Present status of Papaya Mealybug, Paracoccus marginatus Williams and Granara de Willink, in Assam, India, after a decade of its first invasion

Abstract

Background

The North Eastern Region (NER) of India is well known for its rich biodiversity and organic cultivation; however, this is one of the least investigated regions owing to its remoteness. A field study on papaya mealybug (PMB) was conducted to know its present status in Dibrugarh district of Assam, NER India, after its first entry in 2012.

Results

The pest was initially confined in urban and peri-urban localities in 2012 and has now made its entry even in remote villages too; however, many villages still remain uninfested. PMB has not damaged crops much the way it did in major papaya producing states of India. Out of 217 farmers surveyed, only 31.8% have experienced the infestation of PMB in their crops. The pest has now been recorded in places within an elevation of 98–129 m above MSL. The village homesteads help the pest establish in the ecosystem through natural host shifting. 89.9% farmers adopted either no management practices or applied non-chemical measures. We found the presence of more number of Spalgis immatures in the colonies of PMBs in hibiscus than in papaya. After the first invasion of PMB in Assam, initially it was also worried that the pest might invade tea crop and affect the tea economy of the state; however, no report on PMB infestation on tea crop has been found so far.

Conclusions

The PMB has acclimatized and established itself in the crop ecosystem of Assam by natural host shifting. The trend of infestation is constant or increasing. No programme on classical biological control of PMB was taken in the farmers’ fields of the state, but there is no hue and cry situation on the crop damage by PMB. High rainfall affected the spread of the pest and predation by Spalgis sp might have resulted in reduction in population. We recorded variable abundance of S. epeus larva in PMB colonies in different host plants based on which we can formulate the bio-control module for PMB. The detailed study on the role of rainfall and natural enemies on population dynamics of PMB is a researchable issue.

Background

The papaya mealybug, Paracoccus marginatus Williams and Granara de Willink (Hemiptera: Pseudococcidae), is a highly polyphagous invasive pest that affects more than 200 plants (Garcia et al., 2016), many of which many are of economic importance. In the oriental region, the pest was recorded for the first time in Indonesia (Java) and India (Tamil Nadu) in 2008 (Muniappan et al., 2008). In India, variable losses due to Papaya mealybug (PMB) were estimated in different crops (Ayyasamy & Regupathy, 2010; Regupathy & Ayyasamy, 2012; Shylesha et al., 2010; Selvaraj, 2012). Macharia et al. (2017) reported a mean yield loss of 91% on papaya due to PMB infestation in Kenya and the Horticulture Crops Directorate estimated a national economic loss of US$29.8 million in 2017 (Kansiime et al., 2020). PMB invaded relatively later in the North East Region (NER) of India and was reported from Dibrugarh district of Assam during September, 2012 (Sarma, 2013). The pest had entered the region presumably with the infested papaya fruits and invaded initially the localities near to the markets with the trade of papaya fruits imported from outside the NER, and thus, the pest was initially confined to urban and peri-urban areas only (Sarma, 2013).

The North Eastern Region (NER) of India comprising eight states, viz. Sikkim, Arunachal Pradesh, Assam, Meghalaya, Nagaland, Mizoram, Manipur, and Tripura, is known for its rich biodiversity. These NE states occupy 52.03% of the Eastern Himalayan region (Sharma et al., 2008). The state of Assam hosts parts of two global biodiversity hot spots—the Indo-Burman and the Himalayan (Myers et al., 2000). An entry of an invasive pest may pose a threat to this hot spot’s biodiversity. Therefore, periodic surveys of the already invaded exotic species such as PMB in this zone are felt necessary. The ability of peasant farmers in the third world to monitor environmental occurrences around them has been ignored (Atteh, 1984) which is also true for the farmers of NER of India. However, they can provide genuine information on agricultural issues like pest outbreak and invasion of new, exotic pests. Invasion and damage by an exotic pest like PMB is unique, and a farmer can easily recognize it, if they are made acquainted with the pest and its nature of damage. It is becoming easier nowadays with the use of smart phones by many farmers. Moreover, progressive farmers can provide/receive information of horizontal spread of a pest in his/her nearby villages if they are asked for. Since papaya is not a major crop in NER India, sophisticated methods like remote sensing tools would fail to work on it to judge its horizontal spread. Remote sensing data have the potential to distinguish damage by Mealybug and quantify its abundance in cotton in Haryana (Singh et al., 2016). It is primarily because the damage symptoms are produced in large cotton areas. In villages of Assam, papaya is not grown as a crop in large acreage. Almost every household has a few papaya plants in their homestead (locally called as BAARI) where diverse crops/herbs are grown for different purposes, i.e. from vegetable/fruits to medicinal use. Many times, these few papaya plants are also not grown in the same place/yard. Therefore, the symptoms of PMB attack in Assam may not be perceivable by remote sensing satellite. Therefore, even though it is time-consuming, it is felt worthy to survey the farmers individually to know the spread of PMB. Moreover, no report was made on the existing status and extent of horizontal spread of PMB after its first invasion reported from Dibrugarh district of Assam by Sarma (2013). We hypothesized that P. marginatus has invaded more villages over time and farmers managed the pest by different means. Therefore, a survey was conducted during 2020–2022 in order to know—(i) the territorial extension of the pest after a decade of its first invasion in the district, (ii) the management practices adopted by the farmers, and (iii) ecosystem support, if any, where no control measures were taken up by the farmers.

