Estimation and validation of developmental thresholds and thermal requirements for cotton pink bollworm Pectinophora gossypiella

Journal Pre-proof Estimation and validation of developmental thresholds and thermal requirements for cotton pink bollworm Pectinophora gossypiella Hemant Peddu, Babasaheb B. Fand, H.R. Sawai, N.V. Lavhe PII:

S0261-2194(19)30330-8

DOI:

https://doi.org/10.1016/j.cropro.2019.104984

Reference:

JCRP 104984

To appear in:

Crop Protection

Received Date: 6 July 2019 Revised Date:

8 October 2019

Accepted Date: 10 October 2019

Please cite this article as: Peddu, H., Fand, B.B., Sawai, H.R., Lavhe, N.V., Estimation and validation of developmental thresholds and thermal requirements for cotton pink bollworm Pectinophora gossypiella, Crop Protection (2019), doi: https://doi.org/10.1016/j.cropro.2019.104984. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

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Estimation and validation of developmental thresholds and thermal requirements for cotton pink

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bollworm Pectinophora gossypiella

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Hemant Peddua, Babasaheb B. Fandb1, H.R. Sawaia, N.V. Lavhea

4

a

5

Maharashtra, India

6

b

7

Abstract

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The developmental thresholds and thermal requirements of pink bollworm were estimated using laboratory

9

data on its development at six constant temperatures from 15 C to 38 oC. The results were validated using

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field data on male moth catches in sex pheromone traps baited with gossyplure recorded at Nagpur

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(Maharashtra) during 2018 for predicting the initiation of moth emergence and completion of generation

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events. The theoretical lower and upper threshold temperatures estimated using non–linear Sharpe and

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DeMichele model applied to mean development rates were: 14.17/35.43, 15.18/35.48, 11.00/35.48 and

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13.40/35.50 oC, and the thermal requirements estimated as inverse of slope of linear regression were: 72.99,

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285.71, 144.92 and 503.62 degree days for development of eggs, larvae, pupae and egg – adult emergence,

16

respectively. Simulation of life table parameters provided reasonably closer estimates across the tested

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locations. The estimated lower and upper threshold temperatures accumulated the heat units (489.90 –

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497.90) closer to the laboratory estimates (503.62 DD) and sensibly predicted the developmental events in

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pink bollworm with ± 1.0 day error of margin under field conditions. The estimated thresholds and thermal

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requirements may help in comprehending seasonal dynamics of pink bollworm in relation to timings of

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developmental events like beginning and peaks of moth emergence, oviposition and egg hatching. This

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could facilitate in undertaking timely pest management actions such as insecticidal applications.

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Keywords: Cotton, degree days, developmental thresholds, life table parameters, pink bollworm,

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temperature–dependent phenology

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1. Introduction 1

Entomology Section, College of Agriculture (Dr. Panjabrao Deshmukh Krishi Vidyapeeth), Nagpur,

ICAR–Central Institute for Cotton Research, Nagpur – 440 010, Maharashtra, India

Corresponding author e–mail: [email protected]

1

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The pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), a native of Indo–

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Pakistan region (Saunders, 1843; CABI, 2017) is a globally important insect pest of cultivated cotton

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(Gossypium sp.). It is widely distributed in tropical America, Africa, Asia, Australia, Egypt, USA and

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Mexico (CABI, 2017). The life cycle of P. gossypiella is generally completed in 32–35 days, however it may

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vary with prevailing temperature and other environmental conditions, being longest in winter and shortest in

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summer (Chaudhari et al., 1999). The larvae of P. gossypiella cause damage to the tender squares, flowers

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and developing green bolls of cotton crop. The damaged flowers become rosetted whereas green bolls open

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prematurely with poor quality lint and deteriorated fibre quality (Singh et al., 1988; Fand et al., 2019). The

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pest is reported to remain in cotton stalks standing in field, left–over bolls of harvested cotton stalks and

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infested cotton seeds carried to the market yards and ginneries (Mallah et al., 2000; Kranthi, 2015).

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Prior to introduction of broad spectrum insecticides and transgenic Bt cotton, P. gossypiella was a major pest

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of cotton in India causing 20 – 90% yield losses (Patil, 2003). In 1980s, synthetic pyrethroids were

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introduced in India for management of cotton bollworms (Ramasubramanyam, 2004). Subsequently, with

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approval of Bt cotton in 2002 for commercial cultivation (Choudhary and Gaur, 2010), P. gossypiella was

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not a major problem until 2010. However, after a gap of nearly one and half decade, it has recently re–

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emerged as serious pest in India due to development of resistance against Bt cotton (Dhurua and Gujar,

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2011; Naik et al., 2018; Fand et al., 2019). Presently, 88% of the India’s total cotton area is under Bt cotton

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cultivation and Bollgard II constitutes > 99% of the area under Bt cotton (Nagrare et al., 2019). In this,

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context, re–emergence of P. gossypiella on Bt cotton has serious implications in the context of cotton

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production.

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Degree day models based on accumulated heat units are valuable tools in validating insect and crop

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phenologies, predicting the periods of insect activity, and thus undertaking the timely management actions

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(Higley et al 1986; Beasley and Adams, 1996). Many studies have already reported the thermal thresholds

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and heat unit requirements for P. gossypiella (Sevacherian et al., 1977; Huber et al, 1979; Hutchison et al,

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1986; Beasley and Adams, 1996). However, majority of them (except Huber et al, 1979 and Beasley and

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Adams, 1996) have used only lower temperature threshold (LTT), ignoring the upper temperature threshold

2

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(UTT) for predicting the developmental events. The importance of UTT in improving the prediction

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accuracy of P. gossypiella life events has been highlighted (Dhaliwal et al., 1991; Beasley and Adams,

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1996). As the heat unit summations are computed using developmental thresholds and daily minimum and

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maximum temperature, the values estimated for any given species using same thresholds at different

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geographical locations can only be the approximate figures and not exactly the same values because of

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temperature variability (Zalom et al., 1983). This limits the blanket recommendation of thresholds estimated

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at one part of the world for predicting the pest’s life events at another part (Arnold, 1959; Zalom et al.,

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1983). Incorrect base temperatures used in degree day accumulations add to the prediction errors (Brown,

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2013). Moreover, all the above studies reporting thermal requirements for P. gossypeilla were carried out in

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American cotton growing regions, and are seriously lacking from India or other Asian cotton growing

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countries that share similar climatic conditions. Earlier studies on P. gossypiella from India have focused

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only on its biology (Muralimohan et al., 2009; Dhara Jothi et al., 2016), seasonal infestations in field (Singh

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et al., 1988; Patil, 2003; Fand et al., 2019), and resistance against transgenic Bt coton (Dhurua and Gujar,

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2011; Naik et al., 2018). However, temperature–dependent population growth potential of P. gossypiella

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largely remained unexplored. This warrant precise estimation of LTT and UTT for P. gossypiella to gain

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better insights into its bio–ecology and population growth potential under Indian scenario of cropping

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environments and cultural practices.

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The fundamental aim of present study was to estimate and validate the temperature thresholds, thermal

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requirements and temperature–dependant population growth potential of P. gossypiella. The laboratory data

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on P. gossypiella biology at six constant temperatures between 15–38 oC were used computing temperature–

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dependent life functions. The results were validated using a field data on male moth catches in pheromone

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traps for predicting the thermal summations required to initiate in–field moth emergence and to complete the

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generation events.

