20195--R Tamilselvan 27 June-2020

Indian Journal of Entomology Online published (Preview) DoI No.:

RESISTANCE TO THE WHITEFLY BEMISIA TABACI (GENNADIUS) IN COTTON GENOTYPES

R Tamilselvan*, C A Mahalingam, S Mohankumar** and K Senguttuvan***

Department of Agricultural Entomology; **Department of Biotechnology; ***Department of Cotton, Tamil Nadu Agricultural University, Coimbatore, 641003 *Email: [email protected] (corresponding author)

ABSTRACT

This study on the whiteflyBemisia tabaci (Gennadius) on cotton (Gossypium spp.) evaluates the resistant mechanisms viz., antixenosis, antibiosis and tolerance under free-choice and no-choice conditions. Results reveal that the whiteflies select the host only after initial probing. The genotypes, LRA-5166 and DSC-1501 were the least preferred for oviposition under free-choice condition and reduced the nymphal survival (47.50

and 52.50 days), net reproductive rate (R0) (5.45 and 6.31/ female/ lifetime) and intrinsic rate of increase

(rm) (0.061 and 0.063) under no-choice condition, respectively. These exhibited antixenosis and antibiosis. The genotype CCH-4474 demonstrated tolerance with less reduction in the plant height (20.77%), number of internodes (15.27%) and chlorophyll content (13.44%). The high level of resistance in the genotypes LRA-5166 and DSC-1501 could be exploited for genetic improvement of resistant cotton cultivar.

Key words: Gossypium hirsutum, Bemisia tabaci, antixenosis, antibiosis, tolerance, free choice, no choice, LRA 5166, DSC 1501, CCH 4474, oviposition, nymphal surivival, reproductive rate,

Whitefly Bemisia tabaci (Gennadius) (Hemiptera: overlap each other. However, systematic studies on Aleyrodidae) is a highly polyphagous pest causing these aspects are lacking, and hence this study evaluated substantial losses and occur in more than 600 the antixenosis (ovipositional preference), antibiosis agricultural crops and ornamental plant species (fitness parameters) and overall tolerance capacity of (Vázquez et al., 1996). Whitefly contains species cotton genotypes to whitefly. complexes of 41 distinct populations distributed worldwide (Esterhuizen et al., 2013) with 24 biotypes MATERIALS AND METHODS (Perring, 2001). Furthermore, it is an efficient vector Sixty-three cotton genotypes belonging to G. of >100 plant viruses (Geminiviruses) for many hirsutum were initially screened under field condition. economically important crops and is the sole vector of From these the best performed 19 genotypes were begomoviruses (Gottlieb et al., 2006). India is the third selected for further screening in the glasshouse. Based largest producer of cotton (Gossypium hirsutum L.) and on the damage symptoms (Taggar et al., 2012) and B. tabaci causes an estimated 75% damage to cotton, whitefly count, six (Bunny, CCH-4474, GJHV-517, and its management relies on insecticides, leading to DSC-1501, LRA-5166 and TCH-1819) genotypes with resistance to a wide range of insecticides (Crowder et different level of resistance were selected for evaluating al., 2010). Moreover, chemical control affects non- the mechanisms of resistance. The seeds were procured target organisms and the entire ecosystem (He et al., from Department of Cotton, Tamil Nadu Agricultural 2011; Nash et al., 2010). One of the IPM practice is the University, Coimbatore. The study was conducted use of resistant varieties,Preview as it is environment friendly from November 2016 to April 2017 in the insectary, (Vieira et al., 2011). Plants are naturally having the Department of Agricultural Entomology, Tamil Nadu resistance mechanisms viz., antixenosis, antibiosis Agricultural University, Coimbatore (11o00’58”N, and tolerance against the insect attack (Painter, 1951). 76o55’45”E), with B. tabaci collected from cotton Many studies have been conducted to identify resistant field at Coimbatore and the culture maintained on G. cotton genotypes against whitefly (Toscano et al., 2003) hirsutum) in the glasshouse (28± 1oC, 75-90%RH, light and these rely on the occurrence of antixenosis and photoperiod 12 hr) Old plants were replaced with new few on antibiosis (do Prado et al., 2016). Smith (2005) one, whenever needed. The whiteflies from this culture reported that antixenosis and antibiosis frequently were further used to conduct the experiments. 2 Indian Journal of Entomology Online published (Preview)

