Introduction

Globally, an estimated 1,300 insect species are reported to interact with cotton plants1. In India, a significant portion of this diversity is present, with nearly 251 species documented2. These pests inflict substantial losses on harvests every year. Prior to the introduction of genetically modified (Bt) cotton hybrids, spotted and old-world bollworm posed the most serious and recurring threats3. The pink v season synchronizing the last pickings causing no economics damage.

The pink bollworm (Pectinophora gossypiella) is one of the important pests of cotton, causing significant damage if left uncontrolled. It can seriously restrict yield, although infestations vary across seasons and locations4. Interestingly, the pink bollworm was first identified in 1843 by Saunders as Platyedra from specimens collected from India in 18425. The pest is now found in numerous countries across Asia, Africa, North America, Central America, South America, Europe, and Oceania (CABI). After the introduction of Bt cotton in 2002 (central and south zone) and 2005 in North zone PBW incidence was negligible in India. Over time, pink bollworm populations developed resistance to the Cry toxins (Cry 1Ac) during 2009 and subsequently to Cry1Ac and Cry2Ab during 2014. By 2016 and 2017; field failures due to pink bollworm resistance became evident in central zone as well as south zone growing cotton both under irrigated and rainfed conditions. PBW began to make its presence in the North Zone in 2018 onwards. States like Gujarat, Madhya Pradesh, Maharashtra, Karnataka, Andhra Pradesh, and Telangana have experienced yield losses of up to 30%6,7.

Pink bollworm has emerged as a significant threat to Bt-cotton cultivation across various regions in India, including the central, south, and north zones. Field studies indicated the development of resistance in pink bollworm populations to Bt cotton expressing Cry1Ac and Cry2Ab toxins8. This resistance allows them to infest even late-season cotton crops in all cotton growing states7,9,9,10,12.

The ICAR-All India Coordinated Research Project on Cotton (AICRP on Cotton) having well established research network in cotton played a pivotal role in India’s cotton progress over the past five decades. This initiative effectively utilized the research network of State Agricultural Universities (SAUs) involved in cotton research. Originally launched with 15 research centres, it has expanded to a network of 22 centres across 17 SAUs having main objective to develop cost-effective and efficient strategies for management of pests and diseases under varying agroecological conditions in the country (https://aiccip.cicr.org.in/).

As an evolutionary strategy to exploit favourable environmental conditions for growth and reproduction, insect pests exhibit remarkable seasonal variations in their population abundance. The change in dynamics from late season pest to an early invader in absence of other major bollworms like old world bollworm, spotted bollworm etc. is again need attention. This article aims to evaluate current status of pink bollworm infestations across various cotton-growing regions in India vis-a-vis the process of resistance development. By understanding the timing and peak activity periods of insect pests relative to a crop’s growth stages, appropriate management plans can be developed at the national level. The population dynamics data on Pink bollworm recorded under unsprayed condition helped in understanding the process of resistance development and final establishment of resistant population in India verified through series of weekly surveys carried out at farmers’ field.

Results

The data on green boll damage in each zone, due to pink bollworm from 2007 to 08 to 2022-23 have been presented in Table 1 (north zone), Table 2 (central zone), Table 3 (south zone), respectively. Table 4 represents the zone wise mean fruiting Body/ green boll damage (%) due to pink bollworm under unprotected conditions. The data recorded during every Standard Meteorological Week (SMW) on fruiting bodies (green bolls in this study) particularly for PBW of each zone and overall year wise average of each zone was also calculated and presented (Supplementary Tables 1, 2 and 3). An analysis of the data reveals the varying status of pink bollworm infestation across different cotton growing zones of India. Figure 1 represented the zone wise mean Green Boll Damage (%) due to Pink Bollworm under Unprotected Conditions during pre (2007–2013) and post (2014–2023) resistance development phase; whereas Figs. 2, 3 and 4 depicted Standard Meteorological Week (SMW) based Green Boll Damage (%) under Unprotected Conditions in Central, South and north Zone during pre (2007–2013) and post (2014–2023) resistance development phase, respectively.

