Population Dynamics of Sugarcane Moth Borers In Indonesian Cane Fields Dinamika Populasi Hama Penggerek Tebu di Indonesia

We conducted monthly monitoring of lepidopterous moth borers in four sugarcane fields in Java, Indonesia, from May 2009 to May 2011. Fields sampled belonged to Pesantren Baru, Jombang Baru, Gondang Baru and Subang sugar factories. Three main moth borer species were found to inflict damage to sugarcane plantations in all regions, and these are the stalk borers Chilo sacchariphagus (Bojer) and Chilo auricilius Dudgeon and the top borer Scirpophaga excerptalis (Walker). Tetramoera ( Eucosma ) schistaceana (Snellen) was also encountered but only caused minor damage. Borer populations increased with plant age and reached a peak around January – May in most cases, with the onset of rainfall triggering population rise. All borers coexisted in the same plant with no evidence of competition between the two stalk borers ( C. sacchariphagus and C. auricilius ) over their specific feeding location (internode) or between the two stalk borers and the top borer ( S. excerptalis ) over the same plant. This suggests that an infestation by one species does not make the plant less desirable to be colonised by another. Parasitism rates by natural enemies were very low which reflects the challenges facing biological control efforts in Java. Knowledge generated through this project will improve our understanding of borer dynamics in South East Asia and will enhance our preparedness for potential introduction by any of these pests into Australia.


INTRODUCTION
The top borer Scirpophaga excerptalis (Walker) and the stalk borers Chilo sacchariphagus (Bojer) and C. auricilius Dudgeon (Lepidoptera: Crambidae) are the main species infesting sugarcane crops in Indonesia. S. excerptalis is responsible for the majority of dead heart symptoms in both young and mature cane, while C. auricilius and C. sacchariphagus cause dead hearts only in young cane and later tunnel inside the stalk damaging the internodes (Sallam et al., 2010). Several factors influence damage levels caused by borers ultimately in the field, which makes it difficult to precisely determine their economic impact on the crop.
Varietal resistance/tolerance, abundance of natural enemies, weather patterns as well as farming practices such as planting and harvesting dates, the quality of planting material, fallow management and the level of general farm hygiene are all factors that influence borer populations in the field and their impact on yield (Sallam et al., 2014;Maneerat & Suasa-Ard, 2015;Goftishu, et al., 2017;Goebel and Nikpay, 2018;Nikpay et al., 2020). In addition, a number of borer species coexist on the same plant and collectively damage the crop. Based on field trials in Indonesia, the collective impact of S. excerptalis, C. sacchariphagus and C. auricilius has been estimated by (Goebel et al., 2011) to result in a yield loss of 34.5%. However, total crop destruction due to one or more borer species is not uncommon, and a number of sugarcane projects were terminated in West Papua due to total destruction caused by species of Chilo to preliminary plantations (Wilmar Sugar, personal communication).
Borer species occurring sympatrically may exercise interspecific competition over the same host plant. However, they may also avoid direct competition by either exploiting a different microhabitat or adapting to a different micro-or macroclimate. For instance, the spotted stalk borer, Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) is capable of outcompeting C. orichalcociliellus (Strand) and Busseola fusca (Fuller) (Lepidoptera: Noctuidae) where the two species occur sympatrically in sub-Saharan Africa (Kfir, 1997;Ofomata et al., 2000). However, B. fusca was found to be the dominant borer attacking maize crops in the relatively colder highland regions, while C. partellus is most abundant in the warmer lowlands (Ntiri et al., 2016). On the other hand, several borer species still occur simultaneously in the field and collectively damage the crop. For example, both C. infuscatellus and S. excerptalis were recorded to coexist during January-April in Gujarat, India, while C. auricilius and C. sacchariphagus are both abundant from June to December in cane fields (Pandya, et al., 1996). Similarly, the African sugarcane borer Eldana saccharina (Lepidoptera: Pyralidae) is recorded to damage cane plants collectively with Chilo zacconius (Lepidoptera: Crambidae) and Sesamia sp. (Lepidoptera: Noctuidae) in Ghana (Sampson & Kumar, 1986).
In an attempt to reduce reliance on insecticides for the combat of moth borers in Indonesia, Integrated Pest Management efforts have been established and extended to growers through ISRI entomologists and field staff. Major Indonesian sugar factories invest in biological control laboratories and parasitoid breeding and field release. Parasitoids such as Cotesia flavipes (Hymenoptera: Braconidae), Trichogramma spp. (Hymenoptera: Trichogrammatidae) and Sturmiopsis inferens (Diptera: Tachinidae) are frequently released in cane fields in most cane planting regions in (Sunaryo & Suryanto, 1986;Sallam, 2006;Nurindah, et al., 2020). Furthermore, ISRI has instigated a number of pheromone trapping trials where the effectiveness of certain sex attractants sourced from P3GI sugar factory was evident in monitoring borer populations and supporting early warning systems . Knowledge of infestation timing and borer dynamics in the field is essential prior to the commencement of any IPM program. Our work was conducted to study the population dynamics of the main moth borer species in Java and to examine the coexistence potential of the three borers in the same field. In addition, the impact of natural enemies on borer populations has not been fully examined in Indonesia, and more work is needed to assess the role of the range of parasitoid species in a field situation. Knowledge generated through this work will improve the effectiveness of borer management programs, where appropriate timing of chemical, biological or pheromone trapping applications may be established. This knowledge will also improve our preparedness for exotic borers in Australia through better understanding of factors governing their dynamics in cane fields.