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2. Materials and methods

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2.1 Stock colony of pink bollworm

3

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During the cotton growing season of 2018–19, P. gossypiella infested green bolls were collected from

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cotton crop (cultivar: Suraj, non–Bt) raised at the experimental field of ICAR–Central Institute for Cotton

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Research (ICAR–CICR), Nagpur (Maharashtra, India) (21°2’18” N and 79°3’35” E). The collection

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locality is mainly a cotton growing area with medium to deep black soil and mean annual rainfall of 1000

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mm. Both, the green bolls (approx. of 2–3 Weeks old) showing a mark of larval entry hole on their rinds

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and the partially opened bolls (approx. of 4 Weeks old) having live larvae feeding inside with the damaged

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seeds and discoloured lint were collected. The sampled bolls were placed inside the plastic containers (45 ×

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20 cm size, mouth covered with white muslin cloth using rubber band) @ 10 bolls per container. The

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containers were maintained in laboratory at 27 ± 1°C temperature and 65 ± 5% relative humidity till larvae

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completes its development, enter pupation and adults are emerged. The wicks of absorbent cotton soaked

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with 10% honey solution were provided as a food to the newly emerged adults. For rearing subsequent

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generations of P. gossypiella a method of detached green bolls was adopted (Fand et al., 2019).

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Approximately 10 d old, fresh and healthy green bolls from cotton plants (cultivar: Suraj, non–Bt) raised

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inside the net house were excised gently along with their stalks, washed with tap water to remove inherent

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dirt and were shade dried. A molten paraffin wax was applied onto the cut ends of boll stalks to reduce

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moisture loss and prevent decay due to secondary microbial infection (Fand et al., 2019). The bases of boll

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stalks were covered with cotton wick and were immersed individually in 10% sucrose solution inside the

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eppendorf tubes (2 ml capacity to improve the shelf life of detached bolls through supplementation of

95

carbohydrates for boll respiration and to maintain the osmotic potential (Pun and Ichimura, 2003; Fand et

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al., 2019). Such 10 bolls were held in each plastic container (45 × 20 cm size). The newly emerged adult

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moths (< 12 h) were caged @ two pairs per container and such multiple containers were held separately for

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obtaining enough population of P. gossypiella. The moths were fed with 10% honey solution in water (10

99

ml pure honey diluted in 90 ml distilled water) soaked on wicks of absorbent cotton. The moths were

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transferred daily to new containers holding fresh bolls for egg laying throughout the oviposition period of

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females. The hatched larvae entered the bolls, fed and pupated within the bolls itself. The newly formed

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pupae were removed, sexed as males and females (Fry, 2018) and maintained separately till adult

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emergence in small plastic containers (15 × 10 cm) secured with lids having perforated mesh. The newly 4

104

emerged adult moths were paired and transferred to new cages holding fresh green bolls to continue the

105

next cycle. Before actual experiment was initiated, we have successfully reared the pink bollworm on

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detached cotton bolls for three generations to remove any inherent field parasitism or infection of

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entomopathogens. The F4 population onwards was used for conducting temperature-dependent

108

experiments. The study insect was identified from Insect identification service of Division of Entomology,

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ICAR–Indian Agricultural Research Institute, New Delhi, India (Voucher specimen no. RRS No. 1885 –

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1890/17). The PCR amplification of COI gene of mitochondrial DNA was also performed to confirm the

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insect identity (NCBI–GenBank accession numbers MG738712 – 15) (Fand et al., 2019).

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2.2. Data collection at constant temperatures

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The life cycle of P. gossypiella was studied in cohorts of single life stages at six constant temperatures i.e.

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15, 20, 25, 30, 35 and 38 °C maintained inside the controlled incubation chambers (Model: E–36H0,

115

Percival Scientific, USA) in the laboratory. The relative humidity and photoperiods were set at 65 ± 5%

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and 12:12 L:D, respectively. The incubator has a programmable temperature control with ramping and

117

non–ramping adjustments for temperature range between 10

118

as high as 90% at ambient temperatures, whereas light intensity is programmable up to 0 –1250 µ

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moles/m2/s. The life stages of P. gossypiella were evaluated at each test temperature as described below.

120

Eggs: In the evening of a day before actual start of experiment, four pairs of mated adult moths were

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released separately inside four plastic containers each holding 10 detached cotton bolls. The moths were

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removed from the containers in the next day morning and the eggs laid on the bolls were counted. A total of

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200 eggs (~12 h old) in four replicates, each with 50 eggs laid on different bolls were held in plastic

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containers inside the growth chambers for evaluation at each of the test temperatures. The egg hatching

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from each of the test temperatures was recorded daily.

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Larvae: A batch of 20 neonate larvae (< 12 h old) from P. gossypiella stock colony was released onto 10

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bolls @ two larvae per boll and were held in a plastic container (45 x 20 cm size). A total of 100 larvae in

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five different containers were evaluated for their development at each test temperature. The observations on

5

– 44 . The humidity control is adjustable to

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the development time, larval mortality and the numbers of pupae were recorded daily from all the five

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replicates in each of the constant test temperatures.

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Pupae: A total of 100 newly formed pupae (~12 h old) were isolated from P. gossypiella stock colony and

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held separately in batches of 25 inside four different plastic containers (15 x 10 cm size) kept in incubation

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chambers at each test temperature. The pupal durations and the number of adults emerged in respective test

134

temperatures were recorded daily.

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Adults: Ten pairs of newly emerged adults (~12 h old) from P. gossypiella stock colony were caged

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separately @ one pair per mating jar made of plastic containers (30 x 15 cm size) each holding ten green

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cotton bolls. The adult moths were fed with 10% honey soaked over absorbent cotton wick. The moths

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were transferred daily to the new containers holding fresh cotton bolls. The daily numbers of eggs laid on

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green bolls were counted from each jar to calculate total fecundity per female. The longevity of each male

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and female adult was recorded at respective test temperatures. In case male adults died earlier, the females

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in respective cages were provided with new male adults to ensure optimum mating and fecundity.

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2.3 Data analyses and modelling tools

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2.3.1 Estimation of immature development times

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The concepts of same shape property (Sharpe et al., 1977) and rate summation (Curry et al., 1978) were

145

applied to estimate the variability in the distribution of development times of immature life stages of P.

146

gossypiella viz., egg, larva and pupa at various constant temperatures. According to these concepts, the

147

intrinsic distributions of development times of an insect at different temperatures fall on the top of each

148

other when normalized by the mean of each distribution. This helps in rationalising the mean rate of

149

development as a lognormal distribution of tolerances among individuals of cohort. Accordingly, the

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cumulative probability distributions of P. gossypiella immature development times under different test

151

temperatures were estimated, normalized and arranged in a frequency distributions. The mean development

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time and cumulative frequencies of survivorship for each life stage of P. gossypiella were calculated at

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different constant temperatures. For describing the distribution of immature development times, three

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different distribution models i.e. probit, logit and Cloglog were fitted to the experimental data and the logit

6

155

distribution was selected as the best fit model based on Akaike’s Information Criterion (AIC) (Akaike,

156

1973). The equation of logit distribution function is given below. =

157



(1)

158

Where, F(x) is the probability to complete development at time x, lnx is the natural logarithm of the days

159

observed, a is the intercept corresponding to temperature i, and b is the common slope of the regression

160

model.

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2.3.2 Estimation of immature development rates

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The development rates of immature life stages at different test temperatures were estimated by taking the

163

inverse of development times (1/d) of respective life stages. Non–linearity was observed in egg and larval

164

development at temperatures above 38°C and 35°C, test temperatures respectively. Therefore, while fitting

165

a linear model to the data on egg and larval development, these temperatures were excluded and the data

166

was fitted for remaining temperatures only (Egg:15°C –390 35 C; Larvae: 15°C –30°C). Entire range of

167

test temperatures (15°C –38°C) was selected for pupal development rate. The following equation of linear

168

regression model was fitted to estimate the temperature–dependent development rates (Campbell et al.,

169

1974).