Antixenosis mechanism of resistance was analysed For observing the tolerance, changes in plant from the ovipositional preference on the selected six phenology due to whitefly infestation was conducted genotypes under multiple choice test. The genotypes under no-choice condition. The plants of selected were grown in earthen pots (soil: farmyard manure: genotypes were raised in the pots. Two pots of each 1:1) up to a standard 14-leaf stage and placed in a treatment were arranged in greenhouse, out of which screen house to avoid any external infestation and the one served as control (uninfested) and replicated four plants watered daily (Jindal and Dhaliwal, 2009). One times. The plant height and number of nodes of each plant from each genotype represented one replication plant at standardized stage were recorded and the pots and there were four replications. In all, 24 pots (4 pots/ were caged (45x 25 cm dia). On one set of test genotype, genotype) were placed randomly in the greenhouse, @ 150 pairs of whitefly collected from test colonies ten pairs/ plant (240 pairs) were collected from main were released in each cage. Other set of genotypes colony with aspirator and released equidistantly in the served as control. After 45 days, the plant cages were greenhouse. The numbers of adults settled on lower removed, and the plant height and number of nodes surface of top three fully opened leaves were counted in each infested and uninfested plants were counted. after 6 hr of release by tilting the leaves without The chlorophyll content in infested and uninfested disturbing the whiteflies. After three days of release, plants were recorded using SPAD (Soil Plant Analysis eggs were counted on the top three leaves of each plant Development) chlorophyll meter. Data analysis was and subsequently at weekly intervals for 3 weeks. The performed by SPSS 21.0 software. The data were pots were tilted and total leaf areas were examined under subjected to ANOVA test and the means were compared a stereomicroscope (40x) to count the number of eggs using Duncan’s multiple range test after a significant laid on each genotypes. F-test (p = 0.05

The antibiosis in genotypes on whitefly biology, RESULTS AND DISCUSSION fecundity, survival and sex ratio was evaluated. The cotton plants were grown in the same stage as described above. In Plant species vary considerably in their suitability each treatment leaf cage was attached to the lower surface as hosts for arthropods. There are sequence of host of fully opened top leaf @ 1 cage/ plant on 4 cotton plants selection process by the insects which includes habitat as replications. In each leaf cage, three pairs of freshly location, host location, host acceptance, and host use emerged adults from colonies maintained separately in (Bernays and Chapman, 1994). Whiteflies use visual, the screenhouse were confined for egg laying. After 24 olfactory and gustative cues in host plant selection hr, adults were removed along with leaf cages. The leaf (Chermenskaya et al., 2009). portion under each leaf cage was marked and only 40 Antixenosis eggs (10 eggs/ replication) were selected and the rest were removed carefully with a needle and a fine brush. Again, In cotton, the antixenosis mechanism of host plant the leaf cages were attached to the leaves on the marked resistance was evaluated based on the oviposition area to prevent oviposition by B. tabaci from outside and preference of the whiteflies (Jindal and Dhaliwal, the duration and survival of various developmental stages, 2011; Toscano et al., 2003). In free-choice condition, i.e., eggs, nymphal instars, pupae and adult were recorded the settlement of B. tabaci after 6 hr after release and daily using stereomicroscope binocular (40x). ovipositional preference were observed (Table 1). The numbers of whiteflies settled on the lower leaf surface For observing the fecundity, longevity and life table of different cotton genotypes differed significantly. The parameters, a day after the adult emergence, females minimum number of whitefly adults settled on TCH-1819, were separated and confined in a micro cage, clipped to whereas the maximum was recorded on CCH-4474. the under surface of the leafPreview for oviposition. The number The genotypes, LRA-5166 and Bunny were at par with of eggs oviposited were recorded daily and the total life TCH-1819 and the remaining genotypes were at par span of the female observed to calculate their fecundity with CCH-4474. The oviposition preference of whitefly and longevity. Based on the procedures developed by showed significant differences among different genotypes. Birch (1948), and the lifetable parameters viz., gross The genotype DSC-1501 recorded lowest number of reproductive rate (GRR), net reproductive rate (R0), eggs laid during the three consecutive weeks after release intrinsic rate of increase (rm), finite rate of increase (k), with strong antixenosis effect against whitefly whereas population doubling time (t), and mean generation time during the 1st week of release Bunny recorded the highest (T) were calculated. number of eggs and in 2nd and 3rd week TCH-1819 has Resistance to the whiteflyBemisia tabaci (Gennadius) in cotton genotypes 3 R Tamilselvan et al.

