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Review

Retrospection of Outbreaks of Spodoptera mauritia Boisduval in NER India: The Solution Lies in Ecological Engineering, Not in Insecticides

by
Arup Kumar Sarma
1,*,
Christian Damgaard
2 and
Prasanta Neog
3
1
Department of Entomology, BN College of Agriculture, Assam Agricultural University, Biswanath Chariali 784176, Assam, India
2
Department of Ecoscience, Aarhus University, Vejlsoevej 25, 8600 Silkeborg, Denmark
3
Department of Agrometeorology, BN College of Agriculture, Assam Agricultural University, Biswanath Chariali 784176, Assam, India
*
Author to whom correspondence should be addressed.
Sustainability 2021, 13(22), 12824; https://doi.org/10.3390/su132212824
Submission received: 9 September 2021 / Revised: 13 November 2021 / Accepted: 15 November 2021 / Published: 19 November 2021
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Abstract

:
Rice cultivation in North East India is organic by tradition; however, the recent outbreaks of the rice-swarming caterpillar, Spodoptera mauritia Boisduval, have compelled rice-farmers to use synthetic insecticides. The outbreak in 2016 affected more than 56,768 ha of winter rice in 28 districts of Assam. About 25,545–42,576 L insecticide was applied in the state to combat the outbreak. This is one of the highest insecticide loads ever to be added to the rice ecosystem of Assam. Such a load, if added repeatedly with the reoccurrence of outbreaks, may affect the innate resilience of the rice ecosystem in the long run. In this paper, the outbreak of RSC has been analysed from an ecological perspective in order to replace the existing policy of exclusive dependence on insecticide. The review will help the researchers, extension workers and policy makers of the rice producing countries, more specifically in Asian countries, which together account for more than 91% of the world’s rice production.

1. Introduction

According to a report by GRiSP, IRRI [1], rice is grown on more than 144 million farms worldwide—more than any other crop—on a harvested area of about 162 million ha in more than 60 countries. It is the basic food for the majority of the Asian population, including the region’s 560 million poor. “Rice-producing Asia” accounts for more than 91% of the world’s rice production. Besides Asian countries, rice is grown in Latin America and the Caribbean countries, West African countries, East and Southern African countries, the U.S. and Mexico in North America and in some EU countries.
The North Eastern Region (NER) of India (Figure 1) is one of the largest panhandles in the world and is known for its unique geographical location, rich biodiversity and traditional organic rice farming. It is connected to the rest of India by the Chicken’s Neck corridor, a narrow stretch of land of about 21–40 km located at Siliguri in the Indian state of West Bengal. NER comprises eight states–Arunachal Pradesh, Assam, Manipur, Meghalaya, Mizoram, Nagaland, Tripura and Sikkim (not shown the map) with an area of 262,230 sq. km, almost 8 percent of India. Conservation International has up-scaled the Eastern Himalaya hotspot to include all the states of NER [2]. In NER India, fertiliser consumption is only about 12 kg/ha and use of chemical pesticides is also meager (0.14 g/ha) [3], most of which is used in vegetable ecosystems. It is noteworthy that Sikkim—a state in NER India–is the first “fully organic” state in the country that won the FAO’S Future Policy Gold Award in 2018 (also known as “Oscar for Best Policies”), beating 51 nominated policies from 25 countries.
The Rice Swarming Caterpillar (RSC), Spodoptera mauritia Boisduval (Lepidoptera: Noctuidae), has been reported in more than 30 countries, including India [4], with its year round activity in multi-cropped areas [5]. As per the reports from various countries (Table 1a), it is seen that RSC outbreaks occurred nine times in the past two decades (2001–2020) as compared to just ten times in 10 decades in the past century. This clearly indicates that the outbreaks of RSC are becoming more frequent. In India, the most severe outbreak of RSC was observed in about 125,000 hectares in 13 districts of the state of Odisha in 2009, recording 80–90% damage [4], followed by in 56,768 ha in Assam in 2016 [6].
In recent years, severe outbreaks have occurred in different parts of India [4,7], including Assam [8,9,10,11,12]. From the outbreak of RSC in Assam (Table 1a,b), it is seen that the recent outbreak in 2016 is one of the most devastating outbreaks of any “Oscar for Best Policies”), beating 51 nominated policies from 25 countries.
The Rice Swarming Caterpillar (RSC), Spodoptera mauritia Boisduval (Lepidoptera: Noctuidae), has been reported in more than 30 countries, including India [4], with its year crop-pest ever experienced in the state, with an infestation in more than 56,768 ha in Assam [6] (Figure 1).
In Assam, the highest outbreak area in 2016 was in the Upper Brahmaputra valley zone, followed by the Lower Brahmaputra valley zone and the North Bank plain zone (Table 1c). However, based on the area infestation per district, it is seen that the outbreak was most severe in the Upper Brahmaputra Valley Zone, followed by North Bank Plain Zone.
An outbreak may cause great financial losses to farmers within a short time span. Therefore, government agencies distributed insecticides free of cost to the affected farmers. In addition, farmers’ own procurement also percolated in the rice ecosystem in the form of spray during these outbreaks. However, it is a matter of concern that such a massive addition of insecticides may pose a threat to the resilience of the rice ecosystem of Assam in the future.
Unfortunately, the Assam government considered the recent RSC outbreak in 2016 an emergency event solely during the period of the outbreak itself, but not as an event of real concern thereafter, since no scientific strategic action was taken to prevent its reoccurrence. Enough tools and means are available for the management of RSC as a pest at micro level in rice fields, but there is a need for holistic strategies to prevent outbreaks. Strategies to prevent the outbreak of RSC as an event of crisis are required, not just management of the pest species as a harmful entity. Therefore, in this paper, an attempt has been made to analyse the recent outbreaks of RSC based on ecological perspectives in order to provide input towards a suitable policy to replace the existing exclusive dependency on insecticides for combating pest outbreaks. Adoption of the strategies proposed here would help prevent repeated outbreaks of RSC and maintain the innate resiliency of the rice ecosystem sustainably. These strategies would also help in combating RSC outbreaks in other rice-growing countries with similar rice ecosystems.
Even though the RSC outbreak is a burning issue in the context of sustainable rice production, there is a dearth of systematic review on it. Therefore, an effort has been made here to review the related literatures in order to emphasise the ecological strategies to combat the RSC outbreak by adopting non-chemical means.