170

=

+

(2)

171

Where, r (T) is the rate of development (days-1) at temperature T (°C), and, a and b represent the intercept

172

and the slope of the equation, respectively.

173

Due to poor predictability of linear model at high test temperatures (>35 ), we further fitted non-linear

174

Sharpe and DeMichele model (Sharpe and DeMichele, 1977) for estimating the non–linearity in

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development rates at test temperatures higher than 35 . This is a biophysical model considered the most

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appropriate for describing temperature–dependent life processes in poikilothermic organisms. It hypothesizes

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that, the development of poikilotherms is driven by a rate determining enzyme or enzyme complex which

178

has three basic reversible energy rates: inactive at cold temperatures, active at optimum temperatures and

179

inactive at high temperatures (Sharpe and DeMichele 1977; Schoolfield et al. 1981). The equation of the

180

model used is given below. 7

=

181



.

∆ &

!

.

∆

" " $% &

!

"

" #

%$

∆ '

!

" " $% '



(3)

182

Where, r (T) is development rate at temperature T (°K); R is universal gas constant (1.987 cal degree-1 mol-

183

1

184

enthalpy of activation of reaction catalysed by enzyme (cal mol-1); ∆Hl is change in enthalpy at low

185

temperature (cal mol-1); ∆Hh is change in enthalpy at high temperature (cal mol-1); Tl is low temperature at

186

which enzyme is half active and Th is high temperature at which enzyme is half active.

187

2.3.3 Developmental thresholds and thermal requirements

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The slope and intercept of the linear regression model provided the estimates of LTTs and thermal constant

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requirements (DD) (Campbell et al., 1974). The ratio of intercept and slope (a/b) was taken as LTT,

190

whereas the inverse of slope (1/b) was taken as the DD required for completion of development of

191

respective immature life stages of P. gossypiella. The parameter estimates of Sharpe and DeMichele model

192

provided the values for ‘Tl’, ‘To’ and ‘Th’ representing the LTT, optimum temperature (To) and UTT,

193

respectively. The obtained values were in °K which were converted to °C by using the relationship °C = °K

194

– 273 (Fand et al., 2014; 2015).

195

2.3.4 Estimation of immature mortality

196

The cumulative frequencies of survivors from each cohort were calculated and mortality was estimated by

197

subtracting the number of cohort survivors from total sample size. The temperature–dependent mortality in

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immature life stages was estimated by fitting Wang model (Wang et al. 1982). The mathematical equation

199

of three parameter version of model (Wang–1) used for assessing mortality in egg and pupal stages is as

200

given below.

201

(

202

Similarly, the four– parameter version (Wang–3) was used for larval mortality. The following equation of

203

the model was used.

204

(

); P is development rate at optimum temperature To (°K), assuming no enzyme inactivation; ∆Ha is

= 1−

= 1−

+ ",-!#

+ ",-!#

#

0

./

$% ", - !#

# ./ $% ", - !# 0&

./# $% 1 2 0

(4)

./# $% 1 2 0'

(5)

8

205

Where, m (T) is the rate of mortality at temperature T (°C); Topt is the optimum temperature for survival

206

(°C); B, Bl and Bh and H are the fitted parameters of equation.

207

2.3.5 Adult survival

208

The inverse of adult survival times (1/days) were treated as the survival rates or ageing rates. The

209

temperature–dependence of survival rates of male and female adults was determined by fitting a Stinner

210

equation shown below (Stinner et al. 1974).

211

r T =

6

5"

67 8

+

6

59

(6)

67 7 8: 8

212

Where, r(T) is the survival rate (1/day) at temperature T (°C); To is the optimum temperature (oC); c1 and

213

c2 are the maximum and minimum temperatures (°C) when T ≤ To and T > To, respectively; K1 and K2 are

214

constants representing the slope and the intercept, respectively.

215

2.3.6 Fecundity and relative oviposition rate

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The total fecundity, the age specific rates of oviposition and adult survival are the key factors in determining

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the temperature effects on reproduction in insects (Fand et al., 2015). The total number of eggs produced per

218

female of P. gossypiella during her whole life span represents the total fecundity. The following equation of

219

Guassian with log model was fitted to determine the temperature effects on total fecundity of females.

220

f T = <= + a . exp −0.5. log G

221

Where, f(T) is a mean lifetime fecundity at temperature T (oC); y0 and T0 are the minimum and optimum

222

temperatures (ºC), respectively for oviposition; a and b are the fitted parameters of equation.

223

The age–specific oviposition rate of P. gossypiella at each test temperature was described by an exponential

224

model. It is the proportion of the total number of eggs produced during a given age interval compared with

225

the total lifetime reproductive potential of the female. The cumulative offspring production rate was plotted

226

against normalized female age expressed as ratio of female age in days divided by mean survival time. The

227

formula of the exponential model used for assessing the relative oviposition rate is given below:

228

y= 1 − e

HI!

I9

J

$

K

(7)

LHM IM9 5MN O

(8)

9

229

Where, y is the cumulative oviposition frequency; X is the normalised age of female expressed as a ratio of

230

age in days and median survival time; a, b and c are the equation parameters.

231

2.3.7 Simulation of life table parameters

232

Using the functions established for development, survival and reproduction in P. gossypiella at six constant

233

temperatures between 15–38 °C, the life table parameters were simulated stochastically following cohort

234

updating and rate summation approach (Curry et al., 1978). The sex of progeny was determined by

235

generating random values between 0 and 1 (Kroschel et al., 2013; Fand et al., 2014). As the temperature

236

and female age did not significantly affect the female proportion in the progeny, constant female rate of 0.5

237

was assumed while carrying out simulations. The following life table parameters were estimated with the

238

initial number of eggs set to 100 and 10 replications for simulations at each of the test temperatures. (R : =

Q 5R STUV × XYYHURZ [RZ\T\H



239

a. Net reproductive rate

240

b. Generation length in days (T) = !_ $ + !_7$ + !_`$ + !ab$ × TR c=% %

Q YH ZHU T U] Z:^

V

(9) (10)

241

Where, d1, d2, and d3 are the median development rates for immature life stages of PBW i.e. Egg, Larva and

242

Pupa, respectively; sf is the mean survival rate of the female and TR 50% is the normalised age of the females

243

until 50% oviposition. (re =

fJ

244

c. Intrinsic rate of increase

(11)

245

d. Finite rate of increase

(h = exp re

246

e. Doubling time

(ij =

247

2.3.8 Modelling tools

248

All the analyses related to estimation of temperature–dependent development of P. gossypiella were

249

performed using Insect Life Cycle Modelling (ILCYM) software, version 3.0 (International Potato Centre,

250

Lima, Peru) (Tonnang et al. 2013). ILCYM is open source software which has three basic components viz.,

251

model builder, validation and simulation, and population analysis and risk mapping. The ‘model builder’

252

contains several linear and non–linear models used for estimating temperature–dependent life processes in

253

insects. The deterministic and stochastic simulations of life table parameters are performed with ‘validation

g

(12)

7

(13)

Zk

10

254

and simulation’ module. The geographical information system (GIS) component is linked to ‘population

255

analysis and risk mapping’ module which help in mapping of the pest risk in different geographical areas.

