratio
(Rosenheim and Hoy 1988a)
In this method, young female parasitoids (Aphytis melinus) were exposed to pesti-
cides for 24 h that would cause about 50 % mortality. Afterwards the live A. melinus
parasitoids were removed and provided with host insects (Aspidiotus nerii), to
assess their longevity, progeny production and sex ratio of their offspring. On day 1,
adult parasitoids were allowed to emerge from parasitized Aspidiotus nerii by keep-
ing them in an emergence cage. The emerged parasitoids were given with honey as
food. On the day after parasitoid emergence, the host materials were removed and
the parasitoids allowed for mating. On day 3, plastic cups (30 mL) capped with
gauze which was dipped for 5 s into the insecticidal solution and air dried, were
used as exposure surface. Approximately ten female of A. melinus, were added to
each plastic cups with treated guaze. The vials were held for 24 h under constant
light and observations recorded. A total of ten surviving females from treatment and
control were transferred to glass jar containing mature oleander scales for parasitoid
oviposition. Mortality was assessed on every successive day and the dead parasit-
oids were removed daily and honey solution given as food. This procedure was
continued till the death of all parasitoids. Potatoes removed from the glass jars were
maintained for parasitoid development and emergence.
The development rate of the parasitoid, A. melinus was studied by keeping 20
female parasitoids with excess A. nerii for oviposition for 24 h. The parasitoids
were removed and the host insects monitored daily for parasitoid emergence until
21 days. All the parasitoids emerged were collected, counted and sex determined.
Parasitoids were mounted on slides according to the procedure given by Rosen and
DeBach (1979). Hind tibial length was also measured under micrometer as an index
of parasitoid size.
4.4.9 Sublethal Effect Bioassay (Jones et al. 1998)
In this experiment, about 50 Bemisia argentifolii adults were confined on the abax-
ial side of a sweet potato leaf with the help of a 23 mm dia. clip cage for 4–5 h for
egg laying. After 3 days, two female parasitoids (already mated) were confined in
this experimental leaves for 8 h to allow parasitisation. After 5 days of parasitisation
(parasitoids in first larval stage), the leaves were sprayed with test insecticides. The
sprayed leaves were excised and kept in the experimental unit for parasitoid emer-
gence. The experimental unit consists of 60/150 × 25 mm tissue culture dish covered
on top with organdy for ventilation. Another spray was given to other plants at
12 days after parasitisation (parasitoid at pupal stage).
On the 15th day of parasitisation, healthy parasitoid pupae were collected individu-
ally and kept in small capsules containing a droplet of pure honey for assessing the
parasitoid emergence. Mating and reproduction of the survivors of the pupal spray
treatment was assessed. Parasitoids were paired according to the treatment and allowed
for mating. Each pair was then allowed in culture dish containing 200–300 IInd instar
B. argentifolii in a leaf. The progeny production was assessed, counted and sexed.
5 Pesticide Risk Assessment for Parasitoids 135
4.4.10 B
ioassay to Measure Host Foraging Ability Using Wind Tunnel
(Stapel et al. 2000)
In this method, the parasitoid, Microplites croceipes females starved for 2 days were
allowed individually to feed on 2 μL extrafloral nectar droplet collected after insec-
ticidal treatment until satiation. The wasps were transferred individually to glass
vials with honey/water solution. The next day, they were exposed to hosts and frass
individually and made them to sting once before evaluating their flight response. To
stimulate a flight response in the wind tunnel, a cotton leaf fed overnight by
Helicoverpa zea was placed upwind and wasps were released 1 m downwind indi-
vidually. The response of wasps was recorded if it initiates the flight within 5 min.
and those landing on leaf. Actually for completion of flight three chances were
given. After completion of wind tunnel experiments, longevity was assessed by
exposing the wasps individually into vials with honey/water solution.
4.4.11 W
alking Behaviour in Response to Chemical Stimuli (Saljoqi et al.
2012)
Walking behavior of the parasitoid, Trichogramma chilonis is determined with the

