Incidence of Groundnut Leafminer (GLM), Aproaerema modicella (Deventer) (Lepidoptera: Gelechiidae) and its Parasitic Fauna on Alternate Leguminous Hosts in Tamil Nadu, India

The groundnut leafminer (GLM), Aproaerema modicella (Deventer) (Lepidoptera: Gelechiidae) is a serious pest of groundnut and other leguminous host plants in South and South-East Asia (Wightman et al., 1990). The larvae construct blister-like mines in the mid-rib on the dorsal side of the leaf. The entire leaf eventually turns brown, rolls up and dries out. When there is a severe infestation, the crop appears to be burned up in appearance (Ranga Rao and Rameshwar Rao, 2013). A. modicella feeding limits the photosynthetically active leaf area, resulting in yield losses ranging from 50 to 100 per cent (Namara et al., 2019). Because of concealed nature of the pest, biological control based on natural enemies may be an environmentally and economically sound approach for the management of A. modicella than synthetic insecticides. In this context, it is critical to have an understanding on the indigenous natural enemies in order to build sustainable pest control tactics.
       
The parasitoid ecosystem associated with A. modicella is extensive and diverse, with atleast two trophic levels, involved (Shanower et al., 1993). Many species of parasitoids of A. modicella viz., Avga choaspes Nixon, Stenomesius japonicus (Ashmead), Sympiesis sp. and Tetrastichus sp., Chelonus sp., Bracon sp., Brachymeria sp., Temelucha sp. and Goniozus sp. are reported from Asia (Shekarappa et al., 1990; Basha et al., 2012; Murugasridevi et al., 2019). Over 40 primary and secondary parasitoids belonging to 12 families have been cultured from A. modicella and found to parasitize up to 50 per cent of A. modicella larvae in a single generation (Shanower et al., 1993; Kenis and Cugala, 2006). Success of any biological control programme depends on the exploration of indigenous natural enemies. In this respect, extensive surveys were carried out in Sivagangai and Coimbatore districts of Tamil Nadu on the occurrence of GLM, A. modicella and its parasitic fauna during 2016 to 2018.
       
On the other hand, alternative host plants with including cultivated and weed species, not only harbor herbivorous pests but also beneficial predators and parasitoids, especially during the inter-harvest period (Saeed et al., 2015). GLM were found to feed on leguminous host plants viz., groundnut, pigeon pea, soybean, green gram, alfafa, hairy indigo, rice bean, egyptian clover, snout bean and weed plants viz., Babchi, Psorelea coryfolia L., Red spiderling, Boerhavia diffusa L. and Slender amaranth, Amaranthus viridis L., (Shanower et al., 1993). Hence, ascertaining the significance and extent of alternative host plants on both cultivated and weed species can be crucial in avoiding polyphagous pest populations from forming on a ‘main’ or ‘focal’ agricultural species (Tabashnik et al., 1991). For instance, alternative host plants can serve as pest reservoir during off season of main hosts, with pests subsequently migrating back onto the main host plants (Clementine et al., 2005). They can also be agriculturally advantageous when they host natural enemies populations (Naveed et al., 2007). Taking this into consideration, incidence of A. modicella and its parasitoids were recorded in other alternate leguminous hosts of A. modicella viz., redgram and babchi.

Extensive surveys were conducted during 2016 to 2018 (July to October) in Sivagangai and Coimbatore districts of Tamil Nadu, India to document the damage potential of A. modicella on Groundnut and its associated parasitoids. In addition, incidence of A. modicella and its parasitoids were recorded in other alternate leguminous hosts viz., redgram (Cajanus cajan L.) and babchi (Psorelea corylifolia L.) at Coimbatore district of Tamil Nadu (Fig 1c).
 

 
Assessment of damage potential of A. modicella
 
Damage potential was assessed in twenty five randomly selected plants from each location based on symptoms (detected by the presence of small brown blotches on (or) in the leaves and the webbing of leaflets) by relative sampling. The per cent damage was calculated from top twenty fully opened leaflets from the central axis of each plant and percent damage was worked out by adopting the procedure described by Muthiah and Kareem (2000).
 