256

The present study employed the ‘model builder’ for estimating the temperature dependent life functions,

257

and the ‘validation and simulation’ for life table parameter simulations. Using ‘model builder’ module,

258

several mathematical linear and non–linear equations were fitted to the data for estimating the temperature–

259

dependent distribution of development times, rates of development, survival and reproduction. While

260

running the tool, an option for ‘run multiple models’ was selected which successively displayed the fitted

261

sub–models with their respective statistics.

262

2.3.9. Statistical analyses

263

The cumulative probability distributions of P. gossypiella immature development times under different test

264

temperatures were estimated, normalized and arranged in a frequency distributions. The mean development

265

time and cumulative frequencies of survivorship for each life stage of P. gossypiella were calculated at

266

different constant temperatures. The development rates of immature life stages at different test temperatures

267

were estimated by taking the inverse of development times (1/d) of respective life stages. The best fitted

268

models of distribution time, development rate, mortality, longevity and fecundity for different life stages

269

were chosen based on widely accepted goodness of fit indicators such as AIC (Akaike 1973) and coefficient

270

of determination (R2). Analysis of Variance (ANNOVA) and Least Significant Difference (LSD) were used

271

as post–hoc tests, and the significance was tested at p ≤ 0.05 level for probability thresholds and hypothesis

272

testing (Fisher 1953).

273

2.4 Validation of established life functions

274

2.4.1 Simulation of life table parameters using real time daily temperature data

275

The simulation procedure in ILCYM is based on the daily minimum and maximum temperature data

276

(Tonnang et al. 2013). The data were collected from Automatic Weather Stations at six locations

277

representing North, Central and South cotton growing zones of India as mentioned below: North Zone –

278

Hisar (2016), Haryana State; Central Zone – Nagpur (2017), Maharashtra State; Surat (2017) and Junagadh

279

(2017), Gujarat state; South Zone – Dharwad (2010), Karnataka state; and Coimbatore (2016), Tamil Nadu

280

State. The annual maximum temperatures for Hisar, Nagpur, Surat, Junagadh, Dharwad and Coimbatore 11

281

fluctuated between 13.2 – 46.7ºC, 19.4 – 45.5ºC, 26.1 – 39.6ºC, 20.8 – 44.6ºC, 17.8 – 39.4ºC and 25.0 –38.6

282

ºC, respectively. Similarly, the minimum temperatures for these locations ranged between 1.5 –32.2 ºC, 5.0

283

–35.8 ºC, 13.5 – 28.6 ºC, 5.6 –27.9 ºC, 9.2 – 37.8 ºC and 13.4 – 27.5 ºC, respectively.

284

Diurnal temperature variability was accounted using a time step length of 15 minutes. For half day

285

temperature predictions, a cosine function was used and the temperature–dependent life table parameters of

286

P. gossypiella were calculated for each 15 minute time step. The equation used for predicting the

287

temperatures for first half–day is given below (Kroschel et al. 2013).

288

Ti =

289

Where, Ti is the temperature (oC) of time step i (i = 1, 2, 3, ...48; and Min and Max are the daily minimum

290

and maximum temperatures, respectively.

291

The above procedure was then repeated to estimate temperatures for the second half–day using minimum

292

temperature of the next day in the equation and the simulations were carried out so on for rest of the period.

293

The life table parameters were simulated stochastically (Curry et al. 1978) and compared with observed

294

values obtained in constant temperature experiments.

295

2.4.2 Validation of developmental thresholds and thermal requirements

296

The threshold temperatures and thermal requirements of P. gossypiella estimated based on constant

297

temperature experiments in the laboratory were validated for their robustness and accuracy in predicting the

298

developmental events under field conditions. Field data on male moth catches in sex pheromone traps

299

baited with gossyplure recorded at Nagpur (Maharashtra) during 2018 was used for predicting the thermal

300

summations accumulated between beginning of the moth emergence and occurrence of subsequent field

301

peaks of moth catches. The time lapse between these two events was considered as completion of one in–

302

field generation of P. gossypiella (Beasley and Adams, 1996). The heat units required for completion of the

303

said developmental event were accumulated using laboratory estimates of LTT and UTT, and daily data on

304

minimum and maximum temperatures recorded for the year 2018 at Nagpur location. A sine wave method

305

with horizontal cutoff was used in degree day estimation (Allen, 1976). The heat units accumulated were

306

compared with both the laboratory estimates and those reported in literature.

mH

7

mT

× cos !

× T =.c no

$+

mT

7

mH

(14)

12

307

3. Results

308

3.1 Distribution of immature development times and adult survival times

309

The durations of the immature development and adult survival in P. gossypiella decreased significantly

310

with increase in temperatures from 15°C to 35°C (Table 1). Shrinking of the egg chorions and larval bodies

311

was observed at 38oC indicating no egg and larval development at this temperature. There was reasonably

312

good agreement between the development times of P. gossypiella life stages observed at different test

313

temperatures and those predicted by the model. The cumulative logit distribution function fitted to the data

314

was sensible enough to describe the variability in development times of immature stages and survival times

315

of adult stages of P. gossypiella (Table 2).

316

3.2 Temperature–dependent development rate of immature stages

317

The test temperatures at which immature development rates deviated from linearity were excluded while

318

fitting linear relationship and the linear regression was fitted to the data recorded at remaining temperatures

319

only. The linear model reasonably estimated the development rates for eggs, larvae and pupae of P.

320

gossypiella at temperatures between 15 –35 oC, 15 – 30 °C and 15 – 38 °C, respectively (ANOVA: All

321

stages, p< 0.003; R2 >0.97; egg: df = 1,3; F = 92.83; larva: df = 1,2; F = 303.21; pupa: df = 1,4; F = 146.60)

322

(Table 3).

323

The projected drop in the immature development rates at temperature of ≥ 35 oC was precisely estimated by

324

a non–linear Sharpe and DeMichele model (ANOVA: All stages, df = 6,8; p<0.01; AIC < -10.0; R2 > 0.95; F

325

= 130.97 (eggs), 228.95 (larvae) and 71.25 (pupae) (Table 3, Figure 1). The linearly increasing development

326

rate in egg stage declined sharply after 35oC, indicating that no egg development will be supported at

327

temperature above 35 oC (Figure 1a). The larval development rate was non–linear below 20 oC as can be

328

seen from zig–zag lines or non–smoothness of fitted curve, and it increased linearly above 20 oC till 35 oC,

329

after which it again declined sharply to reach abscissa (Figure 1b). A smooth curve obtained for pupae

330

indicated a slower rate of development at temperatures between 15–20 oC, after which it increased rapidly

331

until temperature reaches 35oC (Figure 1c).

332

3.4 Developmental threshold temperatures and thermal requirements

13

333

The LTTs for development of eggs, larvae, pupae and egg–adult emergence in P. gossypiella, taken as the

334

ratios of intercepts and slopes (a/b) of linear regressions were 11.23, 11.37, 11.00 and 11.20 oC,

335

respectively. Similarly, the thermal constants expressed in degree days (DD), estimated by taking inverse of

336

slopes of linear regression lines were 72.99, 285.71, 144.92 and 503.62 DD for eggs, larvae, pupae and

337

egg–adult emergence, respectively (Table 3).

338

The LTTs and HTTs estimated by a non–linear Sharpe and DeMichele model for the immature life stages of

339

P. gossypiella were: 14.17/ 35.43 oC (eggs), 15.18/ 35.48 oC (larvae), 11.00/ 35.48 oC (pupae) and 13.40/

340

35.50 oC (egg–adult emergence). Similarly, the optimum temperatures (To) estimated by the model for

341

immature development were 24.83, 24.74 and 27.28 oC for eggs, larvae and pupae, respectively (Table 3).