2. Materials and Methods

In this review, the outbreaks of RSC that have occurred in recent years in Assam, India, have been analysed and emphasised based on some ecological perspectives. However, literature on works done in similar aspects on RSC in other places has also been referred to in order to analyse the outbreak issue in larger perspective. There are four factors that favour the population build-up of this pest as identified by the International Rice Research Institute (IRRI), Philippines [16]. These are: (i) Presence of many alternate host plants such as grasses; (ii) Period of drought followed by heavy rain; (iii) Presence of dryland and wetland fields; and (iv) Presence of all stages of rice crop. These factors have been considered as guiding principles while reviewing the outbreaks. Field studies made in different districts, particularly of Dibrugarh, have also been highlighted. Pertaining research issues for development of a suitable module for prediction and prevention of such outbreaks in future are also mentioned. Some analyses are made based on the experience gathered from the different agricultural extension activities, such as on-farm testing, front-line demonstration, training, awareness programmes, method demonstration etc., conducted with the participation of hundreds of farmers during 2009–2018 under the supervision of Krishi Vigyan Kendra (Farm Science Centre), Dibrugarh, Assam Agricultural University, India. Such experience was gathered from (i) the pest-related observations made in the rice fields and (ii) feedback from the hundreds of rice-growing farmers across the Dibrugarh district. The observations on the pest were made in standing crop from mid-July to mid-December every year, whereas the feedback from the farmers was taken throughout the year during the interaction with farmers under different extension programmes. Most of the farmers were poor and marginal, belonging to all communities; i.e., the schedule tribe, scheduled castes, other backward classes, and unreserved categories. The reviewed materials were obtained from national and international research papers, reports, and relevant books. The review also includes results from work carried by the authors and synthesis of pertinent unpublished observation over the years.

3. Results

3.1. More Outbreaks of RSC Are Likely to Occur in the Future

Both rain and drought are associated with outbreaks of RSC, as “periods of drought followed by heavy rains” are favourable for swarming caterpillars [16]. This factor came into effect to cause outbreaks of RSC in the Dibrugarh district of Assam on two occasions, i.e., in 2012 and 2016 [11,12], and possibly in other districts as well.
Climatic change in the timing of the onset of the monsoon rains and the frequency of droughts has been observed in recent decades in South East Asian countries, including India [17]. Climatic variability at higher magnitudes in North East India has already been documented to cause erratic behaviour of rainfall in terms of changing rainfall patterns, increases in frequency of high-intensity rains leading to localised flash floods, reduced numbers of rainy days and the occurrence of midseason and terminal dry spells [18]. Analysis of long-term rainfall data indicated decreasing trends in annual and monsoon rainfall, with an increasing number of rainfall-deficient years from 2001 onwards in Assam [18,19,20]. Winter rice is affected by both flash floods and dry spells in the North Bank Plain Zone of Assam, and intermittent dry spells during the growing season of winter rice are becoming a major weather risk, causing widespread damage to the crops [21] in recent years. Such intermittent dry spells prevailed in other agricultural zones as well; for example, in the Dibrugarh district of Upper Brahmaputra Valley Zone [13,14]. Therefore, based on the outcome of the research cited above, it can be stated that there is probability of occurrence of “periods of drought followed by heavy rains” in coming years and consequent outbreaks of RSC in the state. Localised flash floods, as predicted by Patle and Libang [18], would carry the caterpillars from infested rice fields to uninfested ones and intensify the severity of RSC in areas experiencing flash floods.
Projections using the IMPACT model developed by the International Food Policy Research Institute suggest that climate change will lower global rice production in 2050 by 12–14% relative to the 2000 level. The anticipated changes in global climate in the form of rising temperatures, greater frequency of extreme weather events (for example, floods and droughts) and greater incidence of pests and diseases are likely to make things more complicated for rice production [1].
Recently, the Spodoptera frugiperda J. E. Smith, a congeneric species of S. mauritia, is gaining impact due to its recent invasions in many countries. S. frugiperda is so invasive that within three years of its first report from West Africa, it has spread to more than 40 countries in Africa [22] and many Asian countries. Therefore, it is likely that a similar situation may arise related to S. mauritia as well. Under the changing climatic conditions, outbreaks of S. mauritia may occur at any point of time in any rice growing country.

3.2. Crop’s Phenological Stage Determines the Loss Due to RSC Outbreak

The RSC outbreak in 2016 occurred during the mid-vegetative stage of winter rice. Rice being a resilient crop, the infested plants could recover the attack of RSC by producing sufficient compensatory tillers, and the overall yield remained almost unaffected [12]. The mean foliage-feeding population of RSC and the hiding population at the base of the plants were reported to be 36.8 per sqm and 6.31 per hill during the outbreak [11]. In another report, the RSC per hill was reported to be 1–2 to 4–18 during the RSC outbreak in 2016 [12], with a mean range of 2.5–10 per hill. Thus, 45,000–118,000 larvae were present per hectare cropped area during the outbreak. Since the 6th instar larvae of S. mauritia excrete urea as nitrogenous waste [23], it is presumed that RSCs that attained 6th instar before insecticidal exposure might have added some amount of urea in rice fields through its excreta during the outbreak period. This is a researchable issue and may be studied at the onset of such outbreaks in the future. Had the outbreak occurred 20–25 days later, there would have been a remarkable loss due to the phenological inability of producing compensatory tillers. If future outbreaks occur in the late vegetative stage of rice, farmers will suffer financially. This is why focus should be on preventing the recurrence of the outbreak of RSC as an event, not just on managing the pest as a single entity in rice fields.