the highest. The genotype LRA-5166 was statistically t 5.95 6.62 6.55 8.35 similar to the least preferred genotype DSC-1501 and 11.36 10.99 the genotype CCH-4474 fall in the moderately preferred group. With regard to oviposition preference in free- T 24.41 25.16 27.53 26.75 30.18 26.91 choice condition, initially more whiteflies settled on CCH-4474 and DSC-1501, but these genotypes were

λ least preferred for oviposition. Hence, it was proved 1.110 1.112 1.123 1.087 1.063 1.065 - Intrinsic rate of increase; of rate Intrinsic - m the theory of “appropriate/inappropriate landings” (Finch and Collier, 2000) that the selection of host for m r Lifetable parameters 0.116 0.083 0.104 0.061 0.063 0.106 oviposition is mainly based on initial probing. 0 9.23 6.31 5.45 R Antibiosis 17.14 13.90 18.43 The developmental time and survival of different a d * cb bc cb ab instars are the important parameters to evaluate Total 47.50 80.00 8.239 antibiosis (Cruz et al., 2014). The suitability of the host 75.00 65.00 70.00 52.50 c a a c b * plant to insect pests is based on the developmental time ab and reproduction (Sarfraz et al., 2007). The survival of 82.50 62.50 62.50 82.50 75.00 4.433 Pupae 70.00 the life stages on the six genotypes was significantly a a b b * st ab ab

different except for the egg and 1 instar (Table 1). The rd

3 egg survival ranged from 92.50 to 97.50% in Bunny 68.50 67.50 instar 82.50 90.00 3.712 77.50 81.50 and CCH-4474, respectively (Fig. 1). The genotype a c * bc ab ab abc LRA-5166 recorded low nymphal survival as compared nd 2 Survival % 72.50 92.50 3.490 instar with other test genotypes. The total survival from egg 87.50 80.00 80.00 82.50 to adult emergence was lowest on LRA-5166 (47.50%) a a a a a a NS

st and DSC-1501 (52.50%) which was categorized as 1 90.00 90.00 82.50 87.50 80.00 92.50 instar a resistant genotype whereas highest on TCH-1819 0.266 a a a a a a (80.00%) (Fig. 1). The genotype CCH-4474 also NS -Net reproductive rate in no./ female/ lifetime; T-Generation time (days); r (days); time T-Generation lifetime; female/ no./ in rate reproductive -Net

0 reported having lower percent survival. In LRA-5166 Egg 92.50 97.50 90.00 95.00 92.50 95.00

0.805 and DSC-1501 the nymphal stages of B. tabaci were a d d * cd bc ab reduced and therefore should be considered as strong antibiosis effect acting in these genotypes. Similarly, 9.882 the developmental period of B. tabaci was longer week rd

3 on resistant beans variety (Berlinger, 1986) and the 28.17 ± 0.99 69.00 ± 4.56 72.33 ± 3.02 60.67 ± 2.45 49.17 ± 1.10 40.58 ± 2.14 nymphal period was lower on susceptible than on c a a e b d * resistant genotypes of tomatoes and cucumber (Pai and Shih, 2003). The nymphal mortality of B. tabaci greatly 8.129

week varies depending on the host plant (Latournerie-Moreno nd 2 et al., 2015). According to Baldin and Beneduzzi (2010), 80.33 ± 2.41 43.00 ± 3.93 45.75 ± 1.43 94.42 ± 2.51 58.67 ± 1.63 84.42 ± 1.09 greater nymphal mortality of B. tabaci was on resistant a a a b b b *

in cotton genotypes-Oviposition preference (free-choice test); Survival of immature stages; and life table parameters Cucurbita pepo variety which exhibited high antibiosis levels. 10.049 week st Oviposition/leaf (week after release) 1