342

3.5 Temperature–dependent immature survival

343

In egg stage, the lowest mortality (11.7%) was observed at 25 oC, which shoot above 30% at 15 oC and

344

35oC test temperatures. The larvae, especially during their early instars were relatively more susceptible to

345

temperature–dependent mortality compared to egg and pupal stages. A single larva that could enter

346

pupation at 15°C did not lead to adult emergence. Maximum pupal mortality (64%) was observed at 15 oC

347

whereas it was less than 40% at temperatures between 20–35 oC. In general, the constant test temperatures

348

below 20 oC and above 35 oC were relatively non–congenial, whereas those between 20–30 oC with ≥50%

349

survival, were relatively favourable for immature development in P. gossypiella. Three parameter version

350

of Wang model (Wang-1) offered a best fit to the temperature–dependent mortality in egg and pupal stage

351

(ANOVA: Both stages, p=0.01; df = 2,2; AIC < -8.0; R2 > 0.88; F = 64.91 (eggs) and 7.54 (pupae). On the

352

other hand, four parameter version of Wang model (Wang-3) was best fitted to the data on temperature

353

dependent mortality in larval stage (ANOVA: p=0.02; df=3,1; AIC= -29.9; R2=0.99; F=1049.40). The

354

optimum temperatures predicted by the model for better survival of eggs, larvae and pupae were 25.25,

355

22.83 and 27.14 oC respectively (Table 4, Figure 2).

356

3.6 Temperature–dependent adult life span

357

In general, males required less time to senescence compared to females, and the adult ageing rates were

358

rapid at low (15oC) and hight (35oC) test temperatures (Table 1). Both the female and male adults of P.

14

359

gossypiella had life span of 11.00 –19.00 days at constant temperatures between 20 – 35 °C. The

360

temperature–dependence of survival times in both female and male adults was well described by Stinner

361

model (Stinner et al., 1974) (ANOVA: for both sexes, df=4,10; p <0.02; R2 > 0.67; AIC < -11.0; F:

362

female=7.52; male=5.10). The optimum temperature for male adult survival (13.39 oC) was considerably

363

lower than that of female adults (21.66 oC) (Table 5, Figure 3).

364

3.7 Temperature– dependent reproduction

365

Due to decrease in female longevity with increasing temperatures, the oviposition period was significantly

366

reduced. For the evaluated range of constant temperatures (15°C –35 oC), the pre–oviposition and post–

367

oviposition periods ranged between 2 –7 days and 1–4 days, respectively. Minimum (11.14) and maximum

368

(102.60) egg layings were recorded at 15oC and 25oC temperatures, respectively whereas; no egg laying

369

was occurred at 38 oC test temperature. The Gaussian with log model described the temperature–

370

dependence of P. gossypiella fecundity (ANOVA: df=3,1; p=0.05; R2=0.99; AIC=29.69; F=111.99). The

371

favourable temperature range for reproduction was predicted between 20 –30 oC, and the minimum and

372

optimum temperatures required for oviposition were 13.07oC and 24.80oC, respectively. (Table 6, Figure

373

4a). The exponential modified function described the relationship between cumulative oviposition rate and

374

female age (ANOVA: df = 2,122; p = 0.00; F = 1017.862; AIC= -238.39; R2=0.94). The 50% of the

375

oviposition was completed by the female at a physiological age of 0.68 (Table 6, Figure 4b).

376

3.8 Life table parameters estimated at constant temperatures

377

Pectinophora gossypiella was unable to develop at constant temperatures of 15 and 38 oC under laboratory

378

conditions, therefore, we estimated life table parameters only for a temperature range 20 oC – 35 oC (Table

379

7). The simulation results indicated temperatures between 25–30 oC as the most favoured range for

380

optimum growth of P. gossypiella. At 25 oC temperature, the population of P. gossypiella attained

381

maximum net reproductive rate (Ro) of 16.302 females/female/generation and fecundity of 56.565 eggs/

382

female/ generation. The intrinsic (rm) and finite (λ) rates of increase were maximal, and the doubling time

383

(Dt) was shortest at temperatures between 25–30 oC. The mean generation time (T) decreased from 63.18 to

384

31.67 days with increase in temperature from 20 to 30 oC under laboratory conditions. A slight increase in

385

the duration of generation time (32.47 days) was observed at 35 oC. 15

386

3.9 Simulated life table parameters

387

Simulations carried out using real time daily temperatures from weather stations reasonably predicted the

388

life table parameters for P. gossypiella at five out of six selected locations viz., Nagpur, Surat, Junagadh,

389

Dharwad and Coimbatore. The life table parameters predicted for Hisar station were slightly deviating from

390

those established by phenology model and those predicted for remaining five stations. The negative values

391

of rm and Dt, lowest values for Ro, GRR, and λ, and highest value of T predicted for Hisar indicated the

392

adverse effects of extreme low (1.5°C) and high (46.7°C) daily temperatures at this location on development

393

and survival of P. gossypiella (Table 7).

394

3.10 Prediction of moth emergence using developmental thresholds and thermal requirements

395

The laboratory estimated mean LTT and UTT of 13.4 and 35.5 °C accumulated the heat units in a range of

396

489.9 – 497.9 DD between the beginning of moth emergence and the occurrence of subsequent peaks of

397

moth captures in gossyplure baited pheromone traps. The moth captures plotted against the calendar dates

398

(Figure 5a) and the accumulated heat units (Figure 5b) have clearly shown the coincidence of peaks of

399

moth captures with estimated heat unit accumulations. From these graphs it was also revealed that though

400

the durations required for completions of developmental events in P. gossypiella varied from a minimum of

401

35 days during August–September to a maximum of 71 days during December–January, however the heat

402

units accumulated between the developmental events remained relatively constant in a range of 489.9 –

403

497.9 DD.

404

4. Discussion

405

The temperature–dependent population growth potential of P. gossypiella reared on detached cotton bolls

406

in laboratory at constant temperatures between 15 – 38 °C is estimated employing a phenology modeling

407

centered on rate summation and cohort updating approach (Curry et al., 1978). Further, the temperature

408

thresholds and thermal requirements for completion of its development were estimated and validated using

409

a field data on male moth captures in sex pheromone traps. The results revealed that population of P.

410

gossypiella could thrive at constant temperatures between 20–35°C, however its optimal growth was

411

observed only between 25 – 30 oC.

16

412

Due to the unsatisfactory results obtained with linear model at high test temperatures and its limitation in

413

estimation of UTTs, we used a non–linear equation of Sharpe and DeMichele (Sharpe and DeMichele,

414

1977) for estimating the development rates. The duration of egg development in present study (10.0 days at

415

20°C – 4.0 days at 35°C) was relatively closer to that of reported by earlier researchers (10.0 days at 20°C –

416

4.3 days at 30°C) (El Sayed and Abd El–Rhman, 1960; Fye and McAda, 1972; Hutchinson et al., 1986). A

417

non–linear trend of larval development observed at constant temperatures above 35°C was strongly

418

supported by the work of Philipp and Watson (1971), and Hutchinson et al (1986), who reported a non–

419

linearity in larval development at temperatures above 32.2°C and 35.5°C, respectively. The pupal

420

developmental durations reported in present study (6.0 days at 35°C – 17.0 days at 15°C) are also well

421

supported by the studies of Philipp and Watson (1971), Hutchinson et al (1986) and Zinzuvadiya et al

422

(2017). However, our findings on larval and pupal durations were not consistent with those of Yones et al.

