RESEARCH ARTICLE

 

Biological control agents and levels of parasitism of Agrotis segetum (Lepidoptera: Noctuidae) in grain production regions of South Africa

 

 

Z. van Eeden^I; B.S. Muller^II; H. du Plessis^I; J. van den Berg^I

^IIPM program, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa
^IIThe National Museum, Bloemfontein, South Africa

Correspondence

 

 

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ABSTRACT

The management of the cutworm, Agrotis segetum (Denis & Schiffermüller) (Lepidoptera: Noctuidae), is challenging since the larvae spend most of their life cycle hiding underneath weeds or in the soil. Crop producers often report poor efficacy of chemical control, necessitating the development of alternative control strategies. Although many species of parasitoids and entomopathogenic nematodes (EPNs), have been reported from around the world where this pest occurs, no comprehensive list of these species exists, and little is known about their occurrence and impact as biological control agents in South Africa. A literature search yielded 75 parasitoid species, and six EPN species that parasitise A. segetum eggs and larvae. To assess the levels of parasitism in South Africa, cutworm populations were sampled from 14 different geographical regions, reared in a laboratory and monitored for parasitism and other mortality factors. The overall parasitism level recorded in this study was high (43.6%), with Macrocentrus collaris (Spinola) (Hymenoptera: Braconidae) being the most common (39.2%) parasitoid species, followed by Gonia bimaculata Wiedemann (Diptera: Tachinidae) (3.2%) and Periscepsia carbonaria (Panzer) (Diptera: Tachinidae) (1.2%). Entomopathogenic viruses were responsible for 26.1% of larval mortalities, while EPNs (Mermithidae) and entomopathogenic fungi caused 15.7% and 3.2% of mortalities, respectively. The incidence of parasitism, particularly by M. collaris, suggest that parasitoids could play a role in the suppression of A.segetum populations.

Keywords: biological control, cutworms, entomopathogenic, nematodes, maize, parasitoids, pest management

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INTRODUCTION

Cutworms (Agrotis spp.) are polyphagous and cause damage to crops such as maize (Zea mays), potatoes (Solanum tuberosum), tomatoes (Solanum lycopersicum), turnips (Brassica rapa) and many other host plants (Van den Berg 2024; 2025). The two Agrotis species that are considered the most important, are Agrotis ipsilon (Hüfnagel) (Lepidoptera: Noctuidae) which has a worldwide distribution, and Agrotis segetum (Denis & Schiffermüller) which occurs in Africa, Europe, the Middle East and Southeast Asia (Blair 1976; Drinkwater 1980; Bowden et al. 1983; Hülbert and Süss 1983; Esbjerg and Sigsgaard 2014; Rodingpuia and Lalthanzara 2021). Agrotis segetum is the dominant cutworm species and most important pest of maize seedlings in South Africa (Du Plessis 2000; Van den Berg et al. 2014; Drinkwater 2017).

Weeds play an important role in the ecology and pest status of cutworms. Agrotis segetum moths do not go into diapause, are active throughout the winter and lay their eggs on winter weeds which provide food and shelter for slow-developing larvae (Drinkwater 1980; Bowden et al. 1983; Drinkwater 2017). These overwintering larvae attack emerging maize seedlings during spring and early summer (Drinkwater 2017). The removal of host plants (weeds) from crop fields at least five weeks prior to planting, is recommended to reduce habitat suitability for larval survival and to ensure that larvae starve to death before the crop is planted (Drinkwater and Janse van Rensburg 1992, Van den Berg et al. 2014, Drinkwater 2017).

Soil applications of pyrethroids, at or just after planting, are commonly done for cutworm control. These applications are often reported to be ineffective and pose risks to the environment and non-target organisms such as parasitoids and predators of crop pests. There is, however, no information available on the diversity and role of natural enemies in the suppression of cutworm populations in South Africa.