Table 1 Green Boll damage due to pink bollworm in different states of India during 2007to 2023 (North Zone).
Full size table
Table 2 Green Boll damage due to pink bollworm in different states of India during 2007 to 2023 (Central Zone).
Full size table
Table 3 Green Boll damage due to pink bollworm in different states of India during 2007to 2023 (South Zone).
Full size table
Table 4 Average of Zonal Fruiting Body/ Green Boll Damage (%) due to Pink Bollworm under Unprotected conditions.
Full size table
Fig. 1
figure 1

Zone wise mean Green Boll Damage (%) due to Pink Bollworm under Unprotected Conditions during pre (2007–2013) and post (2014–2023) resistance development phase.

Full size image
Fig. 2
figure 2

Standard Meteorological Week (SMW) based zonal mean of Green Boll Damage (%) under Unprotected Conditions in Central Zone during pre (2007–2013) and post (2014–2023) resistance development phase.

Full size image
Fig. 3
figure 3

Standard Meteorological Week (SMW) based Green Boll Damage (%) under Unprotected Conditions in South Zone during pre (2007–2013) and post (2014–2023) resistance development phase.

Full size image
Fig. 4
figure 4

Standard Meteorological Week (SMW) based mean Green Boll Damage (%) under Unprotected Conditions in North Zone during pre (2007–2013) and post (2014–2023) resistance development phase.

Full size image

Central zone

The central zone is known to cultivate maximum area under cotton among three cotton growing zone of India. Data on pink bollworm infestation were collected from several key cotton-producing regions of central zone in India. Detailed information regarding the pink bollworm status in each of these centres under irrigated and rainfed conditions is provided below. In central zone 6 locations of Maharashtra (Nanded, Akola and Rahuri), Gujrat (Junagadh, Surat) and Odisha (Bhawanipatna) were selected for study. As Bt cotton was introduced in central and south zone during 2002 and BG-II cotton during 2006 as an resistance management strategy in bollworms to cry proteins.

The green boll damage in Bt cotton due to pink bollworm (%) ranged between 0 and 35.63, 0–51.00 (rainfed) 0.92–30.95 (irrigated), 4.25–15.23 (Rainfed), 0.88–6.32 (Irrigated), respectively at Nanded, Akola, Rahuri (Maharashtra State), Surat, Junagarh (Gujrat State). In non-Bt cotton green boll damage (%) ranged between 0 and 49.20, 7.0–54.0 (rainfed) 9.28–34.41(Irrigated), 4.47–26.21 (rainfed) and 4.24–18.15 (Irrigated), respectively at all above locations including 0–3.33(%) at Bhawanipatna. In central zone the incidence above ETL in Bt was recorded in 2014 (Nanded), 2016 (Rahuri and Surat). In case of non-Bt the green boll damage above ETL was observed earlier than the Bt genotypes, 2013 in Nanded, 2007 in Rahuri, 2010 in Akola, 2009 in Surat, 2012 in Junagarh but green boll damage below was ETL in Bhawanipatna. In central zone in Maharashtra at Nanded and Akola location, highest green boll damage due to PBW was recorded during 2017 in non-Bt genotype and Bt genotypes. When compared between Bt and non-Bt genotypes, at Rahuri irrigated location, highest green boll damage due to PBW was recorded during 2021 in non-Bt and Bt genotype. In Gujrat, at Surat (Rainfed) location, highest green boll damage due to PBW was recorded during 2016 in non-Bt genotype and during 2021 in Bt genotype. In Gujrat, at Junagarh (irrigated) location, highest green boll damage due to PBW was recorded during 2022 in non-Bt genotype and during 2021 in Bt genotype. In the state of Odisha where Bt cotton is not being cultivated, but highest green boll damage (3.33%) in non-Bt genotype due to PBW was recorded at Bhawanipatna during 2018.