help of computer based software. Different sizes of grids were made on an arena
and the parasitoid wasps were set free to walk over these grids. The accuracy of the
result depends upon the size of the grids as smaller the grids size, result will be
accurate and the grids were numbered. A transparent cover slips of length 5 cm and
width 6 cm having very thin boundaries was used for avoiding the escape of wasps.
The test insecticide was sprayed evenly on the adult parasitoids in different insecti-
cidal concentrations and also control with water. The same procedure was carried
out without insecticide also. The software was started as soon as the insect start
moving on the grid and numbers of those grids were entered in the computer from
which the wasp passed away and the observation was recorded for 3 min.
5 Pesticide Risk Assessment for Parasitoids
Parasitoids are considered as the most effective natural enemy for biological control
of insect pests (Murdoch 1994). However, many of the parasitoid populations are be
susceptible to chemical pesticides (Theiling and Croft 1998) and thus can’t be inte-
grated. The toxicity effects can be studied through laboratory toxicity studies, field
safety of insecticides to parasitoids and also risk assessment methods. Risk quotient
is a good indicator for evaluating the safety of insecticides to natural enemies in the
field (Stark et al. 1995). Risk quotient is used for assessing the risk of pesticides to
non-targets (Campbell et al. 2000) and can be used as an indicator of ecological risk
(Peterson 2006). Risk quotient is used to assess the safety of pesticides to parasit-
oids such as Bracon hebetor (Danfa et al. 1998), Trichogramma cacoeciae (Hassan
et al. 1998) and T. chilonis (Preetha et al. 2009).
Pesticide risk assessment to biocontrol agents and natural enemies should be

assessed scientifically and the safer insecticide molecules can be identified and its
compatibility with IPM can be determined (Stark et al. 1995; Jepson and Croft
1998). Low or no toxic effect levels are to be estimated to study the risk of pesti-
cides to beneficial organisms (Leeuwen and Hermens 1995; Koojman et al. 1996;
Bruijn and Hof 1997; Hoeven 1997). Some of the pesticide risk assessment methods
available for parasitoids are given below
5.1 Risk Assessment Methodologies
5.1.1 Risk Assessment Based on Mortality (Miyata et al. 2001)
Dry film residue bioassay method was adopted for assessing the mortality of para-
sitoid adults. The insecticides are categorized based on mortality percentage as
follows:
Mortality Category
<50 % Harmless
50–79 % Slightly harmful
80–99 % Moderately harmful
>99 % Harmful
In topical application method using Potter’s spray tower conducted by Brunner

et al. (2001), the insecticides were graded based on the corrected mortality of the
parasitoid as follows:
<20 % – low toxicity
>20 % and <70 % – moderate toxicity
>70 % – highly toxic.
5.1.2 R
isk Assessment Based on the Reduction in Parasitism (Abdulhay
and Rathi 2014)
In the residual acute toxicity bioassay method, according to IOBC criteria

(Grutzmacher et al. 2004), classified the insecticide as follows:
Class Reduction in parasitisation capacity Category

I <30 % Non-toxic
II 30–79 % Slightly toxic
III 80–99 % Moderately toxic
IV >99 % Toxic
5.1.3 Risk Quotient (Preetha et al. 2009)
Risk quotients can be estimated from the LC50 values based on the formula given
below. The LC50 values at 48 h after treatment are usually used for calculating the
risk quotient.
Recommended field rate g a.i. / ha

Risk quotient =
LC50 of beneficial insect mg a.i. / L

Risk
quotient Category
<50 Harmless
50–2500 Slightly to moderately toxic
>2500 Dangerous
5.1.4 Environmental Impact Quotient (EIQ) (Biddinger et al. 2014)
The environmental impacts of reduced-risk and conventional insecticides were

compared by EIQ analysis which is calculated as follows:
EIQ Field Rating = ∑ ( EIQi * RTi * APi )

Where,
EIQi = EIQ value of pesticide i
RTi = rate of pesticide i
APi = number of applications of pesticide i
5.1.5 T
iered Approach for Risk Assessment (Miles and Alix 2012; http://
www.pesticides.gov.uk)
In Tier I or laboratory tests, the parasitoids are usually exposed to pesticide residues
through glass plates. The Tier I, Hazard Quotient (HQ) was calculated using median
lethal rate (LR50) values for the parasitoids. Tier II tests for parasitoids are done by
exposing them to pesticide residues on leaf surface and mortality assessed. In the
Tier II risk assessment, a 50 % effect trigger is applied that is equal to an HQ trigger
of 1 (depending on LR50 values for parasitoids derived from extended laboratory
tests). If the HQ value calculated is well below the trigger value for the parasitoids,
it was concluded that the use was of low risk. For the parasitoids, HQ trigger = 2.
5.2 Risk of Pesticides on Parasitoids
5.2.1 Risk Assessment Based on Acute Toxicity
Organophosphates and carbamates showed high toxicity to Trichogramma confu-