Predators, parasitoids, entomopathogenic fungi, viruses and nematodes are promising biological control agents of cutworms (Wennmann et al. 2015; Salim et al. 2016; Staude et al. 2022). Carabid beetles have been reported to reduce cutworm numbers in crop fields in the USA as they prey on the eggs, larvae and pupae of these pests (Best and Beegle 1977; House and Alzugaray 1989; Frank and Shrewsbury 2004). Entomopathogenic fungi (EPFs) have been reported to cause mortality of cutworms in Northern Europe (Steenberg and 0gaard 2000), England, Wales (Sherlock 1983) and Egypt (El-Hawary and Abd El-Salam 2009; Ahmed et al. 2022). Similarly, entomopathogenic viruses (EPVs) can infect cutworms and cause mortality under laboratory and field conditions (Allaway and Payne 1983; Boughton et al. 1999; El-Salamouny et al. 2003; Bourner and Cory 2004; Jakubowska et al. 2006; Wennmann et al. 2015). Cutworms are highly susceptible to entomopathogenic nematodes (EPNs) (Morris and Converse 1991). Nematodes of the Mermithidae family have been reported to parasitise cutworm larvae in the USA (Puttler and Thewke 1971; Puttler et al. 1973) and China (Chen et al. 1989; Wang and Wang 1990; Li et al. 1993).

Many parasitoids have been recorded for Agrotis spp. worldwide, mainly from larvae (Schoenbohm and Turpin 1977; Sajap et al. 1978; Levine and Clement 1981; Foster and Ruesink 1984; El-Heneidy and Hassanein 1987; Khan and Özer 1988; Caballero et al. 1989; Caballero et al. 1993; Kara and Tschorsnig 2003; Gözüaçik et al. 2009; Cerretti and Tschorsnig 2010; Lee and Han 2010; Lekin et al. 2016; Salim et al. 2016; El-Hawagry 2018; Hou et al. 2018; Lutovinovas et al. 2018). In Spain, for example, the most important of these were Periscepsia carbonaria (Panzer) (Diptera: Tachinidae) and Macrocentrus collaris (Spinola) (Hymenoptera: Braconidae) (Caballero et al. 1989). The tachinid larval-pupal parasitoid, Gonia bimaculata Wiedemann (Diptera: Tachinidae) have also been recorded in Spain and Turkey (Caballero et al. 1989; Gözüaçik et al. 2009). In other parts of the world, cutworm infestations and their damage are significantly reduced when levels of parasitism are high (Schoenbohm and Turpin 1977; Sajap et al. 1978; Caballero et al. 1993). The lack of information on parasitoid-host associations in southern Africa is highlighted by the fact that only four records exist of Braconidae species (unidentified) that parasitise A. segetum among those that have been recorded for 66 Lepidoptera families in southern Africa (Staude et al. 2022).

Little information exists regarding which Agrotis species dominate in maize fields and the occurrence of biological control agents in South Africa. The following cutworm species have been listed to occur in maize fields: Agrotis subalba Walker, the grey cutworm; A. ipsilon, the black cutworm; Agrotis longidentifera (Hampson), the brown cutworm; and the common cutworm, A. segetum (Drinkwater 2017).

Therefore, the aim of this study was to conduct a survey of the diversity and incidence of biological control agents and to determine which Agrotis spp. occur in grain crop fields in South Africa, and to compile a checklist of parasitoids that have been recorded for A. segetum in other parts of the world.

 

MATERIALS AND METHODS

Collection sites

Larvae of A. segetum populations were collected from maize, soybean and sunflower fields at the localities listed in Table 1. The maize production region was classified into three regions based on their overall environmental conditions and soil type (Haarhoff et al. 2020). The regions are: (i) Western (35% of total annual maize production), (ii) Eastern (45%), and (iii) KwaZulu-Natal (KZN) (10%). The Western and Eastern areas are located on the South African inland plateau (1 500-1 800 m above sea level) (Adisa et al. 2018), with hot summers and very cold winters. The KZN region is known for long hot summers and mild winters, with an average annual rainfall of 500-800 mm (Adisa et al. 2018).