423

(2011) and Shah et al. (2013), reporting lower durations for larva and higher duration for pupa.

424

The LTT (14.17°C) and HTT (35.43°C) estimated by Sharpe and DeMichele model for egg development in

425

P. gossypiella were relatively similar to the earlier reports of LTTs (13.88 – 14.9 °C) (Fye and McAda,

426

1972; El–sayed and Ali, 2005), and HTTs (34.76°C) (El–sayed and Ali, 2005). Similarly, the LTT of

427

15.18°C for larval development was closer to that of 15.22°C (El–lebody et al., 2015), however it was

428

relatively on higher side compared to 12.38 °C (Hutchinson et al., 1986) and 14.07 °C (Yones et al., 2011).

429

The LTT of 11.00 °C estimated for pupal development was in line with 11.69 °C (Hutchinson et al., 1986),

430

however, deviated from 9.57 °C (Yones et al., 2011). Mean LTT of 13.40°C for development from egg to

431

adult emergence was in agreement with the literature reports of LTTs between 13.00 – 13.90 °C (Wene et

432

al., 1965; Huber et al., 1979; Beasley and Adams, 1996), and deviated from the smaller values of LTTs

433

between 10.0 – 12.30 °C (Hutchinson et al., 1986; Lingren et al., 1989; Gergis et al., 1990; Naranjo and

434

Martin., 1993). Similarly, the mean UTT of 35.5°C for development from egg to adult emergence was also

435

consistent with literature reports and has joined an intermediate group between the UTTs of 32.5 – 32.8 °C

436

(Hutchinson et al., 1986; Naranjo and Martin, 1993; Beasley and Adams, 1996) and 37.5 °C (Gergis et al.,

17

437

1990). However, relatively lower values of UTT (~30.0 °C) had been reported in some studies (Wene et al.,

438

1965; Huber et al., 1979; Lingren et al., 1989). Despite minor variations in estimated and reported

439

thresholds, it is encouraging that the combination of estimated thermal thresholds (13.40/35.50 °C) when

440

applied to field data, satisfactorily predicted the peaks of moth emergence based on the required number of

441

heat unit accumulations.

442

The heat unit requirement of 72.99 DD estimated for development of egg stage is similar to that of 71.90 DD

443

(Gergis et al.,1990) and 72.11 DD (Yones et al., 2011); and also in line with a range of 63.27 – 78.62 DD

444

(El–sayed and Ali, 2005) and 54.60 – 73.00 DD (El–Lebody et al., 2015). However, our findings largely

445

deviated from extreme high value of 107.30 DD (Albertos, 1974) and extreme low value of 44.00 DD

446

(Hamed, 2005). The estimated larval heat unit requirements of 285.71 DD were relatively on higher side of

447

previous reports of 276.20 DD (Albertos, 1974), 247.90 DD (Naranjo and Martin, 1993) and 243.47 DD

448

(El–sayed and Ali, 2005), and deviated strongly from 144.00 – 166.38 DD (Gergis et al., 1990; Hamed,

449

2005; Yones et al., 2011; El–Lebody et al., 2015). The thermal requirements for completion of pupal

450

development in P. gossypiella (144.92 DD) are supported by the results of previous researchers, e.g. 167.00

451

DD (Albertos, 1974), 144.90 – 149.60 DD (Naranjo and Martin, 1993), and 115.26 – 140.85 DD (El–Sayed

452

and Ali, 2005). At the same time, the present findings were contradicted by the reports of some researchers.

453

The contrast included the estimates of 93.00 DD at extreme low end (Hamed, 2005) and 232.60 – 248.70

454

DD at extreme high end (Gergis et al., 1990; Yones et al., 2011; El–lebody et al., 2015). The total heat unit

455

requirement of 503.62 DD estimated for completion of development from egg laying to adult emergence

456

were in line with the literature reports, e.g. 499.90 DD (Gergis et al., 1990), 492.00 DD (Beasley and

457

Adams, 1996), 499.13 – 522.11 DD (Yones et al., 2011) and 464.50 – 502 DD (El–lebody et al., 2015).

458

However, our results are contradictory to the lower value of 324.00 DD (Hamed, 2005) and higher range of

459

513.30 – 550.50 DD (Albertos, 1974; Sevacherian et al., 1977; El–sayed and Ali, 2005).

460

The survival rates of P. gossypiella immature life stages varied significantly at different test temperatures.

461

Highest larval survival (68.0%) was recorded at constant temperature of 25oC whereas increased mortalities

462

in immature stages were observed at temperatures below 20oC and above 35oC. Similar trend in immature 18

463

survivorship has been reported (Phillip and Watson, 1971; Gergis et al., 1990; Shah et al., 2013). The

464

senescence rates for both female and male adults were rapid at 15°C and 35°C temperatures.

465

The adult longevities were reduced at these extreme temperatures compared to optimal life span of 13 – 19

466

days observed at temperatures between 20°C and 30°C. This ultimately shortened the reproductive period

467

and reduced the life time fecundity. The pre and post oviposition periods reported in present study were

468

supported by the literature reports (Yones et al., 2011; El–lebody et al., 2015; Zinzuvadiya et al., 2017). The

469

maximum egg laying of 102.6 eggs/ female occurred at 25°C, and reduced drastically at temperatures below

470

20°C and above 30°C. Fairly similar trend in temperature–dependent fecundity of P. gossypiella was

471

reported (Graham et al (1967). The total fecundity in our study was relatively closer to that of reported in

472

literature, e.g. 70.00 eggs per female in a life span of 11.70 days (Cacayorin et al., 1992) and 75 –125 eggs in

473

a period of 9.0 days (Attique et al., 2004). However, it was on lower side compared to a range of 204 – 224

474

eggs/ female reported in literature (El Sayed and Abd El–Rhman, 1960; Philipp and Watson, 1971; Fye and

475

McAda, 1972; Henneberry and Leal, 1979; Zinzuvadiya et al., 2017). Our study presents only the effect of

476

temperature on P. gossypiella fecundity when reared on detached cotton bolls. However, fecundity is also

477

influenced by several other factors such as host nutritional quality, food availability, nutrition of immature

478

stages, and abiotic factors like light intensity, relative humidity, etc. (Attique et al., 2004).

479

The simulation of life table parameters generated valuable information on temperature–dependent population

480

growth potential of P. gossypiella. The temperature effects on P. gossypiella life cycle have been widely

481

studied (Graham et al., 1967; Fye and McAda (1971; Phillip and Watson, 1971; Hutchinson et al., 1986;

482

Yones et al., 2011). Our findings are in line with majority of these studies, e.g. Ro and rm (Phillip and

483

Watson, 1971), λ (Graham et al., 1967) and T (El–sayed, 1960; Fye and McAda, 1971; Hutchinson et al.,

484

1986; El–sayed and Ali, 2005; Yones et al., 2011). However, the values of rm and Ro reported in present

485

study deviated from some of the literature reports. Graham et al (1967) obtained relatively higher values of

486

Ro ranging between 79.232 – 139.852 females/ female/ generation at temperatures between 26.7 – 32.22°C.

487

The development rates, mortality and fecundity are supposed to be highly variable factors and rm is

19

488

computed as a function of Ro, thus it adds to the variability in estimated life table parameters (Fand et al.,

489

2014; 2015).