3.3. Combating the Outbreak thorough Insecticides May Pose Threat to Resilience to Rice Ecosystem

Being an agricultural disaster, recent outbreaks of RSC have been controlled mainly by applying chemical insecticides. Thus, a huge insecticide load percolated into the rice ecosystem of Assam during the outbreaks. The Department of Agriculture of the Assam government supplied synthetic insecticides free of cost to the affected farmers. For instance, the outbreak in 2016 affected more than 34,650 ha area of rice in 28 districts of Assam, and with Dibrugarh being one of the worst hit districts, the state department of agriculture distributed a total of 5150 L liquid insecticide and 1000 kg of dust formulation to combat the menace [12]. This was part of a nick-of-time management approach, and such a free supply was made in other affected districts as well. However, the actual quantity of insecticide applied exceeded the freely supplied insecticide, since many farmers also applied pesticide at their own cost. It is estimated that about 25,545–42,576 L of insecticide may have been applied during the outbreak in 2016 in the state. This is one of the highest insecticide loads ever added to the rice ecosystem of Assam. If used repeatedly in this manner, insecticides would wipe out the natural enemies of all pests, rendering the rice ecosystem vulnerable not only to RSC, but also to other rice pests. The ecological service of these natural enemies is usually ignored during outbreak periods, but it cannot be compensated thereafter. Ecologically, this is a costly affair, particularly in a resilient crop such as rice, in northeast India, where rice traditionally is grown without the use of insecticides. It is noteworthy that the outbreak of RSC in 2016 incurred an expenditure of about Rs. 4,850,000–8,950,000 for insecticides in Assam. This is a costly event in a developing country such as India, where farmers are mostly poor and marginal, and these funds could have been utilised for other welfare schemes for farmers. This emphasises the importance of predicting outbreaks and using non-chemical measures to the fullest to prevent them, yet, so far, the state has not taken any initiative for prediction. The application of insecticides is situation-specific and fruitful only for a particular period of the outbreak, but with repetitive use it would act against the innate resilience of the rice ecosystem and increase the cost of production in the long run, which, again, would cause poor farmers to suffer. Most of the farmers of this region are illiterate and do not possess the scientific knowledge for pest management; and the few who do have the knowledge do not practice it in their farming on account of small holding. Therefore, such a free supply of insecticides would bring a change in farmers’ attitudes and may lead to their injudicious use, which is not desirable in organic rice ecosystems. For this reason, ecological engineering should replace the insecticidal management of pest outbreaks.

3.4. Summer Ploughing Had a Great Impact on the RSC Outbreak

The Upper Brahmaputra Valley Zone (UBVZ) of Assam was affected the most, with an infested area of 22,289 ha, amounting to 64.31% of the total outbreak area in 2016 [12]. All three worst-affected districts—Sivasagar, Golaghat and Dibrugarh—belong to this zone, and each experienced the outbreak in more than 5000 ha. Five out of seven districts of UBVZ were among the ten worst-affected districts of Assam. It was observed that the outbreak was more severe in areas with monocultures of rice, as in the UBPZ, where rice fields remain fallow after the harvest of winter rice. In such localities, most of the paddy fields remain fallow from December to July. This allows the hibernated pupae of RSC to live uninterruptedly, which results in higher adult-emergence and fecundity, boosting the pest load in the next rice crop. It is noteworthy that summer ploughing (or ploughing for a second crop after the harvest of winter rice) helps to reduce the pest load in the next crop, as it exposes the hidden pupae of RSC to insectivorous birds and sunlight. Even though summer ploughing is a recommended practice, its use is not up to the desired level, and hardly 4–5% of rice growers adopt it in UBVZ. This must be made mandatory for rice growers, for instance. A policy could be formulated to include only farmers who adopt summer ploughing as beneficiaries of government schemes. This is important in order to retain the organic rice culture in the state. Once implemented in Assam, it is expected that other states of NER India will also follow this policy in the future.