Larvae were sampled in October, November, January and February during the 2023/24 and 2024/25 cropping seasons. At each location, areas with seedling stand loss was identified within fields since the likelihood of finding cutworm larvae in these areas was high. Insecticides were applied at all the collection sites prior to larval collection, except at Kokstad, Mooirivier, Underberg, and Harrismith. This was because collections were only made at localities where producers reported cutworm infestations and because they did not postpone insecticide applications for a few days until larvae could be collected. If any evidence of cutworm damage to maize seedlings, weeds or cover crop plants were evident, the surrounding topsoil (3-10 cm) was carefully searched, and any observed larvae were collected. Nearly all larvae (> 98%) that were collected were in the 5th or 6th instar. Larvae that are in earlier stages of development do not easily sever seedings and are not often observed in the field. Larvae were placed inside plastic containers aerated with plastic mesh-infused lids (380 mm x 270 mm χ 140 mm) and provided with weedy plants retrieved from the collection sites as a temporary food source. Different quantities of larvae were collected from each collection site and then transported to the Entomology laboratory at the North-West University, Potchefstroom, South Africa. Larvae were in transit for the minimum time feasible (< 36 hrs).

Rearing conditions and causes of mortality of cutworm larvae

After the larvae arrived at the laboratory, they were removed from the plant material and transferred into individual plastic containers with aerated mesh-infused lids (50 mm χ 50 mm χ 50 mm). Larvae were reared on artificial diet inside these containers until they either pupated, parasitoids emerged, or died. Stonefly Heliothis Premix Diet (Ward's Natural Science Establishment, LLC, USA) was provided as food for larvae. To prevent starvation of larvae, food was provided ad libitum. The containers were kept in an insect rearing room at 28 ± 1 °C, 65 ± 5% humidity and a 14L:10D photoperiod.

Larvae were inspected every second day and those that appeared sick or parasitised were removed and kept separately to identify the possible causes of mortality. Parasitoids that emerged were kept separately for each larva. Pupae were kept inside containers until moths or parasitoids emerged. The number of parasitoid pupae that were present in each container after the larvae died was determined for one of the parasitoid species, while the numbers of parasitoid cocoons per container was determined for another. The mean number of parasitoids that emerged per larvae was then calculated. Parasitoids were then identified to species level.

Entomopathogenic nematodes that emerged from larvae were placed in 70% ethanol. The number of EPNs per parasitised cutworm larva was recorded. Dead larvae that had a dark brown appearance and from which no parasitoids emerged were considered to have died from an EPV infection. Dead larvae covered with white or green spores were considered to have died from an EPF infection. The number of dead larvae exhibiting symptoms ofEPVs or EPFs were also recorded. If the cause of larval death could not be identified, these were indicated as unknown.

Species identification and compiling of checklist

The parasitoid species reared from larvae were identified by means of the taxonomic keys of Crosskey (1984), Emden (1960) and O'Hara and Cerretti (2016). Voucher specimens of the Tachinidae were deposited in The National Museum, Bloemfontein, South Africa, and the Braconidae in the Iziko South African Museum, Cape Town, South Africa (https://www.waspweb.org/Ichneumonoidea/Braconidae/Macrocentrinae/Macrocentrus/Macrocentrus_collaris.htm). A literature search was conducted to compile a comprehensive list of A. segetum parasitoids. This search included CABI abstracts, Google Scholar and published literature on this pest.

Data analysis

Descriptive analyses were used. The percentage contribution of each of the mortality factors to overall larval mortality at each of the sampling localities were determined.