490

Simulations carried out using real time daily temperatures from weather stations reasonably predicted the

491

life table parameters for P. gossypiella at five out of six selected locations viz., Nagpur, Surat, Junagadh,

492

Dharwad and Coimbatore. The life table parameters predicted for Hisar station slightly deviated from those

493

established by phenology model and those simulated for remaining five stations. The negative values of rm,

494

lowest values for Ro, GRR, and λ, and highest value of T predicted for Hisar indicated the adverse effects of

495

daily temperatures on development and survival of P. gossypiella, restricting its population growth at

496

temperature extremes. Analysis of daily data on annual range of minimum (1.5 – 32.2ºC) and maximum

497

(13.2 – 46.7ºC) temperatures at Hisar location used in simulation of life table parameters revealed that these

498

temperatures were falling well below the LTT (13.4°C) and rising well above the UTT (35.5°C) estimated

499

for P. gossypiella. Thus, the temperature–dependent phenology model of P. gossypiella presented here is

500

sensitive enough to catch minute variations in daily temperatures and thus may give reasonably valid results

501

of life table simulations.

502

The heat units of 489.90 – 497.90 DD accumulated between two successive moth emergence peaks under

503

field condition were closer to the laboratory estimates of 503.62 DD required to complete development

504

from egg to adult emergence. Thus, the validation results have clearly indicated that the LTT and UTT of

505

13.4 and 35.5°C estimated for P. gossypiella development based on constant temperature studies in

506

laboratory were reliable enough to predict the pest’s developmental events with ± 1.0 day error of margin

507

under field conditions. A margin of error of 5.72 – 13.72 DD observed between the degree days

508

accumulated under field conditions and those estimated by laboratory experiments was equivalent to ±1.0

509

day in terms of duration in days. This deviation can be ascribed to the fact that the developmental

510

thresholds for an organism in field may be different from laboratory determined thresholds because of

511

variable field temperatures (Beasley and Adams, 1996). This margin of error can be reduced by correction

512

of established thresholds for field data employing coefficient of variation technique that provides best

513

combination of LTT and UTT that gives lowest coefficient of variation of degree days between the

514

developmental events (Arnold, 1959; Beasley and Adams, 1996). 20

515

In conclusion, the results of present study may help in comprehending seasonal dynamics of P. gossypiella

516

in relation to its peak abundance in field conditions, predicting the developmental events like beginning and

517

peaks of moth emergence, dates of oviposition and egg hatch, etc. This could facilitate better timing of

518

management actions such as insecticidal applications thereby enhancing the efficacy of pest control. The

519

present model, if projected to potential climate change may help in future adaptation planning for this pest

520

by allowing identification of regions with the probable increase or decrease in folds of P. gossypiella

521

incidence and spread.

522

Acknowledgements

523

This study is a part of the research work titled “Estimation of developmental thresholds and thermal

524

requirements for cotton pink bollworm, Pectinophora gossypiella (Saunders)” carried out by the first author

525

for award of the Masters Degree (M.Sc.) in Agricultural Entomology submitted to Dr. Panjabrao Deshmukh

526

Krishi Vidyapeeth (Dr PDKV), Akola, Maharashtra, India. The authors are thankful to the Professor,

527

Entomology Section, College of Agriculture, Nagpur (Dr PDKV, Akola) for approval of the present research

528

work. The authors also gratefully acknowledge the Director, ICAR–CICR, Nagpur (Maharashtra, India) for

529

providing necessary facilities and support to carry out present investigations.

530

Conflict of interest

531

The authors declare that they have no conflict of interest

532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550

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Zalom, F.G., Goodell, P.B., Wilson, L.T., Barnett, W.W., Bentley, W.J., 1983. Degree–days: the calculation and use of heat units in pest management. University of California DANR Leaflet 21373. Zinzuvadiya, H.D., Desai, H.R., lakum, M.B., Rajkumar, B.K., 2017. Biology of Pink Bollworm, Pectinophora gossypiella Saunders (Lepidoptera: Gelechiidae) on artificial diet under controlled condition. Trends in Biosci. 10: 5363–5371. 23

Figure captions Figure 1. Temperature dependent development rates (1/days) of immature stages of P. gossypiela. Eggs (a) larvae (b) and pupae (c). Fitted function: Sharpe and DeMichele model. The bold line is the selected model output and dashed lies above and below represents the upper and lower 95% confidence bands. Bars represent standard deviation of the mean. The dashed straight line represents hypothetical linear model. Figure 2. Temperature-dependent mortality rates of immature life stages of P. gossypiela: Eggs (a), larvae (b) and pupae (c). Fitted curves; Wang model, the upper and lower 95% confidence intervals of the model are indicated by blue lines. Markers are observed means Figure 3. Temperature-dependent senescence rates (1/days) for adult life stages of P. gossypiela: female (a) and male (b). Fitted curves, Stinner model, the upper and lower 95% confidence intervals of the model are indicated by blue lines. Bars represent standard deviation of the mean Figue 4. Temperature-dependent total egg production curve (a). Fitted curve, Gaussian with log; the upper and lower 95% confidence intervals of the model are indicated with blue lines. The dots are observed data points. Cumulative proportion of egg production in relation to female age expressed as normalized time (senescence/mean senescence time) (b). Fitted curve: Exponential modified function; the upper and lower 95% confidence intervals of the model are indicated. The dots are observed data points at each of the test temperatures. Age of the female at 50% oviposition is indicated. Figure 5. Field emergence of male moths of P. gossypiella predicted using developmental thresholds of 13.4/35.5 °C and degree day accumulations between two successive emergence peaks. The duration in days to moth emergence between two successive peaks varied with

seasonal temperatures (a), however the heat units (DD) accumulated between any two successive peaks remained more or less constant (b).

Table 1. Mean development time (days) of P. gossypiella life stages at different constant temperatures in laboratory. The numbers in parentheses are standard errors Development time (days) Temperature ( C)

Egg Observed

15

20

25

30

35

Survival time (days)

Larva

Predicted

Observed

Pupa

Predicted

Observed

Female

Predicted

Observed

Male

Predicted

Observed

Predicted

17.00

16.51

96.00

92.92

17.00

16.37

9.50

9.15

9.50

8.72

(0.05)

(0.10)

(0.00)

(0.18)

(0.08)

(0.13)

(1.43)

(0.31)

(1.52)

(0.32)

10.00

8.77

30.00

29.94

17.00

15.83

18.50

16.35

19.00

15.64

(0.11)

(0.08)

(0.46)

(0.21)

(0.40)

(0.24)

(1.20)

(0.33)

(1.51)

(0.40)

7.00

6.07

22.00

21.06

9.00

9.66

19.00

15.97

16.00

14.44

(0.05)

(0.06)

(0.27)

(0.14)

(0.29)

(0.17)

(0.36)

(1.62)

(0.38)

5.00

3.51

15.00

14.71

6.00

5.80

14.00

12.44

13.00

11.30

(0.08)

(0.04)

(0.17)

(0.13)

(0.06)

(0.08)

(0.76)

(0.22)

(0.83)

(0.22)

4.00

3.15

16.00

15.68

6.00

5.367

13.50

12.27

11.00

9.84

(0.05)

(0.04)

(0.23)

(0.11)

(0.11)

(0.08)

(0.98)

(0.26)

(0.94)

(0.30)

(1.47)

Table 2. Estimated parameters of the cumulative distribution function fitted to normalized development time frequencies for immature stages and survival time for adult life survival stages of P. gossypiella. Fitted function logit model. The numbers in parentheses are standard errors Intercepts (a) for temperature ( C) Life stage Egg

Larva

Pupa

Female

Male

Slope (b)

AIC

R2

224.06

0.95

136.16

0.84

283.23

0.90

143.47

0.90

153.64

0.89

15

20

25

30

35

-52.078

-40.33

-33.51 (1.98)

