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Biology and management of groundnut leafminer

H. DU PLESSIS & J. VAN DEN BERG School of Environmental Sciences and Development, North-West University, Potchefstroom, 2520, South Africa Corresponding author: [email protected]

Abstract The groundnut leafminer (Aproaerema modicella), has been reported from east African countries since 1998 and from South Africa since 2000. The study aimed at determining the biology and management of groundnut leafminer (GLM) in South Africa. In a survey, 10 parasitic Hymenoptera species were identified. Two hyperparasitoids were also recorded for the first time in South Africa. GLM flight activity patterns were studied using pheromone traps at the border of groundnut fields at four localities in South Africa. Research progress in pest behaviour was hampered because male and female moths could not be distinguished.. Morphologi- cal characteristics of both larvae and pupae were identified either by use of the naked eye or a stereomicroscope according to sex. Flight activity coincided with the peak production period of groundnut, with the highest number of moths recorded between January and May each year. The optimum time of insecticide application and the number of applications for GLM control were determined and significant differences in efficacy observed.

Key words: Flight activity, groundnut, groundnut leafminer, IPM components, South Africa

Introduction The presence of pink coloured gonads visible through the larval cuticle is a distinguishing characteristic of male Groundnut crop is major source of income for small-scale GLM larvae (Shanower et al., 1993). Van der Walt et al. farmers in Africa. The crop is also used as animal feed and (2008) reported distinguishing characteristics in A. farmers may harvest more than a tonne of groundnut hay modicella pupae which were visible under a light per hectare (e.g. cultivar Harts) (Van der Merwe & microscope. Swanevelder, 1988). However, groundnut production is limited by groundnut leafminer, Aproaerema modicella Moth flight activity. GLM flight activity patterns were (Deventer) (Lepidoptera: Gelechiidae), which is a well studied using pheromone traps at the border of groundnut known pest in Asia. It was first reported in East Africa fields in four localities. Peak flight activity was found to during 1998 after which it rapidly spread throughout East coincide with the main groundnut production period with and Southern Africa. Groundnut leafminer (GLM) was first the highest number of moths recorded between January reported in South Africa, in the Northern Cape, during the and May (Du Plessis, 2011). Timing of planting therefore, 1999/2000 growing season (Du Plessis, 2003). The pest largely affect both the time and severity of GLM spread over the entire groundnut production area of South infestation, irrespective of locality. These are important Africa within a single season. Heavy infestations by GLM aspects when investigating and planning for flight activity cause groundnut leaves to turn brown, with subsequent and GLM infestation levels. (Du Plessis, 2011) found that loss of leaves which in turn reduces the photosynthetically the mean number of moths captured was an indicator of active leaf area (Shanower et al., 1993). This, results in subsequent larval incidence and can therefore, be used to losses of biomass in terms of hay production and yield determine the optimum timing of insecticide applications (Du Plessis, 2003) An integrated pest management system for GLM in Crop host plants. Cultivated host plants of GLM such as South Africa is being developed. The aims of this paper groundnut, soybean and lucern and a non-host crop, are therefore, to report on past and current research cowpea, were evaluated to determine the suitability of conducted to determine distinguishing morphological these plants for development and survival of GLM larvae characteristics of male and female larvae and pupae, the and possible role that it could have in the off-season carry- moth flight activity pattern of GLM, the suitability of other over of the pest (Van der Walt, 2007). The period between crop host plants for development and survival of GLM egg laying and appearance of damage symptoms on leaves larvae, the optimum timing of insecticide application is an indicator of suitability of these host plants for larval against GLM on groundnut and the GLM parasitoid development and the time it takes a first instar larvae to complex and possible changes in diversity in three become large enough to tunnel into leaves. Visible damage groundnut production areas from 2006/07 to 2010/11. was observed on groundnut 8 ± 2.0 (S.E.) days, soybean 11 ± 1.7 days and lucern 16 ± 0.5 days after oviposition. Morphological characteristics of larvae and pupae. No eggs were laid on cowpea. Although more lesions Accurate identification of the sex of GLM larvae and pupae occurred on soybean than on groundnut and lucern, facilitates behavioural studies with moths of known sex. survival rate of GLM larvae was highest on groundnut 170 H. DU PLESSIS & J. VAN DEN BERG (92.1%) compared to soybean (77.2 %) and lucern (56.5%) at an experimental farm near Brits (25°38’S; 27°46’E) in the (Van der Walt, 2007). Lucern are therefore, regarded as the North West province during the 2006/7 season. To ensure least suitable of the three crop hosts. a high infestation level, the trial was planted late in the growing season (10 January 2007). Seven treatments were Parasitoids. A survey was carried out at four localities involved in this study that included application of where groundnut is produced to identify GLM parasitoid Cypermethrin (30 g a.i. mixed in water of 150 l ha-1) at an species. These localities were: Potchefstroom (26°44’S; interval of 13; 6, 9 and 13; 10 and 13; 6, 10 and 13; 9 and 27°03’E) (North-West province), Vaalharts (27°53’S; 13; 6, 9, 11 and 13 and 6, 11 and 13 weeks of planting 24°50’E) (Northern Cape Province), Burgershall (25°06’S; (WAP). The groundnut cultivar, Akwa, was planted using 31°04’E) (Mpumalanga province) and Brits (25°28’S; 7.5 X 50 cm spacing, giving rise to a plant population 27°45’E) (North-West province) during the 2006 and 2007 density of 266 666 plants ha-1. Treatment blocks were 4 m production seasons (Van der Walt et al., 2009). Nine long and 2 m apart to prevent spray drift effects. Data, on identified and one unidentified species of parasitic larval mortality and leaf damage were collected from the Hymenoptera were recorded (Table 1). shoot developing from the second node on the main branch. Sampling commenced one week before the last Materials and Methods application (12 WAP) and was done weekly until 17 WAP. Two shoots, from each of the two centre rows of each Parasitoid. A survey was conducted during the 2010/11 block, were sampled and the total number of leaves, GLM season to determine which GLM parasitoid species damaged leaves and live larvae were determined. occurred in the major production areas and whether the parasitoid complex changed over the last four years. A Results and Discussion similar survey was done in these areas during 2006, six years after the first report of the pest in South Africa. Survey of parasitoids. Parasitoid species recorded during GLM infested plants were collected once, during the 2010/ both the 2006/07 and 2010/11 surveys were Goniozus sp., 11 production season from Brits (25°38’S 27°46’E), Giyani (an unidentified Baraconid species), Apanteles sp., (23° 38’S; 30°43’E), Potchefstroom (26°44’S; 27°05’E), Brachymeria sp. and Pteromalus sp. The species recorded Mookgopong (24° 31’S, 28°43' E) and the Vaalharts area during the second survey which were not found in 2006/ (irrigation scheme) (27°50’S; 24°50’E). All larvae and pupae 07 were an Apanteles sp. and Pteromalus sp. in from infested leaves were reared in 90 mm diameter petri Potchefstroom and a Brachymeria sp. in Brits (Table 1). dishes at 25 + 1 °C at a 14L:10D photoperiod until GLM While no GLM parasitoids were recorded from Vaalharts moths or parasitoids appeared. Moist cotton balls were during the 2006/07 survey, several species were recorded supplied as a source of humidity and larvae were provided during the 2010/11 production season. These species were: with fresh leaves. Parasitoids were identified by a Brachymeria sp., Pachyneuron sp. and an unidentified Hymenoptera taxonomist. Ichneumonid Eurytoma sp. (collected from Tshiombo) and Pteromalus sp. (collected from Brits, Potchefstroom Chemical control and optimum timing of insecticide and Mookgopong) which are hyperparasitoids. This was application. The optimum timing and number of times for the first record of hyperparasitoids of GLM in South insecticide applications for GLM control were evaluated Africa.