 

RESULTS

Incidence of larval mortality

A total of 2 723 larvae were collected from all the sites. The mean mortality of larvae from all sampling localities was 63.2% (n = 1 663). Larval mortality ranged from 41.6% to 92.1% for the different localities (Table 2). The overall mean incidence of larval parasitism was 43.6% and the overall mean incidence of larvae that died due to EPF and EPV infections were 3.2% and 26.1% respectively. The overall mean incidence of mortality due to EPNs were 15.7% while 11.4% of larvae died of unknown causes.

Biological control agents of Agrotis segetum

Three parasitoid species were encountered during this study, two that emerged from larvae and one that emerged from pupae. These species were Periscepsia carbonaria (Panzer) (Diptera: Tachinidae), Gonia bimaculata Wiedemann (Diptera: Tachinidae) and Macrocentrus collaris (Spinola) (Hymenoptera: Braconidae). Photos of the voucher specimens of these three species are provided in Figure 1. An EPN species (Mermithidae) was also identified from larvae. The percentage contribution of different biocontrol agents to overall mortality of A. segetum larvae and pupae is provided in Figure 2.

 

 

Macrocentrus collaris occurred at all sites (Figure 2) and was responsible for the highest overall incidence of mortality (39.2%). The highest incidence of parasitism by M. collaris at a single site was at Kroonstad (75.5%) and the lowest at Harrismith (4.6%). The number of parasitoids that emerged per cutworm larvae ranged between 20 and 130 (mean = 68).

Periscepsia carbonaria was recorded at three of the fourteen sites, i.e., Wakkerstroom, Parys and Winterton, and was responsible for 1.2% of the overall larval mortality (Figure 2). The highest incidence of parasitism by P. carbonaria was at Parys (10.0%) and the lowest at Winterton (1.5%). The number of parasitoids that emerged per larva ranged from 1 to 4 (mean = 2).

Gonia bimaculata was recorded at five of the fourteen sites, i.e., Wakkerstroom, Parys, Kroonstad, Bronkhorstspruit and Lichtenburg (Figure 2) and contributed to 3.2% of the overall larval mortality. The highest incidence of parasitism was recorded at Bronkhorstspruit (22.2%) and the lowest at Kroonstad (0.5%).

The mermithid nematode occurred at six of the fourteen sites (Figure 2) with the highest incidence of parasitism recorded at Vrede (73.9%) and the lowest at Kokstad (14.9%).

The number of EPNs that emerged per cutworm larva ranged from 1 to 41 (mean = 5). EPFs were recorded from seven of the fourteen sites (Figure 2). The highest incidence of infection was recorded at Newcastle (11.9%) and the lowest at Kroonstad (1.1%). Larvae with EPV infections were recorded from 10 of the fourteen sites (Figure 2) with the highest incidence of EPV infected larvae being recorded at Underberg (71.0%) and the lowest at Harrismith (7.7%).

Checklist of Agrotis segetum parasitoids

The literature search yielded 57 parasitoid species, belonging to the Hymenoptera and Diptera. These were 12 species of Braconidae, 13 species of Ichneumonidae and 28 species of Tachinidae. The three parasitoid species recorded during this study have previously been recorded on A. segetum in other parts of the world (Table 3). Six species of entomopathogenic nematodes (Mermithidae and Steinernematidae) were recorded (Table 3).

 

DISCUSSION

Macrocentrus collaris was the most abundant parasitoid (29.2%) recorded across all the entire maize production region. This parasitoid was also recorded in Russia where it was abundant and widespread on A. segetum in cotton fields (Ragimov and Rustamova 1977). Macrocentrus collaris was also recorded as a parasitoid of cutworms in Spain (Caballero et al. 1989). Macrocentrus spp. are all koinobiont endoparasitoids of lepidopteran larvae. Although a few of these species attack noctuids such as cutworms that feed on roots or inside stems of plants, they are most frequently observed to attack Pyralidae and Tortricidae that feed in shoots or rolled leaves (Shaw and Huddleston 1991). Hosts of Macrocentrus spp. are easily attacked during movement between plants and the middle-instars are largely targeted. Oviposition takes place into any part of the haemocoel of the overwintering host. The parasitoid larvae feed on the host before emerging from it to complete their feeding externally and moult into the final instar. Individual brownish cocoons are spun and arranged within a communally spun outer envelope on the surface of the larva (Shaw and Huddleston 1991).