3.5. Bird-Perches Are Not Just a Bamboo Structure, but an Effective Ecological Tool

The ecological and economic importance of insectivorous birds in suppressing potentially harmful insect-pests on a global scale can be realised from the fact that insectivorous birds consume an estimated 400–500 million tons of prey annually [24]. More than 50% of bird species are predominantly insectivorous, and nearly 75% eat invertebrates at least occasionally [25]. The beneficial response of birds influencing insect outbreaks (for example, spruce budworms, Choristoneura spp.; cicadas, Magicicada spp.; and Mormon Crickets, Anabrus simplex) is well documented in U.S. Biological Survey reports, as summarised by Whelan et al. [26]. Such a detailed report on the role of birds influencing pest outbreaks in rice ecosystems in India is lacking and has a tremendous scope for research.
Ecological services of insectivorous birds are yet to be explored to their fullest extent in rice pest management in Assam. Of the 818 avian species recorded from North East India, 689 species have been reported from the state of Assam [27], and 166 species in the agricultural landscape from 2014–2019 [28]. Out of 56 bird species recorded in rice–rice crop sequences, 46 have been reported to be insectivorous [28]. Moreover, 24–28 species visit the rice crop at different phenological stages [29]; however, farmers are not successful in utilising their ecological services in pest management, which is also reflected in the occurrence of the recent RSC outbreaks itself. There is every possibility of recording more insectivorous bird species in the rice ecosystem if it is surveyed systematically in all agro-ecological zones of this Eastern Himalayan hotspot.
Erecting bird-perches in rice fields is a traditional practice in Assam, and the use of T-shaped bird-perches has been recommended by Assam Agricultural University. However, in reality, this recommendation is not followed by rice farmers on a large scale, and the ecological services of birds are still underutilised in the rice ecosystem of the state (Figure 2 and Figure 3). Figure 2 indicates an overcrowding of birds due to an insufficient number of perches, whereas Figure 3 shows birds perched on power transmission lines in the absence of other suitable perching structures in crop fields. In Assam, 11 bird species, including black drongo and pied mynah, have been reported to utilise the T-perches in the crop fields, the highest number being nine in the month of September–coinciding with higher pest prevalence [29]. Notably, the massive outbreak of RSC in 2016 occurred in September. It is a fair indication that farmers failed to harness the ecological services of these nine species during September due to non-adoption of bird-perches at the recommended level. Farmers should be made aware of this simple and effective tool not only during outbreaks (Figure 4), but also as a requirement in each Kharif season, and policy must be formulated to include only farmers who adopt bird-perches in their paddy fields as beneficiaries of government schemes.
Black drongos are known to feed late in the evening or at night, often on insects attracted to artificial lights [30,31,32], and hence, they can serve as an effective RSC predator. Farmers attract the birds to their crop fields using artificial perches in fields to encourage them to feed on pest insects of crops other than rice as well [33,34]. Black drongos have every feature of a good predator: they fly with strong flaps of the wing and are capable of fast manoeuvres that enable them to capture flying insects [35]. With short legs, they sit upright on thorny bushes, bare perches or electricity wires. Since black drongos can perch on grazing animals, their role in pest suppression in rice ecosystems cannot be ignored, as the presence of grazing animals in rice ecosystems is a common feature in India.
In the absence of such perches in rice fields, birds use other structures such as roosting trees, fencing and even the power-transmission lines near to rice fields (Figure 3). Large flocks of insectivorous birds were found sitting on power transmission lines over rice crops (Figure 3) during the outbreak of swarming caterpillars in Assam [12]. These birds act as an indicator of outbreaks of pests in rice fields and are helpful, particularly in cropped areas large enough to monitor manually. Ecological services of such insectivorous birds may be exploited by using T-perches. T-perches can make the birds converge over rice fields for pest suppression and, thus, they should not be considered a mere bamboo structure, but as an ecological tool. Such structures, if installed at the early vegetative stage, can save litres of insecticides, reduce the cost of cultivation and, above all, keep the rice ecosystems pesticide free and friendly to natural enemies of RSC.
T-perches may not work effectively if the birds are not within their territory, and if the T-perch is not installed at the proper point of time. Therefore, we must apply other tools/management to attract birds to the rice ecosystem, such as for example, growing plants for food and nesting for birds, minimum disturbance to their habitat, raising rice nurseries in/near the main field, retention of the excess seedlings in the nursery itself, etc.

4. Discussion

4.1. Identifying the RSC Hubs at Each Agricultural Development Circle

RSC hubs are low-lying waterlogged grassy areas that provide year-round ecological niches to RSC. They are usually seen in localities near to rivers/other perennial water bodies or in places that experience recurrent floods. Due to less anthropogenic interference, the population of RSC remains least interrupted in most such hubs; only few populations are naturally affected by insectivorous fish and birds. Only in some cases does grazing by herds of buffaloes/cows or contract fishing or ritual community fishing disturb their natural habitat. In all these cases, the egg-mass of RSC is destroyed to a varying extent, depending on the area of the hub disturbed by grazing or fishing. However, fishing has the innate demerit that it may reduce the population of insectivorous fish in the area. Such a hub consistently acts as a breeding ground for RSC and supply the initial population of RSC to the rice fields nearby. As RSC larvae cannot swim, they are carried to the rice fields or other unaffected places by inundation. Therefore, an early flood increases the dispersal of RSC from such hubs and contributes to bringing on an outbreak. To date, the maximum flight distance of S. mauritia adults has not been studied; however, their high flight distance may be inferred from that of their congeneric species. For instance, S. litura can fly up to 1.5 km [36] and S. frugiperda can even fly up to 500 km during migration [37]. If we consider its flight range at par with that of S. litura, a common polyphagous pest species in entire NER India, a female adult of S. mauritia will certainly find at least one rice field or another grassy hub within this range during Kharif season (June to September). This is why the outbreaks of RSC occur mostly in the Kharif season in Assam and such hubs play a contributive role therein. One such RSC hub has been identified in the Lejai area of the Dibrugarh district [12], and more hubs must be identified in each agricultural development circle of the state in order to monitor and predict the RSC populations effectively in future. Population build up of RSC in these hubs would provide effective input for prediction of outbreaks. Concerned government agricultural extension workers may be trained to identify such hubs and gather information from them. Locating such hubs and periodic recording of data on RSC populations may be considered as a mandatory activity by the State Agriculture Department.

4.2. Government Must Ban Cutting of Roosting Trees and Killing of Birds in Rice Ecosystems

Roosting trees within a crop ecosystem provide shelter to insectivorous birds and help in pest management. The mythological Lord Krishna is a cow-shepherd in India, and is worshipped as a God. Some tree species, e.g., Ficus banghalensis, Tamarindus indica, Millettia pinnata, Diospyros melanoxylon etc., are planted near crop-fields and allowed to grow till their death. As these trees grow over time, a place of worship also grows near them (Figure 5). From a scientific point of view, these trees provide an ecological service as shelter for many creatures, including insectivorous birds. With the modernization in rice farming, the ecological role of these trees in pest suppression have been ignored, and the number of such trees in rice fields is gradually decreasing with time (Figure 4), leading to them having become extinct from some rice fields (Figure 3 and Figure 4). Until a few decades ago, roosting trees were an integral part of the rice ecosystem of Assam. Even though there are a sufficient number of trees around rice fields today (Figure 2, Figure 3 and Figure 4), the plots in the middle of large rice fields are not within the territory of many insectivorous bird species. Therefore, pest suppression by birds mostly takes place at the boarders of rice fields, which is why the RSC outbreaks usually start in interior plots. Moreover, farmers usually prefer to observe the pest status in plots near to the road, not the interior plots, because of easy accessibility, which is why most of the farmers cannot detect the early stage of an outbreak. They get the information through a flock of birds (Figure 3), and therefore, the presence of birds is undoubtedly of value for the rice ecosystems of Assam, where most of the farmers have small land holdings. Government should implement policy to grow such roosting trees in rice ecosystem and ban the cutting of the existing trees in order to harness the benefit from the insectivorous birds to its maximum.
Most of the people of NER India are non-vegetarian, and wild birds are killed for food in many places. This practice should be banned by the government. Since school-going children are also involved in such killings, awareness programmes on the ecological role of birds should be organised in schools and colleges.