B. tabaci No preoviposition period was observed in B. tabaci; 43.33 ± 2.56 27.17 ± 1.69 37.67 ± 1.64 71.08 ± 2.76 67.75 ± 2.94 63.33 ± 1.67

Preview oviposition commenced 24 hr after adult emergence.

a a a b b b * Fecundity varied among the cotton genotypes, with 15.50 14.75 14.50 21.00 19.25 5.956 19.75 the highest fecundity observed on Bunny (59.25±

(No./leaf 0.99 eggs). The lowest fecundity was recorded on after 6 hr) No. settled populations reared on LRA-5166 (27.50± 0.50 eggs) and differed significantly with other genotypes (Fig.

Bunny 2). The fecundity on DSC-1501, CCH-4474, GJHV-517 and TCH-1819 was 32.00± 0.79, 41.50± 2.53, 49.00± Genotypes Table 1. Performance of Table CCH-4474 DSC-1501 LRA-5166 F value GJHV-517 TCH-1819 λ- Finite rate of increase; t- population doubling time (days) Means in a column with the p=same 0.05);letter R not significantly different (DMRT, 2.27 and 57.00± 1.95 eggs, respectively. Adult female

4 Indian Journal of Entomology Online published (Preview)

Fig. 1 Age- specificFig. 1 Age-specific survivorship survivorship (lx) and fecundity (lx) and (m fecundityx) of B. tabaci(mx) of on B. cottontabaci genotypeson cotton genotypes A. Bunny; B. CCHA. Bunny;-4474 B.; C. CCH-4474; GJHV-517 C.; D. GJHV-517; DSC-1501 D.; E. DSC-1501; LRA-5166 E.; F.LRA-5166; TCH-1819 F. TCH-1819

70 Fecundity 14 longevity varied among the genotypes, maximum was observed on TCH-1819 (11.63± 1.21 days) and the least d Longevity d 60 12 on LRA-5166 (6.13±1.42 days). Similarly Jindal et al. c (2007) reported that female longevity and fecundity 50 10 bc significantly differed in whiteflies on resistant and 40 ab 8 susceptible cotton genotypes and also based on host a Days plants (Pai and Shih, 2003). 30 6 Eggs (no.) Eggs Most important fitness parameters factors that can be 20 4 used to assess the resistance to insects are the life table Previewparameters, in particular the intrinsic rate of natural 10 2

increase (rm), the higher rm values indicates increased 0 0 host susceptibility (Goodarzi et al., 2015; Khanamani et al., 2013). The life table parameters of B. tabaci are

shown in the Table 3. The net reproductive rate (R0) of whitefly on Bunny, CCH-4474, GJHV-517, DSC-1501, Genotypes LRA-5166 and TCH-1819 were 17.14, 9.23, 13.90,

Fig. 2. Longevity and fecundity of B. tabaci females on cotton 6.31, 5.45 and 18.43, respectively. The intrinsic rates of genotypes increase (rm) for Bunny, CCH-4474, GJHV-517, DSC- Resistance to the whiteflyBemisia tabaci (Gennadius) in cotton genotypes 5 R Tamilselvan et al.