The second most abundant parasitoid was G. bimaculata (3.2%). This parasitoid has also been reported to parasitise A. segetum in Egypt, Italy, Korea, China, Spain and Turkey (Caballero et al. 1989; Gözüaçik et al. 2009; Lee and Han 2010; El-Hawagry 2018; Hou et al. 2018). Other tachinids that were reported as parasitoids of Agrotis spp., including A. ipsilon, are Gonia chinensis (Wiedemann) (Diptera: Tachinidae), Gonia ornata Meigen (Diptera: Tachinidae) in China and Italy (Lee and Han 2010; Hou et al. 2018), Linnaemya comta (Fallén) (Diptera: Tachinidae) in the USA, Spain and Turkey (Levine and Clement 1981; Caballero et al 1989; Kara and Tschorsnig 2003; Stireman et al. 2006) and Tachina magnicornis (Zetterstedt) (Diptera: Tachinidae), Spallanzania hebes (Fallén) (Diptera: Tachinidae), Peleteria rubescens (Robinaeau-Desvoidy) (Diptera: Tachinidae) and Phryxe vulgaris (Fallén) (Diptera: Tachinidae) were recorded as parasitoids of Agrotis spp. in Italy (Cerretti and Tschorsnig 2010).

Gonia spp. incubates microtype eggs in which ova are ingested by hosts as they feed. These eggs hatch within the gut of the host larvae, and the emerging first-instar parasitoid larva burrows into the haemocoel (Stireman et al. 2006). Gonia bimaculata seem to be monophagous on Agrotis species since no records were found in the literature of it parasitising other lepidopteran hosts.

In the current study, the least abundant parasitoid (1.2%) was the tachinid fly, P. carbonaria. Periscepsia carbonaria was also found as a parasitoid of A. segetum in cotton fields in Russia (Ragimov and Rustamova 1977) and multi-parasitism of up to four parasitoids emerging from a single host-larva has been recorded. This is similar to observations made during this study where three to four parasitoids emerged from each parasitised A. segetum larva. Periscepsia carbonaria has also been confirmed as a parasitoid of A. segetum in other countries such as Pakistan (Khan 1989; Khan 2002), Turkey (Kara and Tschorsnig 2003; Gözüaçik et al. 2009; Lekin et al. 2016; Lutovinovas et al. 2018), Spain (Caballero et al. 1989) and India (Kumari and Chandla 2010; Chandel et al. 2022).

Larvae from P. carbonaria eggs are laid externally on A. segetum larvae, after which they infest the host during their first instar (Zethner et al. 1987). The parasitoid larvae move freely in the haemocoel for five to six days before forming a respiratory tunnel through its integument. It progresses through two additional larval instars after which the parasitoid larvae leave the host to pupate. Periscepsia carbonaria parasitises A. segetum and A. ipsilon larvae and older larvae (L4-L6) are less parasitised compared to younger larvae (L1-L3) (Khan 2002). Similar to G. bimaculata, P. carbonaria also seem to be monophagous on Agrotis spp. since no records were found in the literature of it parasitising other lepidopteran hosts.

The second highest overall incidence of mortality was caused by entomopathogenic viruses (26.1%). Although the viruses were not identified in this study, other studies reported that cutworms are susceptible to EPVs (Zethner et al. 1987; Bourner et al. 1992).