- 23.34 (1.31)

-21.31

18.57

(3.09)

(2.37)

(1.19)

(1.09)

-97.21

-72.91

-57.67

-59.04

21.45

(7.04)

(5.18)

(4.09)

(4.20)

(1.52)

-30.30

-29.94

-19.06

-18.19

10.84

(1.41)

(1.37)

(0.89)

(0.85)

(0.49)

-12.02

-15.17

-15.05

-13.69

-13.61

5.43

(1.22)

(1.51)

(1.51)

(1.39)

(1.39)

(0.52)

-9.72

-12.35

-11.99

-10.89

-10.27

4.49

(0.99)

(1.23)

(1.19)

(1.09)

(1.04)

(0.42)

-65.38 (4.68)

-24,.58 (1.11)

Table 3. Estimated parameters of the linear and non-linear models fitted to median development rates (1/days) for immature life stages of P. gossypiella. The numbers in parentheses are standard errors. Linear model: Test temperature range used for fitting linear relationship: Egg stage (15-35°C); larval stage (15-30 °C) and pupal stage (15 -38 °C). Theoretical lower development threshold (Tmin), calculated by intercept/slope, ignoring minus sign. Thermal constant calculated by taking inverse of slope (b) i.e. 1/b. Non-linear model: Values of Th and Tl in oK (for Life stage

Linear model a

b

Tmin

= oK-273).

Sharpe and DeMichele Model

DD

R2

F

df

p

P

To

Ha

Hh

Th

Tl

AIC

R2

F

df

P

72.99

0.97

92.83

1,3

0.00

0.17

297.84

16621.42

595843.10

308.43

287.17

-10.46

0.99

130.97

6,8

0.00

(0.004)

(0.00)

(0.00)

(0.00)

(0.04)

(0.90)

0.05

297.74

12032.10

393406.10

308.49

288.181

-28.70

0.99

228.95

6,8

0.00

(0.01)

(0.00)

(0.001)

(0.00)

(0.92)

(0.00)

0.13

300.28

14309.74

601602.57

308.48

284.00

-14.61

0.95

71.25

6,8

0.01

(0.00)

(1.27)

(0.00)

(0.00)

(0.07)

(0.00)

−

−

−

−

−

−

−

−

−

−

−

( C) Egg

-0.154

0.014

(0.04)

(0.00)

11.23

13 Larva

Pupa

Egg– Adult

-0.039

0.003

(0.005)

(0.00)

-0.076

0.007

−

−

11.37

11.00

11.20

285.71

144.92

503.62

0.99

0.97

−

303.21

146..60

−

1,2

1,4

−

0.00

0.00

−

Table 4. Estimated parameters of the non-linear model fitted to mortality rate for immature life stages of P. gossypiella. Fitted equation: Wang model. Numbers in parentheses are standard errors Life stage

Parameter estimates Topt

Egg

25.25 (0.23)

Larva

22.83 (0.35)

Pupa

27.14 (1.16)

B

Bl

4.30 (0.25)

-

5.39 (0.98)

Bh -

H

R2

F

df

P

0.04 (0.00)

-21.88

0.98

64.91

(2,2)

0.01

1.26 (0.13) 1.26 (0.13) 0.13 (0.00)

-29.91

0.99

1049.40

(3,1)

0.02

-8.83

0.88

7.54

(2,2)

0.01

-

-

AIC

-

0.07 (0.01)

Table 5. Estimated parameters of the non-linear function fitted to the mean senescence rates for adult life stages of P. gossypiella. Fitted equation: Stinner model. Numbers in parentheses are standard errors Life stage

Parameter estimates c1

Female

Male

c2

k1

k2

To

AIC

0.11

0.08

-12.58

0.63

21.66

(0.01)

(0.00)

(0.04)

(0.028)

(0.57)

1.94

0.11

-0.49

0.22

13.397

(0.78)

(1.17)

(5.59)

(9.52)

(4.13)

R2

F

-14.28

0.75

-11.34

0.67

df

P

7.52

4,10

5.10

4,10

0.005

0.02

Table 6. Estimated parameters of non-linear models fitted to temperature-dependent reproduction of P. gossypiella. Fitted functions: Gaussian with log model for total fecundity; Exponential modified for cumulative oviposition rate. Numbers in parentheses are standard errors. Temperature-dependent reproduction Total fecundity Tmin

Topt

(yo)

(To)

13.07

24.79

89.35

0.14

(3.35)

(0.21)

(4.95)

(0.01)

a

b

AIC

Cumulative oviposition rate R2

F

df

p

a

b

c

R2

F

df

P

0.94

1017.86

2,122

0.00

AIC

29.69

0.99

111.99

3,1

0.05

-0.27

1.82

0.08

(0.20)

(0.64)

(0.47)

-238.79

Table 7. Pectinophora gossypiella intrinsic rate of natural increase (rm), net reproductive rate (Ro), gross reproductive rate (GRR), mean generation time (T, in days), finite rate of increase (ƛ) and doubling time (Dt, in days) as mean (±SE) inferred for constant, fluctuating and real time daily temperatures, when reared on detached cotton bolls in laboratory. Numbers in parentheses are standard errors

Life table parameter

―

Stochastic simulations in laboratory (15-38°C) 0.03

―

Constant temperatures in laboratory 15°C

rm

―

Ro

―

GRR

―

T

―

ƛ

―

Dt

―

20°C

25°C

30°C

35°C

-0.01 (0.00)

0.06 (0.00)

0.07 (0.00)

-0.01 (0.01)

0.92 (0.20)

16.30 (1.71)

6.13 (0.45)

0.77 (0.22)

20.739 (3.96) 63.18 (0.88) 0.99 (0.00) 40.68 (29.96)

56.56 (3.91) 44.60 (0.07) 1.06 (0.00) 11.23 (0.44)

27.70 (4.29) 31.67 (0.14) 1.06 (0.03) 12.28 (0.56)

11.33 (1.67) 32.47 (0.10) 0.99 (0.01) 24.58 (32.97)

38°C

Simulations using real time daily temperatures from weather stations Hisar Nagpur Surat Junagadh Dharwad Coimbatore -0.004 (0.01)

0.01 (0.02)

0.04 (0.01)

0.01 (0.03)

0.02 (0.02)

0.039 (0.01)

4.30

0.79 (0.59)

2.44 (0.01)

5.29 (3.08)

2.69 (1.99)

3.16 (2.02)

5.65 (3.21)

―

38.24

―

51.96

―

1.03

―

24.69

28.18 (5.08) 88.13 (2.77) 0.99 (0.01) 41.55 (6.75)

29.60 (7.51) 53.48 (1.79 1.01 (0.02) 25.12 (4.26)

36.05 (5.28) 41.44 (1.41) 1.04 (0.01) 18.78 (7.42)

27.141 (2.28) 51.87 (3.07) 1.01 (0.03) 32.85 (8.98)

24.66 (3.10) 51.52 (1.84) 1.02 (0.02) 16.07 (2.69)

32.73 (9.50) 42.85 (1.22) 1.04 (0.014) 18.57 (6.67)

Highlights •

Threshold temperatures and thermal requirements for pink bollworm were estimated and validated

•

The developmental thresholds of 13.4oC/35.5oC and thermal requirements of 503.62 DD were estimated for development from egg to adult emergence

•

Simulation of life table parameters provided reasonably closer estimates across the tested locations

•

The estimated thresholds precisely predicted the pink bollworm developmental events under field conditions

1

Conflict of interest The authors declare that they have no conflict of interest