The overall zonal average within a year in Central zone (all locations) recorded no green boll damage due to PBW in Bt cotton till 2011. The green boll damage recorded in Bt cotton after 2012 (0.0–1.67%) and its incidence above Economic threshold level was recorded after 2015 (10.03%). In non-Bt cotton genotypes green boll damage due to Pink Bollworm was recorded from 2007 onwards wherein it persisted above ETL. A declining trend in green boll damage in Bt-cotton was recorded after 2021 onwards both in Bt as well as non-Bt genotypes (Table 4) may be attributed to less carryover due to implementation of management strategies. During 2009-13 phase green boll damage due to PBW was first recorded after 42nd SMW onwards in non-Bt and 48th SMW onwards in Bt genotype but during 2014-23 phase, green boll damage recorded from 36th week onwards both in Bt and non-Bt genotype (Supplementary Table 1) indicating its earlier appearance particularly the resistant population.

The weekly data were recorded (Standard Meteorological Week wise) on non-Bt and Bt-genotype and assessed for studying difference in green boll damage. Between 2009 and 14, pre-resistant development phase, difference in green boll damage in Bt and non Bt genotypes ranged between 0 and 60%, with a higher incidence in non Bt genotypes. Whereas between 2014 and 23, the difference green boll damage (%) between Bt and non- Bt genotypes was ranged between 1.47 and 16.98%. The reduced difference in green boll damage recorded in non-Bt and Bt assumed survival and establishment of resistant individual are dominating, affecting both Bt and non-Bt equally (Supplementary Table 1).

South zone

In South zone, green boll damage due to PBW was observed since 2007 in Dharwad, 2011 in Raichur and 2018 in Chamrajanagar both in Bt and non-Bt. The green boll damage (%) in Bt –genotype ranged between 1.89 and 31.00 (Dharwad), 4.55–64.15 (Raichur), 5.87–14.23 (Chamrajnagar). In non-Bt genotype, green boll damage (%) due to PBW was 4.95–56.00, 10.45–73.33and 4.98–19.23, respectively in South zone locations. In South zone highest green boll damage at Dharwad location was recorded during 2023 (18.58%) in Bt and (20.92%) in non-Bt. In Raichur, highest damage in Bt and non-Bt was recorded during 2017 (64.15 and 73.33%). In case of Chamarajanagar, the highest damage due to PBW in the form of green boll damage was recorded during 2020 (14.23) in Bt and during 2022 in non-Bt (19.23%).

In South cotton growing zone of India, average zonal (three locations) green boll damage (%) due to pink bollworm was noticed since 2007, 4.84(1.89–20.92) to highest 34.69 (5.23–64.15) during 2017 but its presence above ETL was observed after 2017 onwards in case of Bt genotypes. The non-Bt genotypes were infested by pink bollworm since 2007, recorded above ETL, 22.72%. The highest mean green boll damage 41.37% recorded during 2017. The green boll damage due to Pink Bollworm noticed above ETL during the period of study (Table 4).

Based on weekly data recorded on green boll damage (Standard Meteorological Week wise) between 2009 and 13, pre-resistant development phase the difference in green boll damage in Bt and non Bt genotypes ranged between 0 and 26.72%, non Bt genotypes recorded with higher incidence. Whereas between 2014 and 23, the difference Bt and non Bt was ranged between 0 and 16.44%. The difference green boll damage recorded in non-Bt and Bt genotypes in South zone was probably less in South zone in comparison to Central zone because the appearance of PBW in South zone cotton is generally from 44th SMW onwards both 2009-13 and 2014–2023 phases, wherein survival of resistant moths of pink bollworm and its impact was rapid, affecting both Bt and non-Bt equally (supplementary Table 2).