Assessment of parasitization of leafminers
 
To assess the per cent parasitization of GLM, twenty five plants were selected at random from each location and infested leaves with live and parasitized larvae were brought to the laboratory and observed for the emergence of parasitoids (Muthiah and Kareem, 2000). Absolute counts were made for working out the per cent parasitization and parasitoid (different) species emergence. A sample size of 30 larvae per location was maintained. From the sample size, per cent parasitization and parasitoid (different) species emergence were worked out by the following formula:
       
The parasitoids emerged from various hosts were preserved in 70 per cent ethanol and identified with the help of available literatures and by the taxonomic experts viz., Dr. A.P. Ranjith, Ashoka Trust for Research in Ecology and the Environment (ATREE), Bengaluru, Karanataka and Dr. Santhosh Nair from Malabar Christian College, Calicut, Kerala.

Endophagous herbivorous insects live within plants resulting in the formation of remarkable new plant architectures such as galls and mines. These insect-derived shelters presumably offer protection from natural enemies and hostile environmental conditions, but they are also thought to enable the resident to feed selectively on tissues with high nutrient content and low defense responses. However, leafminers were found to support more species of parasitoids than insects in any other feeding niche (Hawkins et al., 1997). Lack of mobility of leafminer larvae, high visibility of the mines and scant physical protection offered by the leaf epidermis make them more susceptible to their parasitoids (Hawkins, 1994).
       
In view of the above facts, pest management strategy based on parasitoids may be safe, sustainable and a well known biological control approach against arthropod pests in agricultural ecosystems. In this situation, faunistic surveys of parasitoids could constitute the baselines upon which further applicative studies can be integrated (Tomanović et al., 2014; Petrović et al., 2019).
       
The survey conducted during 2016 to 2017 revealed maximum occurrence of A. modicella in Pirankulam (98.10%) and Alagapuri village of Sivagangai district (96.40%) followed by Department of Oilseeds, Tamil Nadu Agricultural University (TNAU) of Coimbatore district (94.30%) and Arunagiri village of Sivagangai district (93.20%) (Table 1 and 2).
 

 

       
Observations on the natural parasitization revealed highest parasitization at Pirankulam village of Sivagangai district (46.67%) followed by Alagapuri village of Sivagangai district (43.33%), Department of Oilseeds, TNAU, Coimbatore (40.00%) and Arunagiri village of Sivagangai district (40.00 %) (Table 1 and 2).
       
The survey during the period of 2017 to 2018 revealed highest damage by A. modicella in Alagapuri (98.45%) and Pirankulam village (88.70%) of Sivagangai district followed by S. Vagaikulam (85.80%), Arunagiri village of Sivagangai district (85.50%) and also at the Department of Oilseeds, TNAU, Coimbatore (85.40%) (Table 3 and 4).
 

 

       
Similarly, the highest parasitization was also recorded at Alagapuri village of Sivagangai district (46.67%) followed by Pirankulam village of Sivagangai district (36.67%), S. Vagaikulam (33.33%), Arunagiri village of Sivagangai district (33.33%) and also at the Department of Oilseeds, TNAU, Coimbatore (33.33%) (Table 3 and 4).
       
This is in corroboration with the findings of Muthiah and Kareem (2000) who documented higher incidence of A. modicella with 90.10 per cent leaflet damage and 28.00 per cent parasitism at Dharmapuri district. However, in the present investigation, A. modicella incidence and its parasitization was comparatively higher than the earlier documentation. It may be due to the continuous and staggered cropping of groundnut which might have favoured increased incidence of A. modicella in rainfed conditions. Since, rainfed zones practice limited insecticidal sprays, higher A. modicella incidence might have favoured higher parasitization than the earlier reports. Similarly, Shekharappa et al., (1990) also reported positive correlation between A. modicella population and their associated natural enemies. Likewise, Murugasridevi et al., (2019) also reported increased parasitization with the increased availability of A. modicella larvae at various groundnut growing areas of Tamil Nadu.
       
Sivagangai district, being a rainfed zone, the insecticides usage is very minimum and hence, it might have favoured the continuous availability of A. modicella population for the establishment of high parasitic fauna in this location. This is also in accordance with Cherian and Basheer (1942), Logiswaran (1984) and Muthiah (1995) who reported maximum A. modicella damage on rainfed groundnut than the irrigated crop in Tamil Nadu.
       