sum with LC50 values ranging from 0.037 to 0.29 and from 0.17 to 1.61 mg a.i./L,
respectively. Among the seven different classes of insecticides, the least toxicity
was exhibited by insect growth regulators with LC50 values ranging from 3907 to
10,154 mg a.i./L. Based on risk quotient analysis, the neonicotinoids tested except
thiamethoxam, pyrethroids and phenylpyrazoles are reported safe to T. confusum.
Avermectins and IGRs were also found safer to the parasitoids. Organophosphates
and carbamates tested are either slightly to moderately toxic or highly toxic (Wang
et al. 2013).
The median lethal concentration of thiamethoxam was 0.0014 mg a.i./L to T.
chilonis and reported as highly toxic followed by imidacloprid (0.0027 mg a.i./L)
tested on insecticide coated vial (scintillation) residue bioassay. The values of
acephate and endosulfan showed lower toxicity with an LC50 of 4.4703 and
1.8501 mg a.i./L, respectively. Based on risk quotient, among the tested chemicals
chlorantraniliprole was harmless and the remaining insecticides viz., thiameth-
oxam, imidacloprid, ethofenprox and BPMC were dangerous to T. chilonis (Preetha
et al. 2009).
Organophosphates viz., chlorpyrifos, fenitrothion, phoxim, profenofos and tri-
azophos and carbamates viz., carbaryl, carbsulfan, isoprocarb, metolcarb, and
primicarb are found to exhibit high toxicity to T. japonicum, with an LC50 of 0.035–
0.49 mg a.i./L, followed by antibiotics (abamectin, ivermectin and emamectin),
phenylpyrazoles (ethiprole, and fipronil), pyrethroids (cypermethrin, fenpropathrin
and lambda-cyhaothrin), and neonicotinoids (imidaclothiz, nitenpyram, thiacloprid,
acetamiprid, imidacloprid and thiamethoxam). The insect growth regulators like
hexaflumuron, tebufenozide, chlorfluazuron and fufenozide are found to be least
toxic to Trichogramma japonicum with an LC50 of 3383–30,206 mg a.i./L by dry
film residue bioassay method. Based on risk quotient analysis, phenylpyrazoles,
pyrethroids, insect growth regulators, neonicotinoids except thiamethoxam and
antibiotics except abamectin are classified as safe to T. japonicum whereas most of
the OPs and carbamates tested were moderately or highly toxic (Zhao et al. 2012).
Organophosphates and carbamates were highly toxic to T. evanescens. Among
the phenylpyrazoles, ethiprole was less toxic. Based on LC50 values, avermectins
(1.29–2.57 mg a.i./L), pyrethroids (2.26–14.03 mg a.i./L) and neonicotinoids (1.12–
239.1 mg a.i./L) were found to be less toxic, whereas insect growth regulators
exhibited a low toxicity to the parasitoid, with very high LC50 values (3383–5650 mg
a.i./L). Based on risk quotient, avermectins, neonicotinoids, pyrethroids and IGRs
are safe or low toxic to the parasitoid, T. evanescens. Phenylpyrazoles except ethip-
role, most of the OPs and carbamates falls on slightly to moderate toxic category or
highly toxic (Wang et al. 2014).
For T. chilonis, lambda cyhalothrin, carbosulfan and indoxacarb were reported to