North zone

No incidence of PBW was observed either on Bt or non-Bt genotypes at all locations studied till 2011 in North zone. The incidence of green boll damage due to PBW in non-Bt was recorded since 2012 in North zone only at experimental sites cultivating both Bt and non-Bt genotypes for experimental purpose only. However, in non-Bt genotypes, in Punjab (Bathinda) and Rajasthan (Sriganganagar) average population above ETL was noticed during 2015 and 2012, respectively but in Haryana the green boll damage due to Pink Bollworm in non-Bt was recorded after 2012. The damage recorded in non-Bt genotype was 03.00–17.38% (Bathinda), 5.14–29.83% in Hisar, 07.04–34.0% in Sirsa and 2.37–76.0% in Sriganganagar (Rajasthan). In case of Bt-hybrid green boll damage (%) was observed in 2018 at Bathinda (Punjab), since the study location was confined very near to cotton ginning cum oil extraction mill, 2019 in Hisar as well as 2020 in Sirsa (Haryana) and 2021 in Sriganganagar (Rajasthan). In Punjab (Bathinda) it ranged between 3.78 and 25.71. In Haryana, 0.00–24.50 and 0.0–20.50% in Hisar and Sirsa; 0.0–32.50%in Rajasthan (Sriganganagar). In North zone in Punjab (Bathinda) highest green boll damage in Bt- genotype was recorded during 2021 and non-Bt genotype during 2015 (17.38%). In Haryana at locations of Hisar and Sirsa, highest green boll damage due to PBW was observed during 2021 (24.50%) in Bt, 29.83% in non-Bt. In Sirsa highest green boll damage in Bt (20.50%) and non-Bt (34.00%) during 2021. In Sriganganagar (Rajasthan) highest green boll damage (%) in Bt-genotype was during 2023 and non-Bt was recorded during 2021.

In North cotton growing zone of India, based on average of five locations of zone green boll damage due to pink bollworm was recorded since 2018, 0.95 (0.0–3.78%) to highest 20.75 (10.0–32.50) during 2023 but its presence above ETL was observed after 2021 onwards in case of Bt genotypes. The non-Bt genotypes were infested by pink bollworm since 2012, recorded above ETL green boll damage (%), 12.52 (10.60–14.17%) since 2013 onwards (Table 4).

It clearly indicated that the cotton–wheat cropping system does not allow the extended crop duration wherein more than 99% area under cotton was under Bt genotypes at farmers field locations. Resistant development activity has not been possible due to timely termination of cotton crop for wheat sowing in preceding season but the resistant bollworm population transported from south and central zone to North was established within two-three years, equally affecting the Bt and non-Bt genotypes. Based on the above data it is clearly evident that, 2009-13 and 2014-23 phases of development for PBW survival as such has not occurred in North zone (supplementary Table 3).

Pink bollworm proportionate infestation in North, Central and South Zone during 2016–2023 at farmers field locations

The majority of the area under cotton is occupied by the BG-II hybrids. The farmer’s field location surveys were conducted from 2016 onwards. In the North Zone, the percentage of locations exceeding the ETL (green boll damage > 10%) ranged from 0.00 to 49.65% between 2016 and 2023. During the initial years (2016–2020), very few locations crossed the ETL. However, there was a significant rise starting from 2021, reaching a peak of 49.65% in 2023.In the central zone, the percentage of locations crossing the ETL varied between 4.76 and 26.66%. The highest number of locations crossed the ETL in 2017, while the lowest occurred in 2022. Overall, the trend has been decreasing since 2017. The south zone witnessed the highest number of locations crossing the ETL in 2017 (25.65%). The lowest number of locations exceeded the ETL in 2023 (9.37%). In Both central and south zone, the locations above ETL showed a decreasing trend and similarly the average green boll damage due to Pink Bollworm also exhibited the same trend (Table 5). The decreasing trend in south and central zone and alarming rise in north zone due to carryover through stacked cotton stalks and stored cotton seed in ginneries is a matter of concern and discussion warranting lot of research.