METHODS
Four sugarcane fields where borer abundance was evident were chosen for this study in Java, Indonesia. The fields were about one hectare each and belonged to Gondang Baru, Jombang Baru, Pesantren Baru and Subang sugar factories and were planted with varieties PS851, PS864, PS862 and PS951, respectively. These varieties showed moderate -high susceptibility to borers in a previous study with the exception of PS851 which sustained relatively low borer damage (Sallam et al., 2014). The study commenced shortly after planting or harvesting of the first crop, and field sampling was conducted monthly from May 2009 to May 2011 in all blocks. Fields were planted conventionally at a row spacing of 1.35 meters. In each field, 10 transects (10 meter long each and at least 5 rows apart) were selected randomly in each sampling occasion and 5 plants in each transect were sampled for borer abundance, making a total of 50 sampled plants/field. Numbers of dead hearts, damaged internodes and larval and pupal stages for each plant were recorded. Stalks that showed borer damage were sliced longitudinally and borer stages recovered. Pest stages obtained were taken to the laboratory and bred until they either produced adult moths or a parasitoid. The pest species or the emerged parasitoid was then identified by ISRI and SRA entomologists. If a borer stage was not found the species responsible for the damage could still be identified by examining the tunnel shape or the dead heart symptom. Plant age and rainfall levels (with a lag of 0, 1, 2 or 3 months) were correlated with subsequent borer damage data using Pearson Correlation Coefficient. A linear model was fitted to borer counts and post-hoc mean comparisons were performed accordingly to compare the frequency of occurrence by one species with the frequency of occurrence by more than one species together at the plant, stalk or internode level (SAS Institute Inc. 2011).