Methods

The present survey was conducted in Dibrugarh district of Assam during March 2020 and December 2022 in order to know its horizontal spread, extent of establishment in the new ecosystem, and the present status of infestation in a gap of a decade. The said district has been considered for this study since an initial survey in 2012 was conducted in the same district through personal visits to farms based on the report from farmers/extension workers of the State Department of Agriculture, Dibrugarh. No survey report on initial invasion of the pest from other districts of Assam has been documented. In the present survey (2020–2022), farmers were made contact over telephone personally based on the telephone inventory maintained by Krishi Vigyan Kendra (Farm Science Centre), Assam Agricultural University, Dibrugarh, followed by periodic visits to the villages. The respondent farmers (217 nos.) were selected randomly from 36 villages of 7 developmental blocks of the district. Most of the farmers surveyed during 2020–2022 were associated with the Krishi Vigyan Kendra (KVK), Dibrugarh, either as participatory farmers of On-Farm-Testing, Front-Line-demonstration, trainings, and awareness programme or as beneficiaries of other government scheme. Most of the farmers were well informed about PMB through trainings, and awareness programmes conducted by the KVKs or other stakeholders since its entry in 2012. The second survey was initiated during the lockdown period of COVID pandemic (March 2020), and farmers were informed over telephone about the PMB, its mode of infestation, and life stages of Spalgis (a natural enemy of PMB) by sharing photographs and videos through WhatsApp. Field visits were made on several occasions to confirm the infestation for the doubtful cases of PMB infestation and establishment of the pest by observing it on few common host plants available in the ecosystem. The abundance of S. epeus larva in a PMB colony was counted in China rose, Custard apple, Guava, Holy basil, Land Lotus, Papaya, and Rose in randomly selected PMB colonized stems of 10 cm length. We observed 5 plants of each species in each village. The visits to tea plantations of the small tea growers were also made to check PMB infestation, if any, in tea bushes. The farmers were interviewed based on a pre-prepared questionnaire to get the information desired. If the PMB’s infestation was confirmed during the interview itself, the farmer was asked to share photographs on PMB infesting papaya leaves/fruits for further confirmation. For any doubtful information received from farmers, the personal visits were made for confirmatory identification of the pest. Other related information such as time of first invasion, present status of infestation, and management practices adopted was also gathered through personal interaction with the farmers. Traditional or indigenous knowledge refers to any knowledge, novelty, or practice of the indigenous local people and communities in general (Jasmine et al., 2016); hence, Indigenous Technological Knowledge (ITK) used, if any, by the farmers for managing PMB was also surveyed. The input gathered during 2012–2022 through various extension activities (training, group discussion, field day, etc.) of KVK, Dibrugarh, made at farmers’ level has also been considered for drawing conclusions. In order to get confirmatory evidence on few aspects in other districts, pertinent information was also collected by surveying a few locations of two other districts of different ecological zones, viz. Nalbari district situated in the Lower Brahmaputra valley Zone and Biswanath district of the North Bank Plain Zone of Assam, India.

Results

Demographic profile of the respondent

The respondent farmers belong to Schedule Caste (SC), Schedule Tribe (ST), Other Backward Classes (OBC), Tea tribe, and others as shown in Fig. 1.

Fig. 1

Demographic profile of the respondent farmers

We came across farmers of different age and education level. As high as, 49.77% farmers belong to an age-group of 20–35 years followed by 33.64% of 36–50 years and 16.59% above 50 years. Likewise, 47.0% farmers have an education up to 10th standard, 41.47% of 10th–12th standard and 11.52% farmers are graduates.