Table 5 Farmers Field: Pink Bollworm proportionate infestation in North, Central and South Zone during 2016–2023.
Full size table

Discussion

The introduction of Bt cotton marked a significant advancement in cotton cultivation practices worldwide, including India. The approval of Bt cotton in 2002 offered a promising solution to address the challenges faced by the Indian cotton sector. The Genetic Engineering Appraisal Committee (GEAC) initially permitted Bt cotton cultivation only in the central (Gujarat, Maharashtra, Madhya Pradesh) and South (Tamil Nadu, Andhra Pradesh, Karnataka) zone. GEAC given its approval got cultivation of Bt cotton in the north zone in 2005 season onwards. Currently, 96% of cotton being cultivated in India is Bt cotton, predominantly Bollgard II. Six Bt cotton events incorporating single and double genes have been approved by GEAC during 2002–2014. Four other Btcotton technologies are approved also but they are not in commercial use13,14.

Single-gene Bt cotton hybrids occupied the majority of cultivated area during 2002–2009. Double-gene Btcotton adoption witnessed a significant rise from 2009 to 10 onwards14. The development of resistance by PBW to single gene Bt cotton was reported in 2009 and to double gene Btcotton in 2014 from Gujarat8. The data recorded by different AICRP centres from central, south and north zone revealed that Bt cotton technology initially demonstrated significant success in controlling various bollworms, including PBW. This led to minimal PBW infestation during the first decade (up to 2013) of Bt cotton use. But the PBW has re-emerged as a major threat in central- southern cotton belts from 2014 onwards and 2018 onwards in northern zone. It was advised to grow Bt cotton with a permanent directive to comply with refugia either 5% unsprayed or 20% sprayed as a structured refuge. On the other hand, several unfeasibility conditions of the non-Bt refuge being non-isogenic to the main Bt genotype led to adopters’ inadequate adherence to the refugia standards. This has impacted more on pest species (PBW) which is known as functional monophagous and always appear late during the season where the chances of survival on Bt cotton increases particularly at places where crops are extended for more more harvest. The ecological advantage of diapauses mechanisms of different durations in all zones also helped in survival of larval stages of PBW throughout the year and for generation carryover. There was continuous selection pressure on the populations of PBW those were selected for resistance for Cry proteins that went unnoticed and later resulted as development of substantial resistance in PBW to both single (Bollgard) and double-gene (Bollgard II) Btcotton hybrids11. Following this, numerous researchers including9 Dhuruva and Gujar (2011)15, Tabashnik and Carriere (2019)10, Kranthi (2015)7, Mohan et al. (2016)16, Naik et al.. (2020)11, and Kumar et al. (2020)12 reported severe pink bollworm infestation in all cotton-growing zones of India, as well as the development of resistance to Cry 1 Ac and Cry 2Ab.

In the population dynamics studies for insect pests of cotton carried out at AICRP centers, pink infestation levels were lower in Bt/BG-II hybrids starting in 2007 and above ETL levels in non-Bt genotypes, with the exception of the North Zone, where non-Bt genotypes showed signs of infestation starting in 2012. In Bt hybrids, however, the infestation was not significantly different between Bt and non-Bt genotypes in terms of green boll damage until after 2018. The variation in the seasonal mean of green boll damage (%) between Bt and non-Btgenotypes at our experimental sites amply demonstrated that PBW resistance to cry protein developed gradually over a period of five years, eventually becoming established as a result of population carryover from off-season survival sources. Additionally, it is suggested that seeds may have carried the established resistant population to the North Zone12. Given that cotton is the only host and that the pink bollworm typically feeds inside flowers (rosettes) and bolls in the late season, resistance to the pest has developed, with poor refuge compliance and prolonged crop duration hastening the process. Pink bollworm (PBW) infection in Indian cotton fields has recently increased, which brings to light possible issues with the effectiveness of second-generation Bt cotton technology (Bollgard-II) for PBW control. The results of the farmer field location surveys clearly showed how serious the issue was in the north zone; however, current data has shown that the incidence in the central and south zones has decreased. This necessitates potentially the adoption of alternative or integrated pest management strategies to ensure sustainable cotton production and protection of farmer livelihoods. Window-based management techniques that emphasize reducing off-season sources of survival of PBW to prevent further carryover in the next season are validated and being advised through AICRP on Cotton in the country.