4.3. Mandatory Use of Traps for Monitoring the Population Buildup of RSC

The use of light traps and pheromone traps is essential for monitoring the population of RSC and to predict it in ensuing crop seasons. Such traps should be installed at nearby RSC hubs during February–Mayin order to assess the population growth so that the adults’ dispersal to nearby paddy fields can be predicted. Such traps may be installed in rice-fields about 10–15 days after transplanting as a monitoring tool. Due to the lack of suitable mechanism, the detection of the mass arrival of S. mauritia adults in the rice ecosystem failed at the time of the recent outbreaks of RSC in Assam. Their presence was detected only from the characteristic “grazing by cows” symptoms when the caterpillars attacked a considerably large cropped area. The presence of insectivorous birds in large numbers (Figure 3) in and around the rice fields also acts as an indicator of pest attack. The installation of traps could have enhanced the efficiency of the monitoring process and, hence, these traps should be treated not just as a monitoring tool, but also as a resource for crop production.
The State Department of Agriculture has the policy of free distribution of inputs (seed, fertiliser, hormones, etc.) to farmers under one scheme or other. Sometimes, pheromone traps are also distributed to farmers for monitoring the yellow stem borer, Scirpophaga incertulas—a key rice pest in this region, but their use is not up to expectations for many reasons; for example, the untimely arrival of traps at the farmers’ end, poor dissemination of technical knowhow, installation procedures/time, efficacy of lure under the high rainfall environment of Assam, etc. Keeping all these in view, the government should make mandatory the use of traps for monitoring the population build up of RSC.

4.4. Management of Alternate Hosts of RSC Ahead of the Rice Crop Season

Assam is a high rainfall state, receiving an average annual rainfall of more than 1500 mm. High pre-monsoon rainfall may favour RSC in three ways in terms of causing outbreaks in the Kharif season: (a) by inundating crop fields and promoting accumulation of caterpillars in grasses in/near to rice fields, (b) by dispersing caterpillars with water flow to new plots and (c) by encouraging profuse growth of alternate hosts of RSC in the rice ecosystem. It has been observed that with the mechanization of farming, the number of draft animals used for farm operation is declining in the villages. Consequently, some grasses that were regular animal-feed a few decades back are now flourishing in low-lying swampy land, creating RSC hubs. A number of weeds have been reported in rice ecosystems in Assam [38], many of which have been reported as alternate hosts of RSC as well [11,12]. After receiving pre-monsoon showers, these plants grow profusely and support the build up of RSC; and, therefore, these alternate hosts should be managed in March–April. Moreover, mud plastering of the inter-plot bunds in rice fields should be practiced to check the growth of alternate hosts in situ. Growing of flowering plants in bunds in rice fields has shown potential in pest control in Asian countries by sheltering natural enemies [39] and in suppression of weeds. This practice should be popularised in Assam through an extension mechanism.

4.5. The Goodness in theSauri System for Poor and Marginal Farmers

Sauri is a community approach, where all families of a village get involved as one unit in tilling, sowing, transplanting and harvesting of rice. Such practices are common in Asian countries, with different local names. In this practice, farming operations are performed from one end of a rice field to other without considering ownership of the land under operation. Sauri led to an early completion of transplanting and harvesting because of the mandatory presence of representative members from each family. This practice was operative in many villages of Assam up to few decades back, but it has now become almost obsolete with the modernization of rural society and mechanization of farming.
According to IRRI, the presence of all stages of the rice crop is favourable to RSC [16] and is an outcome of staggered planting over the crop season. Staggered transplanting of winter rice is becoming common in Assam for many reasons; for example, non-availability of an adequate number of draft animals, tractors or power tillers at the time of land preparation as well as a lack of transplanters (both human or machine). An increasing area used for tea in many districts of UBVZ of Assam has also diverted the agricultural labourers, creating a crisis at the time of ploughing and transplanting of rice. Such a shortage of farm workers has extended the transplanting period and resulted in the presence of all stages of rice crops in bigger rice fields. This is another reason why the RSC outbreak in 2016 was more severe in UBVZ. Adequate mechanization in terms of providing sufficient numbers of ploughing equipment and transplanters must be assured in each rice-growing village, so that transplanting of rice seedlings may be completed in as short a time span as possible. Therefore, reviving the Sauri system may be good option in this context.