The incidence of larval mortality due to the mermithid nematode was low (15.7%) in comparison with other studies. In Illinois (USA), 64.5% larvae of an A. ipsilon population collected from maize fields were parasitised by Hexamermis arvalis (Poinar & Gyrisco) (Nematoda: Mermithidae) (Puttler et al. 1973). Furthermore, in China, parasitism of up to 63% of A. ipsilon by Hexamermis spp. was reported (Chen et al. 1989). In the present study, A. segetum larvae were often parasitised by more than one nematode, which is similar to reports of up to three or four larvae of Hexamermis agrotis (Nematoda: Mermithidae) recorded from a single A. segetum larva (Li et al. 1993).

The overall incidence of mortality caused by EPFs was low (3.2%). In Northern Europe, 50 to 100% mortality of overwintering A. segetum larvae were ascribed to infection by a rare fungal pathogen, Tolypocladium cylindrosporum (Hypocreales: Ophiocordycipitaceae) (Steenberg and 0gaard 2000). Other authors have also reported EPFs as significant biological control agents of Agrotis spp. In Europe, two naturally occurring fungal pathogens, Entomophthora megasperma (Entomophthorales: Entomophthoraceae) and Fusarium solani (Hypocreales: Nectriaceae), were reported to infect mature A. segetum larvae, prepupae and pupae (Sherlock 1983). Studies conducted in Egypt reported 100% larval mortality of A. ipsilon after treatment with an EPF product (Priority, Isaria fumosorosea (Hypocreales: Cordycipitaceae)) (El-Hawary and Abd El-Salam 2009), 50% mortality of A. ipsilon larvae caused by Beauveria bassiana and Metarhizium anisopliae (Gabarty et al. 2014) and 100% mortality by B. bassiana (Ahmed et al. 2022).

Although parasitoids can parasitise Agrotis larvae during all phases of their life cycle, the effectiveness and consequences of parasitism fluctuate depending on larval instar. Studies have shown that, under laboratory conditions, parasitism rates can be as high as 87.5% in 1st instars and 100% in 3rd instars, with early instars (L1-L3) being the most vulnerable (Caballero et al. 1993). In contrast, later instars show a significant reduction in susceptibility, with parasitism ranging from 34% in the 5^th-instar to 4% in 6^th-instar larvae (Caballero et al. 1993). Since 3rd and 4th instars provide optimum conditions for parasitoid development, parasitoids tend to favour these stages. Since L1-L3 larvae are largely active during the day (Blair 1975) and parasitoids are associated with flowering weeds which provide nectar as food (Foster and Ruesink 1984), the likelihood exists that the L5-L6 larvae collected during this study were parasitised during winter months, or at least several weeks before planting. Although parasitism in the late instars is less common, when it does occur, parasitoids emerge from the late 5th or early 6th instar when the latter stop feeding and ultimately perish (Schoenbohm and Turpin 1977). This suggests a close relationship between parasitoid and host development, with increased parasitism rates that occur when environmental conditions, such as higher temperatures during the planting season, occur (Caballero et al. 1993).

The development of parasitoids within Agrotis larvae results in reduced feeding activity and altered behaviour (Sajap et al. 1978). Initially, they behave exactly like non-parasitised larvae, remaining active and feeding normally until just before the emergence of the parasitoids (Sajap et al. 1978). However, the feeding period is greatly shortened by parasitism, with parasitised larvae still feeding for an average period of 4.5 days as opposed to 10.8 days for non-parasitised larvae of the same age (Sajap et al. 1978). Parasitised larvae damage an average of 4.4 plants, whereas non-parasitised larvae may damage 13.9 plants (Sajap et al. 1978).

Parasitism restricts feeding by 6th instar larvae, which normally consumes 77-86% of a larva's total food consumption during its life cycle (Schoenbohm and Turpin 1977). This is ascribed to the cessation of feeding and decreasing larval activity. Similar to healthy pupating larvae, parasitised larvae tunnel into the soil before parasitoid emergence. When, in the case of M. collaris, parasitoid larvae emerge, they build cocoons close to the host's body, which prevents the host from pupating and ultimately results in its death (Sajap et al. 1978).