1501, LRA-5166 and TCH-1819 were 0.116, 0.083, was observed in GJHV-517, followed by TCH-1819. 0.104, 0.061, 0.063 and 0.106, respectively. The finite The reduction in the chlorophyll content of infested rate of increase (λ) was lowest for DSC-1501 (1.063) plants compared to uninfested plants was minimum and highest for Bunny (1.123). The genotype DSC-1501 in LRA-5166 followed by CCH-4474 was rated as recorded higher population doubling time (t) (11.36) and tolerant. These results corroborated with the findings of Generation time (T) (30.18 days) and lower in Bunny. Dhillon et al. (2005), where the number of productive tillers was lower in the sorghum shoot fly (Atherigona Tolerance soccata (Rondani) susceptible genotypes than resistant. Tolerance is a plant response and not an insect Similarly, increased photosynthetic activity and response and also conferred with various plant increased branching or tillering after arthropod injury compensatory mechanisms such as high relative growth in tolerant plants/genotypes of various crops (Aguirre rate and an increased photosynthetic rate (Stinchcombe, et al., 2013; Kamphuis et al., 2013; Qiu et al., 2011). 2002). Frei et al. (2004) stated that the plant height, number of nodes and chlorophyll content are important In the present study, the genotypes DSC-1501 and parameters to study the tolerance mechanism. In the no- LRA-5166 were least preferred for oviposition when choice condition, the effects of 150 pairs of whiteflies B. tabaci adults were given free choice test. These on the plant characteristics (plant height, number of genotypes exhibited increased nymphal and adult nodes and chlorophyll content) are given in Table 4. mortality and also extend the life cycle of the whitefly The reduction in the plant height from control varied that delays the time required for the population to reach from 20.77 to 45.16% with the minimum in CCH-4474, an economic damage threshold and hold antixenosis and making it a tolerant genotype. The height was drastically antibiosis type of resistance. In addition, the genotype reduced in GJHV-517 followed by TCH-1819 and CCH-4474 exhibited tolerance to B. tabaci with Bunny which were susceptible to whitefly. There have increased photosynthetic activity under no-choice test. been significant differences in the number of nodes in Hence, this research can help to develop resistant cotton infested and uninfested plants in the test genotypes. varieties against whitefly in plant breeding programs. The number on CCH-4474 in infested and uninfested REFERENCES plants was approximately the same, suggesting that whitefly infestation had no adverse effect on this Aguirre L M, Cardona C, Miles J W, Sotelo G. 2013. Characterization of resistance to adult spittlebugs (Hemiptera: Cercopidae) in genotype. The maximum reduction in number of nodes Brachiaria spp. Journal of Economic Entomology 106(4): 1871- 1877. Table 4. Effect of B. tabaci on cotton genotypes Baldin E L L, Beneduzzi R A. 2010. Characterization of antibiosis and (for 45 days, no-choice test) antixenosis to the whitefly silverleaf Bemisia tabaci B biotype (Hemiptera: Aleyrodidae) in several squash varieties. Journal of Genotypes Reduction from Decrease in Pest Science 83(3): 223-229. control (%) chlorophyll Berlinger M J. 1986. Host plant resistance to Bemisia tabaci. Agriculture, Plant No. of content Ecosystems and Environment 17(1-2): 69-82. height nodes from control Bernays E A, Chapman R E. 1994. Host-plant selection by phytophagous (%) insects.: 95-165. 31.08b 27.62c 28.53c Bunny Birch L C. 1948. The intrinsic rate of natural increase of an insect (33.79) (31.29) (32.26) population. Journal of Animal Ecology: 15-26. 20.77a 15.27a 13.44a CCH-4474 Chermenskaya T D, Petrova M O, Savelieva E I. 2009. Laboratory and (27.08) (22.92) (21.47) field evaluation of biological active substances of plant origin 45.16c 39.62d 24.84bc against greenhouse whitefly, Trialeurodes vaporariorum Westw. GJHV-517 (42.21) (38.99) (29.72) (Homoptera: Aleyrodidae). Archives of Phytopathology and Plant Protection 42(9): 864-873. b Previewbc b 29.44 23.84 21.15 DSC-1501 (32.84) (29.19) (27.15) Crowder D W, Horowitz A R, De Barro P J, Liu S S, Showalter A M, Kontsedalov S, Khasdan V, Shargal A, Liu J, Carrière Y. 2010. 22.07a 17.60ab 12.01a LRA-5166 Mating behaviour, life history and adaptation to insecticides (27.82) (24.56) (20.26) determine species exclusion between whiteflies. Journal of Animal 34.54b 36.98d 31.32c Ecology 79(3): 563-570. TCH-1819 (35.95) (37.36) (33.95) Cruz P L, Baldin E L L, Maria de Jesus P. 2014. Characterization of F Value 13.841* 11.388* 16.314* antibiosis to the silverleaf whitefly Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in cowpea entries. Journal of Pest Science Means in a column with the same letter not significantly different 87(4): 639-645. (DMRT, p=0.05) 6 Indian Journal of Entomology Online published (Preview)

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(Manuscript Received: March, 2020; Revised: May, 2020; Accepted: May, 2020; Online Published: June, 2020) OnlinePreview published (Preview) in www.entosocindia.org Ref. No. 20195