Survey on the parasitoid fauna of A. modicella indicated that the larvae of A. modicella were parasitized by 13 species of hymenopteran parasitoids belonging to eight families. Among the 13 species, four species of braconids viz., Chelonus blackburni Cameron, Avga choaspes Nixon, Apanteles spp. and Bracon hebetor Say, three eulophids viz., Stenomesius spp., Aprostocetes spp. and Sympiesis spp., one each in Ichneumonid, (Temelucha spp.), Eurytomid, (Eurytoma spp.), Pteromalid, (Pteromalus spp.), Eupelmid, (Eupelmus spp.), Bethylid, (Goniozus spp.) and Chalcid (Brachymeria spp.) were recorded. The parasitoids were mostly larval parasitoids except C. blackburni, which is an egg-larval parasitoid. The present findings are in accordance with the reports of Praveena (2010) who documented 15 parasitoids of GLM belonging to seven families viz., bethylidae, braconidae, chalcididae, eulophidae, eupelmidae, eurytomidae and ichneumonidae at ARS, Bagalkot. Similarly, Shekharappa et al., (1990) recorded 16 species of hymenopterous parasitoids on GLM during Kharif, 1989. Sumithramma (1998) have reported 41 species of hymenopteran parasitoids attacking A. modicella however, the decrease in occurrence of parasitoid species in the present study may be due to the dynamic nature of parasitoid community structure, with composition and dominant changing throughout the year.
       
Among the different parasitoids recorded, A. choaspes was found to be prevalent with adult emergence of 20.00 per cent at Sivagangai and Coimbatore districts during 2016 to 2018. Previous reports have also indicated higher relative density of A. choaspes at Sivagangai (22.03%) and Coimbatore districts (16.55%) (Murugasridevi et al., 2021).  In addition, the abundance of A. choaspes may be due to the specific relationship that these parasitic wasps have with their host and the host plants (Pérez-Rodríguez et al., 2013) and which also often correlates with host population (Kishinevsky et al., 2017). Since, the percent emergence of parasitoid adults is the main indicator of success in augmentative biological control (Elbehery et al., 2020), the parasitic efficiency of A. choaspes can be verified against gelechiid leafminers and included in the biological control programme.
       
Furthermore, A. modicella and their associated parasitoids recorded on the alternate leguminous hosts viz., redgram and babchi indicated the higher damage of 38.20 and 34.50 per cent by A. modicella and parasitization of 33.33 and 20.00 per cent, respectively during 2017 to 2018. The parasitoids viz., Temelucha spp. Stenomesius sp., B. hebetor and Aulosaphes spp. were found to parasitize A. modicella on alternate leguminous host plants, respectively at Coimbatore (Table 5 and 6). This is in accordance with Fletcher (1920), Manoharan and Chandramohan (1986) who have also reported the occurrence of GLM on C. cajan and P. corylifolia, respectively. Similarly, Arvind (2014) also noticed the severe incidence of A. modicella on P. corylifolia.
 

 

       
The magnitude of damage caused by A. modicella and extent of parasitization by hymenopterous parasitoids in redgram shows that it may provide a favorable habitat for natural enemies because its bushy canopy provides both shelter and pollen during adverse environmental conditions and hosts the prey throughout the year (Saeed et al., 2015). Despite the existence of natural enemies, redgram had the highest densities of A. modicella throughout the year and so appear to constitute key carry over sources of the pest. Apart from this, weed plants may play an excessively significant role in influencing pest dynamics. The magnitude of damage of A. modicella and parasitization in babchi shows that it may provide a favorable habitat for predatory arthropods due to relatively low exposure to pesticides.
       
In this respect, the presence of alternative host plants is detrimental, although this can be addressed if alternative host plants harbor natural enemies of A. modicella. The relative benefits and drawbacks of alternate leguminous host plants are thus difficult to assess, but our findings suggest that their damage incidence and parasitic fauna will have an impact on the ecological balance. In any case, both the alternate leguminous host plants can very well serve as an off-season reservoir for A. modicella. Hence, these hosts should be avoided in the vicinity of groundnut fields.

Altogether, the present study depicts that the parasitic fauna associated with A. modicella is abundant and diverse in rainfed zone. Amongst which, A. choaspes was discovered to be quite ubiquitous in both areas and exhibits host specificity, resulting in high parasitism rates against A. modicella, indicating that it might be employed successfully in augmentative biological control programmes. Hence, further research might be focused on using A. choaspes as a good candidate for augmentative biological control against gelechiid leafminers as it has a relatively higher density and a significant proportion of parasitoid emergence, making it amenable for mass culturing. Moreover, the current study shows that alternate leguminous host plants and weeds must be eliminated from groundnut fields and their surroundings to limit A. modicella damage. Future studies also must imply on the temporal occurrence of A. modicella on other alternate leguminous host plants.

The senior author wishes to thank Department of Science and Technology-INSPIRE, Ministry of Science and Technology, Government of India for supporting this research through research grants.