It is important to note that nearly all the larvae collected in this study were sampled from fields on which one to three insecticide applications had been applied for cutworm control, prior to sampling. However, no information is available on the level of exposure of the larvae to insecticides.

Compared to Agrotis spp. parasitoid diversity reported in other countries (Schoenbohm and Turpin 1977; Sajap et al. 1978; Levine and Clement 1981; Foster and Ruesink 1984; El-Heneidy and Hassanein 1987; Khan and Özer 1988; Caballero et al. 1989; Caballero et al. 1993; Kara and Tschorsnig 2003; Gözüacik et al. 2009; Cerretti and Tschorsnig 2010; Lee and Han 2010; Lekin et al. 2016; El-Hawagry 2018; Hou et al. 2018; Lutovinovas et al. 2018), the diversity in South Africa seems to be low (Staude et al. 2022). The low parasitoid diversity recorded on A. segetum could indicate that this species has spread into southern Africa where it became naturalised. However, the three species recorded during this study (P. carbonaria, M. collaris and G. bimaculata) are also the dominant species that parasitise A. segetum in other regions of the world.

The overall mean incidence of larval parasitism at the different localities in this study was high (mean: 43.6%; range: 4.675.5%). This shows that parasitoids have the potential to supress cutworm numbers in crop fields. However, the beneficial effects of parasitism come into effect too late since parasitised larvae continue to damage seedlings. Cultural control strategies such as the removal of host plants (weeds) from fields to starve larvae to death before the crop is planted, is recommended for cutworm management (Drinkwater 1980). This will result in a reduction in the use of insecticides and protection of beneficial organisms at the start of the cropping season. Development of conservation biocontrol strategies, on the other hand, remains challenging. It is well known that plant species diversity influences the natural occurrence of biological control agents, specifically parasitoids. The host plants (weeds) that ensures survival of the pest are also critical for the survival of the parasitoids which utilise their pollen and nectar. The role that weeds play with regards to the presence and longevity of natural enemies have been reported by several authors (Foster and Ruesink 1984; Foster and Ruesink 1986a, 1986b; Pavuk and Stinner 1992; Capinera 2005). These interactions complicate the development of conservation biocontrol strategies for cutworms, since removal of weeds to control the pest also implies the removal of the resources used by parasitoids.

 

CONCLUSIONS

This study showed that several species of parasitoids, as well as an EPN species, attack or infect A. segetum in South Africa, and that these agents are responsible for high levels of mortality. The high incidence of mortality ascribed to EPFs, EPNs and viruses warrant further investigation to identify possible biocontrol agents for use in the management of A. segetum. Further studies should include more localities within the grain production regions of South Africa and focus on the environmental conditions and cultivation practices that might have an influence on the abundance of biological control agents.

 

ACKNOWLEDGMENTS

This study was funded by GrainSA (Project: 3R00591). The authors thank Dr. Simon van Noort (Curator of Entomology, Iziko Museums of South Africa) and Kees van Achterberg (Naturalis Biodiversity Center, Leiden, The Netherlands) for identification of Macrocentrus collaris.

 

DATA STATEMENT

All data are provided in the paper.

 

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.

 

AUTHOR CONTRIBUTIONS

JvdB and HdP conceived and designed the study. ZvE conducted all field work, data curation and basic statistical analyses. ZvE and JvdB wrote the manuscript. BM identified the dipeterna parasitoids. JvdB, ZvE and BM prepared the manuscript for submission. All authors read and approved the final manuscript.

 

ORCIDS

Z. van Eeden: https://orcid.org/0009-0008-9176-2081

B.S. Muller: https://orcid.org/0000-0002-7304-4050

H. du Plessis: https://orcid.org/0000-0003-1163-1468

J. van den Berg: https://orcid.org/0000-0002-6831-3180

 

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Correspondence:
J. van den Berg
Email: johnnie.vandenberg@nwu.ac.za

Received: 22 August 2025
Accepted: 28 October 2025