4.6. Need for Promoting Entomophagy of RSC, and Rice-Cum-Fish Culture

Entomophagy is common in many ethnic groups of NER India [40,41,42,43,44,45,46,47,48,49,50], where insects are mostly consumed as food and for medicinal purposes. As constraints, such as content of anti-nutrients and contamination of chemicals and biochemical compounds as well as other risks to human health (allergic reactions, disease infection, side effects) are minimal, consumption of silkworm larvae and pupae, water bugs, grasshoppers, field crickets, termites and dragon fly larvae would prove beneficial as a local source of protein, minerals and vitamins [49]. All of the studies cited above have emphasised entomophagy as a part of human nutrition and, specifically, as a protein supplement. The presence of anti-nutrients and the nutrition profile of pre-pupae and pupae of RSC (Figure 6) may be analysed so that they can be recommended for human consumption in the near future. In addition, since RSC are devoured by many bird species, their caterpillars of any stage may be recommended as feed for ducks and poultry. There is no scientific study on RSC as food in NER India; however, there is scientific evidence of using other congeneric species, e.g., Spodoptera frugiperda and other Spodoptera species, in many rural areas of Mexico [51].
Integrated rice-fish farming has been shown as a productive venture in many countries. Insectivorous fish species control many insect-pests of rice and thus, increase crop productivity by curtailing the damage to the rice crop from these pests. Rice-cum-fish culture using local insectivorous fish species has recently been reported as a component for doubling farmers’ income [52]. Based on the suitability of land and water resources, such rice-cum-fish culture can be popularised among rice farmers; and, since RSC outbreaks usually start in low-lying areas, rice-cum-fish cultures would help suppress the initial build up of RSC in low-land paddies. A strict ban on fishing insectivorous fish species in such a low lying-areas prior to rice harvesting should be imposed.

4.7. Provision of Payment for Collection of RSC during Outbreak and Awards to Participating Farmers in Field Research

In the recent outbreak of locusts in the Indian subcontinent, the outcome of the “Catch locusts, Earn money, Save crops” project in Pakistan in February 2020 was quite successful. The project was inspired by an example in Yemen in May 2019, where the motto was, “Eat the locusts before they eat the crop”. The project in Pakistan was a brainchild of Muhammad Khurshid, a civil servant, and Johar Ali, a biotechnologist. Farmers were motivated to collect locusts at night, when locust swarms sit on trees and open ground and remain almost motionless before sunrise. The project paid farmers PKR 20 per kg, and the locusts were later sold to nearby chicken feed manufacturing plants. The outcome was so encouraging that farmers netted up to PKR 20,000 (=$125) per person for one night’s work (https://www.thethirdpole.net/2020/05/28/pakistan-locusts (accessed on 14 November 2021). Such an initiative may also be taken during RSC outbreaks. In Assam, the collection of bunch caterpillars in tea is a common practice on some tea estates, and the government must offer such incentive, by, for instance, paying for the collected mass of caterpillars in outbreak periods instead of providing a free supply of insecticides to farmers.
There are provisions for awarding farmers through many agencies under the Ministry of Agriculture and Farmers’ Welfare, Indian Council of Agriculture. Many on-farm-trials (OFTs), front-line-demonstrations (FLDs) and other extension activities are also carried out at farmers’ crop fields by many organizations in India. Farmers participating in such field research may be encouraged with special awards, which would, in turn, encourage the farmers to lead their communities. In many instances, a community approach is the backbone of successful pest management strategies. This is done more effectively at the farmers’ level by someone from the local villages than by salaried government workers.

4.8. Repeated Awareness of Farmers Is Essential

Most of the rice growers in India are poor and marginal, and do not possess adequate scientific knowledge of farming. Therefore, they must be made aware of the fact that pest management in rice is based on ecological manipulation, not insecticide application. The application of bird perches, mud plastering of inter-plot bunds, symptoms-based inspection, letting flocks of ducks in rice fields, rice–fish farming etc. must be communicated to them in their local language, which requires repeated awareness activities and field visits.
Pictorial extension bulletins should be developed in local language and distributed in mass scale among farmers and extension workers so that they easily can identify Spodoptera mauritia in the field itself in early stages [53]. This will help timely detection and prevent and combat an outbreak. In a survey made in the Dibrugarh district, only 11 out of 563 (1.95%) farmers had some knowledge of the pest before the outbreak [12]. In most cases, the farmers had no knowledge on the nature of damages caused by RSC and the method of inspecting it. They confused the initial localised symptoms of attack as grazing by cattle and did not inspect the base of the plants, which allowed RSCs considerable time to spread to new plots. In some big rice fields, the pest attack was only perceived from the presence of flocks of insectivorous birds (Figure 3) in and around the field.
Agricultural policy in relation to crop-pest management in Assam is not satisfactory, and the policy is chiefly confined to input distribution in a top-to-bottom approach. So far, in pest management in rice, emphasis has been given primarily to distribution of chemical pesticides and, secondarily, to pheromone traps against the yellow stem borer in rice. Instead of supplying insecticides, there is a need to make farmers aware of pest management from the standpoint of ecological approaches in rice farming. It is noteworthy that the government’s policy implemented at rice fields during non-outbreak years would determine the frequency of outbreaks in future.

4.9. Due Emphasis on Research on the Ecological Roles of Insectivorous Birds in Rice Ecosystem

Elphick [54] has shown the distribution of research efforts on bird use of rice fields relative to the amount of land used for rice production in different geographic regions. Research efforts, as measured by the total number of published papers, have been divided such that 36% are from North America, 28% from Asia, 20% from Europe and about a sixth from the rest of the world. However, the proportion of all research is far lower than would be expected on the basis of the amount of land devoted to rice production in Asia (28 vs. 89%). This warrants much research on birds in rice ecosystems globally, particularly in Asian countries.
Rice agriculture is also increasing rapidly in Africa [55], which is also underrepresented in the existing literature. In the Indian subcontinent, waterfowl and wading birds constitute less than 15% of all the bird species recorded in rice fields [56]. However, only a few similar studies have been done on the continent.
Elphick [57] recorded 56 bird species in the rice fields of Sacramento Valley, California. Of these, species that were more common in unflooded fields were all carnivorous or granivorous in winter, whereas species that were more common in flooded fields were mostly insectivorous passerines. Similar comparative studies can be done in rainfed and irrigated rice ecosystems of Asian countries. As stated by Elphick [54], “We have only a rudimentary understanding of the benefits that birds provide to rice growers, although we do know that a range of ecological services accrue under at least some circumstances [58,59,60]”. This is true for the rice ecosystem of many Asian countries and hence, extensive study on the ecological roles of passerines in rice ecosystems is required on a global scale.