be dangerous based on risk quotient and bifenthrin, thiamethoxam, imidacloprid,
acetamiprid, pymetrozine and buprofezin were slightly to moderately toxic.
Thiamethoxam, pymetrozine and buprofezin were slightly to moderately toxic to T.
brasiliensis and the remaining insecticides viz., lambda cyhalothrin, carbosulfan,
indoxacarb, imidacloprid and acetamiprid were toxic to this parasitoid
(Shankarganesh et al. 2013). Based on risk quotient analysis, chlorantraniliprole
was reported to be harmless to T. chilonis while thiamethoxam was dangerous
whereas, buprofezin, flubendiamide and spinosad were slightly to moderately toxic
to T. chilonis (Uma 2013). The acute toxicity of abamectin, emamectin benzoate,
indoxacarb and spinosad against T. chilonis revealed that they were less toxic to the
parasitoid and can be recommended for IPM programme. Among the different
methods evaluated, hazard ratio is found to be the best as it accounted for the field
dose as criteria for determining the toxicity of the insecticides tested (Sampathkumar
and Krishnamoorthy 2013).
Tran and Ueno (2012) stated that the LC50 values were 0.0035, 0.0085, 0.0231,
0.0508 and 8.779 mg a.i./L for imidacloprid, ethofenprox, clothianidin, lufenuron,
and pymetrozine, respectively to Neochrysocharis okazakii, leafminer parasitoid on
vegetables. Based on risk quotient, imidacloprid and ethofenprox are highly toxic,
lufenuron and clothianidin were slightly to moderately toxic. Pymetrozine was
reported to be safe to N. okazakii. Among the four parasitoids viz., Diaeretiella
rapae, Psyttalia fletcheri, Diachasmimorpha longicaudata and Fopius arisanus, D.
rapae is far more robust to pesticide exposure (Banks et al. 2011). Fipronil, chlorf-
enapyr and diafenthiuron were reported harmful, whereas, abamectin and cyperme-
thrin as moderately harmful and slightly harmful to Cotesia plutellae adults by dry
film residue bioassay (Miyata et al. 2001).
5.2.2 Tiered Evaluation of Pesticide Toxicity
The median lethal rates (LR50) was reported to be much higher at Tier II than at Tier
I but the ranking of LR50s for the three parasitoids, Aphidius colemani, A. ervi and A.
rhopalosiphi for insecticides viz., dimethoate, λ-cyhalothrin and imidacloprid were
the same at both the tiers. At Tier I, a hazard quotient (HQ) of more than 2, revealed
all the three pesticides as harmful to A. rhopalosiphi. At tier II, dimethoate exceeded
this trigger value of 2 and imidacloprid with HQ 1.9, reveals the need for further test-
ing. Since the median lethal values vary very much between 24 and 48 h data, 48 h
data can be used to find the risk assessments. The probit and logit models were found
to be nicely correlated with each other and thus both can be used for finding out the
median lethal values, provided goodness of fit to be reported. For finding the median
lethal values, a geometric series of doses based on the field recommended dose and
a factor of two can be used (http://www.pesticides.gov.uk). The residues of deltame-
thrin dissipated over 5 days after treatment. Though deltamethrin was reported to
control aphid at very low dose than the recommended field rate, some aphids are
found to survive inside some crop refuges (Longley and Jepson 1997b). So, persis-
tence of chemical should be also taken into consideration while assessing the risk.
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Index
A Bracon
Aenasius B. brevicornis, 101, 102
A. advena, 114 B. hebetor, 100, 113, 135
A. bambawalei, 114 Braunsia kriegeri, 119
Aleochara bilineata, 100
Anagrus nilaparvatae, 105, 107–109, 114,
128–130 C
Anagyrus species near pseudococci, Ceromasla auricaudata, 102
112, 118, 123 Chelonus
Anaphes iole, 105, 119 C. blackburni, 101, 112
Apanteles spp., 101 C. inanitus, 107, 115
A. galleriae, 118 Coccidoxenoides perminutus, 123
Aphelinus mali, 119, 126, 129 Colpoclypeus florus, 113, 119, 123
Aphidius sp., 112, 119 Compsilura concinnata, 102
A. colemani, 105, 112, 129, 139 Copidosoma koehleri, 101
A. ervi, 105, 115, 117, 139 Cotesia
A. gifuensis, 112 C. marginiventris, 118, 122
A. matricariae, 130 C. plutellae, 110, 113, 115,
A. rhopalosiphi, 112, 124, 133, 139 119, 139
Aphytis Cotesia (=Apanteles)
A. lepidosaphes, 114, 119 glomeratus, 103
A. melinus, 113, 114, 117, 118, 126, 127, 134
Argyrophylax sp., 119
Arrhenophagus chionaspidis, 119 D
Diadegma insulare, 113, 127
Diaeretiella rapae, 105, 113, 117, 130,
B 131, 139
Blaesoziphae kellyi, 101 Diglyphus isaea, 114
Brachymeria nephantidis, 101 Drino bohemica, 102
E R
Encarsia formosa, 103, 105, 106, 113, 114, Rhipidius sp., 100
117, 127
Epipyrops fuliginosa, 101
Eretmocerus S
E. eremicus, 113, 127 Sandalus sp., 100
E. mundus, 100, 105, 115, 124 Sturmiopsis inferens, 100
E. paulistus, 105, 125
E. tejanus, 117
Exerterus amictoriius, 102 T
Tamarixia
T. radiata, 117, 118
F T. triozae, 114
Fopius arisanus, 101, 139 Telenomus
T. busseolae, 117
T. dingus, 105
G T. euproctidis, 106
Gonatocerus ashmeadi, 113, 127 T. remus, 125
T. rowani, 105
Tetrastichus
H T. howardi, 105
Habrobracon hebetor, 110, 113, 117, 118 T. schoenobii, 105
Hemiptarsenus varicornis, 114 Tiphia vernalis, 119
Hyposoter didymator, 107, 117 Trichogramma spp., 104, 109–112
T. atopovirilia, 105
T. bourarachae, 104, 106, 115
I T. brasiliensis, 115, 139
Itoplectis T. cacoeciae, 104, 109, 111, 119, 135
I. maculator, 127 T. chilonis, 100, 101, 104, 106,
I. naranyae, 100 109–112, 114, 115, 117, 118,
121, 126, 127, 135,
138, 139
L T. confusum, 109, 138
Lysiphlebus fabarum, 115, 119 T. cordubensis, 106
T. dendrolimi, 104
T. evanescens, 104, 106, 110, 111, 119,
M 122, 138
Mesolicus tenthredinis, 102 T. exiguum, 104, 111, 117
Microplitis croceipes, 108, 117, 135 T. galloi, 104
T. japonicum, 104, 109, 138
T. minutum, 104
N T. oleae, 104
Neochrysocharis okazakii, 110, 139 T. ostriniae, 106
T. platneri, 111, 113, 123
T. pretiosum, 104, 105, 111, 116, 118,
O 120, 133
Opius scabriventris, 107 T. sp. nr. mwanzai, 106
Trichogrammatoidea
T. bactrae, 104
P T. sp. nr. lutea, 106
Phanerotoma leucobasis, 119 Trichopoda pennipes, 114, 123, 128
Pleurotropis epilachnae, 101 Trissolcus
Pleurotropis sp., 102 T. basalis, 105, 117
Pristomerus sp., 119 T. grandis, 105, 116
Pseudoperichaeta nigrolineata, 118 T. nigripedius, 107, 108