Table 1. Parasitoids reared from groundnut leafminer larvae and pupae collected from crops in South Africa.

Family Species Locality

§2006/07 2010/11

Bethylidae Goniozus sp. Tshiombo Mookgopong, Giyani Braconidae Unidentified Tshiombo Mookgopong, Giyani Braconidae Unidentified Tshiombo Apanteles sp. Tshiombo Potchefstroom Hypomicrogaster sp. Tshiombo Cotesia sp. Thsiombo Calcididae Brachymeria sp. Potchefstroom Potchefstroom, Vaalharts, Brits Eulophidae Baryscapus sp. Tshiombo Eupelmidae Eupelmus (Macroneura) sp. Tshiombo Eurytomidae #Eurytoma sp. Tshiombo Ichneumonidae Unidentified Vaalharts Pteromalidae #Pteromalus sp. Brits* Potchefstroom, Mookgopong Pachyneuron sp. Vaalharts

* Parasitoid reared from soybean infested plant. The rest were from groundnut plants. # Hyperparasitoid. §Data for the 2006/07 season from Van der Walt et al. (2009). Biology and management of groundnut leaf miner 171 Chemical control: Optimum timing of insecticide significantly higher than those in all other insecticide application. The earlier applications, during the mid- application programmes (Table 2). Application of vegetative growing stage, resulted in lower numbers of cypermethrin at 13 WAP resulted in effective control surviving larvae as well as lower incidences of damaged compared to the untreated control treatment. The single leaves, compared to late treatments (Tables 2 and 3). The application was, however, not as effective as two or more number of larvae, in the untreated control treatment, was applications times indicating that more than one insecticide

Table 2. Mean number of live GLM larvae per shoot over a six week period after different insecticide application programmes against GLM.