4.10. Agricultural Policy on Rice–Duck Farming and Complex Rice System (CRS)

Ducks use weeds and pests as their feed sources. Rice-cum-duck farming, on a small or large scale, is common in many Asian countries. Ducks are used as a tool for managing rice-pests in these countries, and many researchers have reported and reviewed the efficacy of ducks in rice-pest management [61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88]. The rice–duck system was analysed scientifically for the first time in Japan as aimago-rice cultivation [77]. Besides pest control, ducks also help by aerating rice plants while pecking at their bases in search of food, and ducks’ excreta falling into the rice system also act as fertiliser [77]. The ecological advantages of the rice–duck system have been proven in various studies. The system has been shown to reduce the costs of pest and weed control [78,79,80], including labour costs [73], and weed suppression may be as high as 99% over the control treatment [79]. It helps in the reduction of sheath blight disease in rice [80] as well as the density of weeds in the seed bank, even up to 90% [81]. An increase in rice grain yield by 20% was also reported over a system without the rice and ducks [82]. Based on the interactions between duck rearing and rice farming practices, Suh [83] has classified their interactions into three different categories and has highlighted their relative merits and demerits. In a stochastic modelling study with the aim of attaining the quantitative assessment and optimal selection of duck density and complex stocking time in the rice–duck agro-ecosystem, a methodology based on proposed mathematical models in terms of comparative economic and ecological benefits was addressed by Dahong et al. [84]. They also emphasised consideration of the reduction of greenhouse gases emitted from the rice field due to the activities of paddy ducks in future studies as a means to better understanding the ecological services of ducks. The complex rice system (CRS), where rice cultivation is integrated with duck, azolla, and fish has already been proven to increase yield and economic results [85] in terms of nutrient enhancement, pest control, feed supplement and biological control [86]. Such biological approaches have replaced the use of chemical pesticides and have lessened negative impacts to the environment [73,85,87,88].
Ducks can voraciously consume the rice swarming caterpillars that remain at the base and leaves of rice plants during outbreaks. From the base of rice plants, ducks can easily search and take away the caterpillars that are not accessible to many other insectivorous birds due to compactness of tillers. These caterpillars are highly palatable to ducks, who consume them in large numbers within a short period. Therefore, if used in large numbers during outbreak periods of RSC, ducks can reduce the menace to a great extent. As RSCs cannot swim, flood-water carries them to different rice fields. With the increasing level of flood water, RSCs occupy the top portion of the plant, which remains out of the water (Figure 7). Under such circumstances, ducks are a more effective predator. As ducks need no perching, they can swim and eat the caterpillars more effectively than many other bird species. Poor farmers can borrow ducks during outbreaks from their fellow farmers in nearby villages that aren’t experiencing outbreaks and use them in their RSC-infested fields. In places where the species richness of natural insectivorous birds is low, it is imperative to use ducks as a control tool. Rice–duck farming alone or as component of CRS should be popularised as one of the integral components of the IPM module in rice, and the government may encourage such rice-cum-duck farming systems as a part of policy for combating RSC outbreaks.

4.11. Precise Prediction of RSC Outbreak Is the Need of the Hour

The International Rice Research Institute, Philippines, has identified four factors that favour the population build up of RSC. They are: (i) presence of many alternate hosts, for example, grasses, (ii) periods of drought followed by heavy rains, (iii) presence of dryland and wetland fields and (iv) presence of all stages of the rice crop [14]. Of these, three factors are invariably present in Assam. Pertaining research also states that drought kills the natural enemies of RSC, and flooding allows RSC to concentrate on rice plants [5]. These weather factors came into effect to cause outbreaks of RSC in the Dibrugarh district of Assam on two occasions, i.e., in 2012 and 2016 [11,12]. The Standard Precipitation Index (SPI) was also used to identify the weather spells favourable for RSC [12]. In order to improve forecasting of pest epidemics, it is important to know the spatial scale at which specific forecasts are reliable [89]; and in order to predict the effect of the different preventive measures as discussed above, it will be necessary to model the population dynamics of RSC during outbreaks in spatial epidemic models [89]. The effect of a limited and targeted use of insecticides may also be included in such modelling studies. To fit such spatio-temporal stochastic RSC population growth models, long-term population data of RSC and the most important drivers should be collected in RSC hubs and nearby rice fields.

5. Conclusions

S. mauritia being a polyphagous species, once it gets settled in a crop ecosystem, it will pass its life stages in other suitable host(s) during the rice off-season, and will continue to damage the rice crop every year to a varying extent. This may lead to a proportionate increase in insecticide application in the rice ecosystem. Most of the rice growing areas are located in developing or underdeveloped countries; therefore, use of insecticides will increase the cost of production and reduce profit for the farmers. This is not encouraging for poor and marginal rice growers. The main theme of this review has been to convey ways to curtail insecticide use through other means (prediction of outbreak, its mitigation through non-chemical means, ecological engineering, etc.) in rice ecosystems.
As mentioned in the review, ecological tools would assist in combating RSC outbreaks in the different countries with similar rice ecosystems, specifically in Asia and some parts of Africa and Latin America. It is noteworthy that out of one million farmers in Latin America who depend on rice as their main source of energy, employment and income, about 0.8 million are resource-poor smallholders with less than 3 ha area [1]. The present review may help the researchers, extension workers and policy makers of the rice producing countries, more particularly Asian countries, which together account for more than 91% of the world’s rice production.