Mode of entry of PMB in Assam

The infestation of PMB was first observed in India in July 2008 at Coimbatore (Muniappan et al., 2008), whereas it was first observed in Dibrugarh, Assam, in September 2012 (Sarma, 2013). The aerial distance between these two places is about 2600 km (https://www.distancecalculator.net/), and this distance was covered in 49–50 months (i.e. @ 1.7 km/day) which indicates that PMB did not fly itself to reach Dibrugarh. It further confirms that the pest entered Assam through trade material presumably through papaya fruit (Sarma, 2013). Long distance transmission through trade material has also been reported (CABI, 2020).

First invasion of PMB in Assam

Even though the invasion of PMB in Assam was reported scientifically for the first time by Sarma (2013) from Dibrugarh district, the pest entered the districts of Lower Brahmaputra valley Zone (LBVZ) of Assam earlier than in Dibrugarh which is situated in the Upper Brahmaputra valley Zone (UBVZ). Preliminary information on its earliest invasion in LBVZ (including the Guwahati city, the state capital) was also confirmed from the feedback of many people including farmers in response an article on the pest published in Assamese language in Prantik (1–15 August 2013; pg: 25)—a reputed Assamese fortnightly magazine. About 15 persons of Kamrup (Metro) district have informed that the PMB invaded their homestead gardens in last part of 2011 or early part of 2012.

Slow spread of PMB to rural areas

The pest was initially confined in urban and peri-urban localities of Dibrugarh in 2012 (Table 1) and has now made its entry in remote villages too (Table 2). It has also invaded the villages near to the bank of mighty river Brahmaputra as well as the bordering villages of other adjoining districts. Being a polyphagous species and seeing the intensity of its damage in major papaya growing states of India, it was thought that PMB would spread the entire districts within a year or two. The present survey has confirmed that the pest has established in the agro-ecosystem of Dibrugarh and the trend of infestation is either constant or increasing. About 2–3% villages are still remaining uninfested; these villages are surrounded by tea gardens where regular spraying of insecticide is done which might have prevented the entry/establishment of the PMB.

Table 1 PMB invaded area as observed in Dibrugarh, Assam, in 2012

Table 2 Farmers response on PMB infestation in different blocks of Dibrugarh district, Assam, India (2020)

Fig. 2

Area invaded by PMB in 2012 and thereafter in Dibrugarh district, Assam

As observed in the present surveys, the pest attacked initially on papaya and hibiscus in its initial invasion in a new locality; later on the pest establishes successfully in homestead gardens/crop fields, but degree of invasion or intensity of attack reduces over time. Many farmers also have the opinion that pruned plants get less infested by PMBs next year. Similar observation was also noticed in other districts, viz. Biswanath and Nalbari district of Assam.

No infestation to tea plantation

It was initially worried in 2012 that the pest could invade the tea crop and may affect the economy of the state in future (Sarma, 2013), since tea is the main exporting material. However, no infestation of PMB in the tea crop has been found so far in Dibrugarh and Biswanath district. The pest has established in the other crop ecosystem, e.g. Papaya, Custard apple, Guava, Rose, Land Lotus, China rose, Holy basil, etc., but as a whole there is no hue and cry on this issue among the rural farmers of Assam now.

Both biotic and abiotic factors worked against the PMB

There was no mass release of imported bio-agent under any classical biological control programme in Assam at farmers’ level, except a symbolic release of Acerophagus papayae in KVK, Kamrup, Assam, by the National Bureau of Agricultural Insect Resource (NBAIR), Bengaluru, Karnataka, India. The pest has not become a menace in Assam like that in major papaya growing states of India, which is an indication of the profound role of the native natural enemies in suppression of this exotic species. Indian Apefly, Spalgis epeus (Westwood) (Lepidoptera: Lycaenidae), a natural predator of mealy bugs, has played a crucial role against the pest and kept the agro-ecosystem resilient against this highly invasive species. The presence of Spalgis in both papaya and hibiscus was initially reported to us by a few farmers and was confirmed later by field visits. Many researchers identified different predatory insect species on PMB (Ayyasamy & Regupathy, 2010; Tanwar et al., 2010; Saengyot & Burikam, 2011; Mastoi et al., 2015); however, we observed the Spalgis epeus larva in PMB colonies in every host plant we observed. No other predator species were omnipresent like S. epeus. We found the abundance of S. epeus larva in a range of 0–3 per colony (in 10 cm length of PMB colonized stem) in different host plants, viz. China rose (0–3.0) > Papaya (0–2.6) > Land Lotus (0–2.1) > Custard apple (0–1.5) > Guava (0–1.3) > Rose (0–0.75) > Holy basil (0–0.6). Of these hosts, the presence of PMB and S. epeus larva in China rose was noticed almost throughout the year. It might be due to the leave geometry of the China rose plants where leaves are plenty, close to each other, a situation preferred by the retiring S. epeus adults to oviposit on the PMB colonies. Such compact leave canopy also prevents the washing out of PMB colony by rainfall to some extent and assure life cycle of S. epeus on PMBs. The average rainfall in Dibrugarh district is about 2110 mm, and the south-west monsoon contributes about 1340 mm (63.5%) during June–September (Guhathakurta et al., 2020). Such heavy rainfall, particularly during monsoon, hindered the spread of the pest and is primarily responsible for slow territorial expansion of the pest.