Insecticide application Mean number of live larvae/shoot Mean programme* Time (week)

1 2 3 4 5 6

1 1.6 0.5 4.4 11.7 12.3 15.8 7.7a 2 1.8 0.6 2.7 6.1 4.9 3.7 3.3b 3 0.1 0.1 2.4 3.6 0.0 1.4 1.3c 4 0.2 0.1 0.9 3.3 1.5 2.5 1.4c 5 0.1 0.2 1.3 1.2 1.4 1.4 0.9c 6 0.0 0.2 0.7 4.2 0.8 1.7 1.3c 7 0.2 0.0 0.0 0.7 0.4 0.1 0.2c 8 0.6 0.1 0.1 0.4 0.4 0.2 0.3c

Mean 0.6A 0.2A 1.6B 3.9D 2.7C 3.4CD

Means within the same column followed by the same lower case letter and means within the same row followed by the same upper case letter do not differ significantly at P = 0.05 (HSD). *Application time per programme is given in weeks after planting (WAP). 1= control (no treatment); 2 = 13 WAP; 3 = 6, 9 and 13 WAP, 4 = 10 + 13 WAP; 5 = 6, 10 and 13 WAP; 6 = 9 and 13 WAP; 7 = 6, 9, 11 and 13 WAP; 8 = 6, 11and 13 WAP.

Source of variation F P

Time (A) 40.1 <0.001 Treatment (B) 83.1 <0.001 Interaction (A x B) 10.7 <0.001

Table 3. Mean percentage damaged leaves per shoot over a six week period as a result of different insecticide application programmes against GLM.

Insecticide application Mean % damaged leaves/shoot Mean programme* Time (week)

1 2 3 4 5 6

1 16.5 18.5 26.4 47.3 43.5 38.3 31.8a 2 24.4 18.8 21.8 40.4 43.1 29.1 29.6a 3 4.5 4.4 13.5 20.7 4.8 18.9 11.1d 4 13.9 16.6 23.4 22.0 26.8 21.7 20.7b 5 5.7 10.2 12.8 20.6 16.0 19.9 14.2cd 6 8.9 15.8 9.3 19.2 14.1 24.5 15.3c 7 6.2 6.8 3.9 6.2 8.8 8.7 6.8e 8 10.9 7.0 7.6 12.8 17.7 16.5 12.1cd

Mean 11.4A 12.2AB 14.8B 21.8C 22.2C 23.7C

Source of variation F P

Time (A) 59.1 <0.001 Treatment (B) 117.6 <0.001 Interaction (A x B) <0.001 172 H. DU PLESSIS & J. VAN DEN BERG application time is necessary per season (P = 0.05). There References was, however, no significant difference between the number of live larvae in plants sprayed two, three or four Du Plessis, H. 2003. First report of groundnut leafminer, times (Table 2). If timed correctly, two insecticide Aproaerema modicella (Deventer) (Lepidoptera: applications per season is therefore, sufficient to provide Gelechiidae) on groundnut, soybean and lucerne in effective GLM control. The interaction between time of South Africa. South African Journal of Plant and Soil insecticide application and number of live larvae was also 20, 48. significant (Table 2). Du Plessis, H. 2011. Flight activity of the groundnut There was no statistical difference in the percentage leafminer (Aproaerema modicella Deventer) in the damaged leaves between the unsprayed and cypermethrin groundnut production areas of South Africa. South sprayed plants at 13 WAP (Table 3). However, the African Journal of Plant and Soil 28, 239-243 interaction between time of insecticide application and Shanower, T.G., Wightman, J.A. & Gutierrez, A.P. 1993. percentage leave damage was significant (Table 3). More Biology and control of the groundnut leafminer, damage occured when the first application was at 10 WAP Aproaerema modicella (Deventer) (Lepidoptera: compared to 9 WAP but there was no significant damage Gelechiidae). Crop Protection 12, 3–10. prevention between two and three cypermethrin Van der Merwe, P.J.A. & Swanevelder, C.J. 1988. ‘n applications times provided the first application was done Peulvrotweerstandbiedende cultivar,Harts. Grondbone before 10 WAP (Table 3). Significantly less damage C.3. Boerdery in Suid-Afrika. Departement van occured with three applications at 6, 9, and 11 WAP (P = Landbou en Watervoorsiening, Pretoria, Suid-Afrika. 0.05) compared to all other treatments. In conclusion, Van der Walt, A. 2007. Small holder farmers’ perceptions, diversity of the GLM parasitoid complex increased over host plant suitability and natural enemies of the the five years between the two surveys and should be groundnut leafminer, Aproaerema modicella monitored further. However, more research is needed on (Lepidoptera: Gelechiidae) in South Africa. MSc insecticides that are more compatible with biological Dissertation, North-West University, Potchefstroom, control agents for inclusion in an IPM system for GLM. South Africa. Van Der Walt, A., Du Plessis, H. & Van den Berg, J. 2008. Acknowledgement Using morphological characteristics to distinguish between male and female larvae and pupae of the This research was funded by the Agricultural Research groundnut leafminer, Aproaerema modicella Council. The authors, gratefully acknowledge Ms U du (Deventer) (Lepidoptera: Gelechiidae). Crop Protection Plessis (ARC) who provided technical assistance and Prof. 25, 182-184. G. Prinsloo who identified the Hymenoptera species. Van Der Walt, A., Du Plessis, H. & Van den Berg, J. 2009. Infestation of groundnut by the groundnut leafminer, Aproaerema modicella (Deventer) (Lepidoptera: Gelechiidae) and rates of parasitization of this pest in South Africa. Crop Protection 28, 53-56.