Author Contributions

Conceptualization, A.K.S.; writing—original draft preparation, A.K.S. and P.N.; writing—review and editing, C.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors acknowledge Rumi Borah Saikia, Agriculture Development Officer, District Agriculture Office, Dibrugarh, Assam, India for the images (2 & 4).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Map of North East India (source: https://www.pngkey.com accessed on 14 November 2021).
Figure 1. Map of North East India (source: https://www.pngkey.com accessed on 14 November 2021).
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Figure 2. Insectivorous birds in rice ecosystem.
Figure 2. Insectivorous birds in rice ecosystem.
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Figure 3. Insectivorous birds on power-transmission line.
Figure 3. Insectivorous birds on power-transmission line.
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Figure 4. Farmers’ awareness on use of bird-perches.
Figure 4. Farmers’ awareness on use of bird-perches.
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Figure 5. A temple near the rice fields.
Figure 5. A temple near the rice fields.
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Figure 6. Pre-pupae and pupae of RSC.
Figure 6. Pre-pupae and pupae of RSC.
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Figure 7. Outbreak of RSC during flood.
Figure 7. Outbreak of RSC during flood.
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Table
Table 1. (a) Legacy of outbreak of swarming caterpillar in rice. (b) Area affected by RSC during its outbreak in 2016 in Assam. (c) Area affected by RSC during the outbreak in 2016 in different agro-climatic zones of Assam (as on 19 September 2016).
Table 1. (a) Legacy of outbreak of swarming caterpillar in rice. (b) Area affected by RSC during its outbreak in 2016 in Assam. (c) Area affected by RSC during the outbreak in 2016 in different agro-climatic zones of Assam (as on 19 September 2016).
(a)
YearArea AffectedRegion/States/CountrySource of Information
1904Not availableSri LankaWikipedia $
1920Not availableSri LankaWikipedia $
1967Not availableAssam, IndiaBaruah (2017) [10]
1969Not availableChattishgarh, IndiaJena et al., 2017 [13]
1969200 acresSabah region, MalaysiaWikipedia $
19696000 sq. milesSarawak region, MalaysiaWikipedia $
1970Not availablePunjab, IndiaJena et al., 2017 [13]
1981Not availableIndonesiaWikipedia $
1993Not availableTamil Nadu, IndiaTanwar et al., 2010 [4]
1999250 haKotma Block, Central IndiaTanwar et al., 2010 [4]
2004100 haDhenkanal, Odisha, IndiaJena et al., 2017 [13]
200750 haTangi Block, Cuttack, IndiaJena et al., 2017 [13]
2008150 haOdisha, IndiaJena et al., 2017 [13]
2009125,000 haOdisha, IndiaTanwar et al., 2010 [4]
2012800 haDibrugarh, Assam, IndiaSarma et al. (2013) [8]; Sarma and Gupta (2018) [11].
2013100 haBarpeta, Assam, IndiaUpamanya et al. (2013) [9]
201656,768 haAssam, IndiaNRRI, 2016 [6]
20161304 haKuttanad, Kerala, IndiaJena et al., 2017 [13]
2017Not availableNalbari, Bangaigaon, Jorhat district of Assam, India.Sampathkumar M. et al. (2018) [14].
2018Not availableKottayam district, Kerala, IndiaAmala et al. (2019) [15]
2018Not availableMayurbhanj district, Odisha, IndiaAmala et al. (2019) [15]
(b)
S. No.DistrictsArea (ha)S. No.DistrictsArea (ha)
1Golaghat6671 b15Kokrajhar192
2Jorhat1871 f16Baksa62
3Majuli1600 g17Bongaigaon90
4Sivasagar6681 a18Sonitpur654
5Charaideu6619Biswanath Chariali1080 j
6Dibrugarh5150 c20Lakhimpur2445 d
7Tinisukia25021Dhemaji62
8Kamrup (R)39022Darrang1265 i
9Kamrup (S)20023Morigaon92
10Kamrup (E)47024Nagaon171
11Nalbari91325Hailakandi20
12Barpeta1269 h26Mancachar15
13Dhubri48827Karbi- Anglong353
14Goalpara2083 e28Dima Hasao54
(a–j): The top ten most infested districts. Total: 34,657 ha (as on 19 September 2016) *
(c)
Name of the ZoneAffected Area (ha)Affected Area Per District (ha)
1. Upper Brahmaputra valley Zone (Sl No. 1–7 in Table 1b)22,2893184.1
2. Lower Brahmaputra valley Zone (Sl No. 8–17 in Table 1b)6157615.7
3. North Bank Plain Zone (Sl No. 18–22 in Table 1b)55061101.2
4. Central Brahmaputra Valley Zone (Sl No. 23–24 in Table 1b)263132.5
5. Barak Valley Zone (Sl No. 25–26 in Table 1b)3517.5
6. Hill Zone (Sl No. 26–27 in Table 1b)407203.5
Source: Sarma and Salam (2018) [11]. * The area of infestation increased in subsequent days and expanded to an area of 56,768 ha as reported by NRRI [6]. $ https://en.wikipedia.org/wiki/Spodoptera_mauritia (accessed on 14 November 2021)
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Sarma, A.K.; Damgaard, C.; Neog, P. Retrospection of Outbreaks of Spodoptera mauritia Boisduval in NER India: The Solution Lies in Ecological Engineering, Not in Insecticides. Sustainability 2021, 13, 12824. https://doi.org/10.3390/su132212824

AMA Style

Sarma AK, Damgaard C, Neog P. Retrospection of Outbreaks of Spodoptera mauritia Boisduval in NER India: The Solution Lies in Ecological Engineering, Not in Insecticides. Sustainability. 2021; 13(22):12824. https://doi.org/10.3390/su132212824

Chicago/Turabian Style

Sarma, Arup Kumar, Christian Damgaard, and Prasanta Neog. 2021. "Retrospection of Outbreaks of Spodoptera mauritia Boisduval in NER India: The Solution Lies in Ecological Engineering, Not in Insecticides" Sustainability 13, no. 22: 12824. https://doi.org/10.3390/su132212824

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