The occurrence of bollworm in cotton was reduced with the introduction of Bt cotton. The Bt cotton was introduced with Standard Operation Procedure (SOP) of refugia (non-Bt) at the periphery of main (Bt) cotton field but extremely poor refuge compliance due to practical feasibility was noted. Due to their polyphagous or oligophagous character, the two bollworms species, Helicovepa armigrea and Earaisspp., were unaffected by low refugia compliance. PBW, a functional monophagous pest that emerges in the late season, has developed resistance to cry protein as a result of exposure to sublethal levels of the protein. The pest first appears in the late season, however reports of it appearing in the Central, South, and early seasons in the North have indicated that it first appears in the midseason17. In order to lessen the spread of diapausing larvae, the study recommends keeping a careful eye on the pests and doing appropriate management studies throughout the offseason. The initial success of Bt cotton in controlling pink bollworm (PBW) diminished over time. Resistance to Bt toxins emerged, leading to increased PBW populations and damage. The central and southern regions experienced this earlier, followed by the northern region. While the initial resistance was low, it gradually increased, necessitating integrated pest management strategies to sustain Bt cotton’s sustainability.

Methods

Population dynamics under unprotected conditions: Cotton planting in India is grouped into three distinct agro-ecological zones comprising 11 states viz. Northern (Punjab, Haryana and Rajasthan), Central (Gujarat, Maharashtra, Madhya Pradesh and Odisha) and Southern zone (Andhra Pradesh, Telangana, Tamil Nadu and Karnataka). Field trials on seasonal dynamics of insect population of cotton were conducted annually at all AICRP research centres across these zones. Bt cotton (Cry1Ac) was initially introduced for Central and South zone (2002) and later to North zone (2005). With the subsequent approval for BG-II (Cry1Ac and Cry2 Ab) in 2006 across India, the systematic pest surveillance on these pests from 2007 to 2023 has been analysed Cotton genotypes from non-Bt and Bt/BG-II backgrounds were sown at experimental farms in an area of 500 sq. meter for each genotype (total 2000 sq. meter). Both BG-II and non-Bt genotypes were selected for the study to align the cultivation practices of local growers and their compatibility. While non-Bt genotypes remained consistent throughout the study period; however, the selection of Bt/BG-II cotton genotypes varied in accordance with the changing cultivation patterns among growers in the region.

Observations

The dynamics data recording initiated one month after sowing. Economic Threshold Level (ETL) to initiate the management action is based on the trap catch data (5–8 moths /trap for 3 consecutive nights), 10% rosette flowers or 5–10% green boll damage (at specific intervals: 90, 105, 120, 135, and 150 Days After Sowing). In the current study the weekly green boll damage by PBW data was recorded at the boll formation stage of the crop, through destructive sampling of 20 bolls per genotype, or 20 bolls per acre or 50 bolls per ha.

Pest surveillance across farmers’ fields

Similarly, to assess the ground situations, weekly random surveys were also conducted at farmers’ fields’/locations of all the three zones to record PBW incidence and Economic Threshold Level (ETL). During each survey, a total of five or more locations from five different villages were monitored wherein 20 bolls from each location was examined following uniform proforma for each location. The pink bollworm incidence was monitored through the rosette flower formation at the flowering stage and later through the destructive sampling of green bolls.

Statistical analysis

Mean separation of various parameters was conducted with α = 0.05 level of significance using SAS statistical software version 9.4 (SAS Institute Inc. 2016. SAS® 9.4 Language Reference: Concepts, Sixth Edition. Cary, NC: SAS Institute Inc.). The figures are prepared using ‘Graph builder’ function of SAS statistical software version 9.4.