Farmers’ practices of managing PMB are mostly organic

Knowing the existing farmers’ practice is an input of knowing their perception level in relation to a pest, trend of management, type of management (whereas organic and inorganic), extent of adoption of ITKs, etc. All these in turn will help in effective policy making on IPM or other modules of management. This is particularly worthy for an exotic invasive pest like PMB.

In the present study, it is found that 89.9% farmers either adopt no management practices or apply few mechanical, cultural, inorganic, and/or organic measures to control PMB in papaya plants. The non-chemical measures include: (i) Removal of infested leaves, (ii) application of red soil at base, (iii) spraying of water with force for removal of insect colony, (iv) spraying of tobacco-leaf soaked water, (v) cleaning of plant parts, (vi) dusting of fire-wood ash, and (vi) wrapping of fruits with cloth/paper. Chemical measures included dusting/spraying of (i) Cypra plus (Cypermethrin 25% EC) @ 25gm in 12L water, (ii) aqueous potash solution in different concentrations, (iii) Falcon (Cartap Hydrochloride 4% GR) @75gm in 15L water, (iv) Rogor (Dimethoate 30% EC) @ 2.0 mL per litre of water, (v) Profex (Profenophos 50% EC) @20-25 mL in 15L water and (vi) vitamins (multi-elemental composition) that commonly used in tea cultivation. Only 10.1% farmers used insecticide, and most of them used it on the recommendation of pesticide vendors. In direct or crucial chemical control, application of recommended concentration of Profenophos, Chlorpyriphos, Buprofezin, Dimethoate, Imidaclopride, Thiametoxam, Acetampride are the most commonly employed against the PMB in India (Krishnan et al., 2016). However, the resistant nature of the waxy coating, the toxicity against natural enemies, and the need for frequent applications of pesticides render insecticidal treatments effective only for the short period (Laneesha et al., 2020).

Farmers have the opinion that the highest control PMB was achieved by insecticide to 70–80% followed by tobacco-leaf soaked water (40–60%), spraying of water with force for removal of insect colonies (30–50%), dusting of wood ash (20%). Other methods had a control of about 10–15%. Removal of infested leaves and pruning of stem resulted in a remarkably low infestation of PMB in the next season.

Discussion

The present study confirms that the invasion of PMB in NER India was first observed in Lower Brahmaputra valley Zone (LBVZ) of Assam. An early invasion in LBVZ itself is an indication of invasion through trade materials from mainland India, since the LBVZ of Assam comes first in the trade route from mainland India to seven states of NER India. The pest made its entry in Assam through trade materials, but within the state it spread on its own from the urban area to rural area. Papaya is not a commercial crop in NER, and it is mostly grown as a component crop in backyard homestead gardens, i.e. papaya plants are sparsely populated. That is why PMBs expanded its territory of invasion slowly.

The invasiveness of the pest in Assam is found to be less as compared to many parts of mainland India (Ayyasamy & Regupathy, 2010; Regupathy & Ayyasamy, 2012; Shylesha et al., 2010; Selvaraj, 2012). The pest is expanding its territory with time, but at a much slower speed than expected. In 2012, it was confined within a periphery of 5 km from Dibrugarh town and now has been expanding to about 56 km. The pest, which was confined within 105–112 m above MSL in 2012, has been recorded now at an elevation of 98–129 m above MSL (Table 2). Out of 217 farmers surveyed in 7 blocks of the district, only 69 farmers (31.8%) have experienced the infestation of PMB in their crops (Table 2). PMB has not damaged much the way it did in other papaya producing regions of India (Ayyasamy & Regupathy, 2010; Regupathy & Ayyasamy, 2012; Shylesha et al., 2010; Selvaraj, 2012), e.g. in the state of Tamil Nadu the agricultural losses due to papaya mealybug were estimated to be 10–60% depending on the crop (Selvaraj, 2012), in some cases even higher (Shylesha et al., 2010).