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Chapter 2

Pesticide Toxicity to Parasitoids: Exposure,

1 Importance of Insect Parasitoids

© Springer Science+Business Media Dordrecht 2016 99

1.1 Insect Parasitoids

Order Family Parasitoid Host

Major Characteristics of Parasitoids

1.2 Mode of Development of Parasitoids

With respect to the host

1.3 Pest Suppression by Parasitoids

1.4 Feeding Habits of Insect Parasitoids

1.5 Major Insect Parasitoids

List of pests controlled by Trichogramma spp.

Crop pests controlled by other insect parasitoids

1.6 Biological Efficiency of Parasitoids in Field Conditions

2 Exposure Routes of Pesticides to Parasitoids

The successful integration of biological control in pest management is based on the

2.1 Exposure via Direct Exposure to Spray Droplets

Chlorpyrifos followed by imidacloprid had the highest toxicity to the wasp, A.

3 Effects of Pesticides on Parasitoids in Agroecosystem

The use of non-selective insecticides resulted in the decrease of natural enemies

3.1 Acute Toxicity

3.1.1 Median Lethal Values

Median lethal concentrations of different insecticides to insect parasitoids

3.1.2 Mortality in Laboratory Assays at Field Recommended Dose

3.1.2.1 Trichogramma spp.

T. evanescens on direct exposure to chemical residues, while, fenvalerate was mod-

3.1.2.2 Anagyrus sp.

Fipronil and α-cypermethrin caused significant acute toxicity of vine mealybug

3.1.2.3 Aphidius sp.

Cypermethrin showed a high survival percentage of aphid parasitoid, Aphidius cole-

3.1.2.4 Chelonus blackburni

Diafenthiuron is moderately harmful to the adults of C. blackburni tested by insec-

3.1.2.5 Bracon spp.

3.1.2.6 Diadegma insulare

3.1.2.7 Diaeretiella rapae

Phosphomidon, dichlorvos and monocrotophos were harmful to D. rapae causing

3.1.2.8 Cotesia plutellae

3.1.2.9 Other Parasitoids

3.2 Chronic Toxicity

adversely affected due to exposure to chlorantraniliprole. Duration of life cycle of

3.3 Persistent Toxicity

3.4 Sublethal Toxicity

Sublethal toxicity is an important strategy effective against the continuous use of

3.4.2 Adult Emergence

Fenitrothion and deltamethrin had a significantly reduced the adult emergence of

(Saber et al. 2005). Lambda cyhalothrin, thiodicarb, profenofos, cypermethrin, spi-

3.4.3 Host Foraging Ability and Longevity

3.4.4 Mobility and Orientation

A significant sublethal effects (arrestment response and walking behavior) of delta-

plants infested with aphids is not altered on exposure of parasitoid to deltamethrin

Deltamethrin at sublethal dose exposed to only males induced an increase of the

Tebufenozide and gamma-cyhalothrin affected the parasitism of the F0 generation of

3.4.7 Generation Time and Sex Ratio of Parasitoids

3.4.8 Life Table Parameters

Pymetrozine reduced parasitoid’s life table parameters in comparison to the control

3.4.9 Offspring Production

An insect growth regulator, diflubenzuron completely blocks the production of

3.5 Field Toxicity

1 Importance of Insect Parasitoids

1.1 Insect Parasitoids

1.2 Mode of Development of Parasitoids

1.3 Pest Suppression by Parasitoids

1.4 Feeding Habits of Insect Parasitoids

1.5 Major Insect Parasitoids

1.6 Biological Efficiency of Parasitoids in Field Conditions

2 Exposure Routes of Pesticides to Parasitoids

2.1 Exposure via Direct Exposure to Spray Droplets

3 Effects of Pesticides on Parasitoids in Agroecosystem

3.1 Acute Toxicity

3.1.1 Median Lethal Values

3.1.2 Mortality in Laboratory Assays at Field Recommended Dose

3.2 Chronic Toxicity

3.3 Persistent Toxicity

3.4 Sublethal Toxicity

3.4.2 Adult Emergence

3.4.3 Host Foraging Ability and Longevity

3.4.4 Mobility and Orientation

3.4.7 Generation Time and Sex Ratio of Parasitoids

3.4.8 Life Table Parameters

3.4.9 Offspring Production

3.5 Field Toxicity

4 Methods to Assess Pesticide Toxicity to Parasitoids

4.1 Acute Contact Toxicity Bioassays

4.1.1 Bioassays with Parasitized Eggs

4.1.2 Bioassays with Parasitoid Pupae

4.1.3 Bioassays with Parasitoid Adults

4.2 Acute Ingestion Toxicity Bioassays

4.2.2 Insecticide Sugar Mixture in Feeding Wells (Tillman 2008)

4.3 Persistent Toxicity

4.3.1 Field-Aged Residues Tested in Laboratory (Rogers et al. 2011)

4.3.2 Residual Toxicity Bioassay (Wang et al. 2008)

4.3.4 Clip Cage Bioassay (Longley and Jepson 1997b)

4.4 Sublethal Bioassay

4.4.1 Behavioural Test (Desneux et al. 2004)

4.4.5 Functional Response Bioassay (Rezaei et al. 2014)

4.4.7 Egg Card Dip Bioassay (Carvalho et al. 2003)

4.4.9 Sublethal Effect Bioassay (Jones et al. 1998)

5 Pesticide Risk Assessment for Parasitoids

5.1 Risk Assessment Methodologies

5.1.1 Risk Assessment Based on Mortality (Miyata et al. 2001)

5.1.3 Risk Quotient (Preetha et al. 2009)

5.1.4 Environmental Impact Quotient (EIQ) (Biddinger et al. 2014)

5.2 Risk of Pesticides on Parasitoids

5.2.1 Risk Assessment Based on Acute Toxicity

5.2.2 Tiered Evaluation of Pesticide Toxicity