As found, the Indian Apefly helped in suppression of the pest. It is noteworthy that NER has a rich biodiversity and is a part of the Eastern Himalaya hot spot; hence, the role of natural enemies in suppression of PMB population cannot be ignored. Nasari et al. (2020) revealed that the most recommended method for managing PMB is use of biological control in about 70% of the literature sources.

Spalgis have been reported in crop ecosystem as well as in non-crop vegetations in many parts of Assam (www.ifoundbuterflies.org; Bora & Meitei, 2014; Choudhury, 2009, 2020; Saikia, 2014) and its adjoining states of NE India (Bora, 2015). Many farmers might have missed it in their inspection since Spalgis has retiring nature, small size, and rather drab colour (Venkatesha et al., 2004). Though the S. epeus is known to be a potential predator of different species of mealybugs (Chacko & Bhat, 1976; Mani et al., 1987; Gowda et al. 1996; Rahiman & Vijayalakshmi, 1998), its activity is rarely noticed in the field wherever insecticides are used indiscriminately for the control of various insect pests (Venkatesha et al., 2004). The presence of Spalgis is not so rare in the crop ecosystem of NE India. This may be due to meagre pesticide consumption (0.14 g/ha) in this region (Roy et al., 2015). Spalgis is an inhabitant of wooded areas (Venkatesha et al., 2004); therefore, its higher abundance may be anticipated in forest dominating NE states. Moreover, other species of Spalgis may be available in this zone, since Kumar (2013) has already reported a very rare species, viz. S. baiongus from Assam. Adult S. epeus lay eggs on the mealybug masses, and the newly hatched larvae remain inside the mealy bug ovisac to consume the eggs of mealybugs (Tanwar et al., 2010). S. epeus has a demonstrated capacity to destroy large numbers of PMB and its bionomics study supports its amenability and suitability for further intensive utilization for augmentative biological control of the papaya mealybug in several countries (Thangamalar et al., 2010; Samaporn & Intawat, 2012; Cham et al., 2014; Chatterjee & Halder, 2017; Nasari et al., 2020). Many predatory insects including Spalgis epius Westwood are considered useful in regulating P. marginatus populations (Sharma & Muniappan, 2022). Assam has also a rich diversity of syrphids (Thangjam et al., 2019); however, we did not find any syrphid species predating PMB. An extensive study is required in order to know their role in PMB suppression.

So far the management of PMB is concerned; it is found that most of the farmers used the insecticides against PMB as per the recommendation of pesticide retailers. This is one of ill-practices associated with pesticides application, and the government must take some policy on it. The sale of insecticide to farmers must be based on the prescription issued by the government extension officers, scientists, and other competent authority.

The pest has established itself slowly in the agro-ecosystem in Dibrugarh district since its entry in 2012. Polyphagous insects have an innate tendency of host shifting. Such a shift is assured in an ecosystem with diverse host plant species. We have observed host shifting from papaya to other host plants in the surveyed villages. Almost every rural household in Assam has a unique backyard (locally called BAARI system) where diverse plants are grown for food, feed, fibre, fuel, plants for rearing silkworm, plants of medicinal value, etc. Even though there is no papaya plant available in each and every backyard homestead or in every season in such a homestead, the diverse plant community of the homestead helps P. marginatus shift from one host plant to other and subsequently assure to sustain and establish. Such a host shift is not only within a homestead, but also from one homestead to another neighbouring one. This is one of the prime reasons why the pest could survive and disperse in such a high rainfall region of the country. The host shifting or/and fitness of different mealybug species in different host plants is also reported by many authors (Amarasekare et al., 2008; Huang et al., 2014; Nisha & Kennedy, 2017; Chuai et al., 2022). The predictive model (Finch et al., 2021) indicates that there is substantial potential for expansion of PMB in Asia, where suitable host crops are highly abundant. Therefore, the pest may invade the crop ecosystem of the entire NER India in future.

Conclusions

The PMB has acclimatized itself with the climate and established in the crop ecosystem of Assam by natural host shifting. It is also noteworthy to state that no programme on classical biological control of PMB was taken in farmers’ fields in Assam. Even after that the crop loss due to PMB attack is not remarkable, especially in rural crop ecosystem. Thus, it is logical to interpret that native natural enemies of PMB have played a significant role in suppression of the pest here. We recorded variable abundance of S. epeus larva in PMB colonies in different host plants based on which we can project successful application of the predator for the biological control of PMB. The entire NER is a part of mega biodiversity hot spot, and there is enough scope of identifying the potential natural enemies of PMB. However, it requires a long-term systematic study in crop ecosystems, forests, and non-crop vegetation in a project mode. The detailed study on the role of rainfall and natural enemies on population dynamics of PMB is a researchable issue in this region.