RESULTS AND DISCUSSION
Three main moth borer species were encountered in all regions, and these are the stalk borers Chilo sacchariphagus (Bojer) and Chilo auricilius Dudgeon and the top borer Scirpophaga excerptalis (Walker) (Lepidoptera: Crambidae). A fourth borer species,Tetramoera (Eucosma) schistaceana (Snellen) (Lepidoptera: Tortricidae), was also encountered but caused minor damage, where larvae only fed externally on the internodes and around the buds in mature cane. This species was therefore excluded from the data analysis. Figures 1-3    Our study showed that the onset of rainfall triggers borer infestation and that borer numbers are correlated with cane age. This agrees with studies on C. infuscatellus, C. tumidicostalis and S. excerptalis which showed borer infestation to escalate during the growing stages of the crop then decline slightly before harvest in Indian cane fields (Borah & Sarma, 1995;Sing & Varma, 1995;Madan, et al., 1999). While studies in Haryana, India, showed that infestation by C. auricilius and S. excerptalis is positively correlated with maximum temperature, relative humidity and rainfall (Sardana & Das, 2001). Our study also showed that all borer species readily coexist on the same plant, which means that an infestation by one borer does not make the plant less desirable to be colonised by another. This might therefore support earlier studies which suggested that selecting tolerant/resistant varieties to more than one borer species may be feasible (Sallam et al., 2010). While the top borer S. excerptalis exploits a different microhabitat (growing point) to the stalk borers (mature stalks), it might be the case that the two Chilo species avoid direct competition by adapting to different macroclimatic conditions. Previous work by (Sallam et al., 2010) suggested that C. sacchariphagus is more adapted to wetter regions whereas C. auricilius is more tolerant to dry conditions. In addition, the late onset of infestation by C. auricilius relative to C. sacchariphagus might be another competition avoiding mechanism, however it might also mean that C. sacchariphagus infested plants are more vulnerable to infestation by C. auricilius. Nevertheless, C. sacchariphagus is by far the dominant stalk borer species currently in Indonesia and is the one responsible for the majority of internode damage in cane fields (Sallam et al., 2010). It is also not clear if the Indonesian population of C. auricilius is the same species considered to be one of the most damaging pests of sugarcane in northern India. C. auricilius is also recorded to be a key pest of rice in Bangladesh and parts of India and China (Husain & Begum, 1985;Neupane, 1990;Meng et al., 1997). Yet the Indonesian population has always been known to mainly feed on sugarcane until (Hattori & Siwi, 1986) reported it feeding on rice in Java and South Kalimantan. DNA phylogenetic studies are currently underway to assist in understanding the status of each of these species and, ultimately, ensure the establishment of pest specific management strategies (Lange, et al. 2004;Braithwaite, et al., 2016) (Andrew Mitchell, Personal communication).
Borer populations and respective damage reached a peak between January -May in most cases. There was a significant positive correlation between plant age and dead heart symptoms (caused by S. excerptalis) and bored internodes caused by C. sacchariphagus and C. auricilius, indicating infestation progression towards time of harvest (Table 1). There was a positive delayed relationship between rainfall and subsequent internode damage by S. excerptalis and C. sacchariphagus two or three months later in Gondang Baru and Jombang Baru, while in Subang damage levels were significantly correlated with 'same month' rainfall. This correlation was not significant in case of C. auricilius in mostly all regions (Tables 2 and 3).  Table 3. P values indicating correlation between rainfall and internode damage caused by C. sacchariphagus (C.s.) and C. auricilius (C.a.) in 4 sugarcane fields in Java.

Pabrik gula
Lag ( Where all borer species occurred simultaneously in one plot, there was no significant difference between borer counts when the occurrence frequency of S. excerptalis alone was compared to its occurrence together with C. sacchariphagus and C. auricilius on the plant level (T= 0.54, df=8, P=0.607) or stalk level (T=0.59, df= 8, P= 0.57). Similarly, there was no significant difference when the combined occurrence of C. sacchariphagus and C. auricilius was compared to the occurrence of each species individually on the internode level (T=1.25, df=5, P=0.26).
Species of parasitoids that were recovered from the collected borers are shown in table 4. All obtained parasitoids attacked the larval stage, and no egg or pupal parasitoids were encountered. Overall parasitism rates were unexpectedly very low and were typically less than 5% in almost all cases. A few exceptions were Cotesia flavipes Cameron (Hymenoptera: Braconidae) on C. sacchariphagus in Subang (2009) andin Pesantren Baru (2010) where parasitism rates were 14. 28% and 12.96% respectively, and in Jombang Baru (2009) where parasitism rate by Diatraeophaga striatalis Towns. (Diptera: Tachinidae) was 15.55% on the same species. D. striatalis was also responsible for 25.0% parasitism rate on C. auricilius in Jombang Baru (2009). Reasons for the very low rates of parasitism are unknown. Laboratory trials in Java demonstrated that approximately 40% of C. flavipes fertile females failed to lay eggs in C. sacchariphagus or C. auricilius larvae (Sallam, unpublished data). More work is needed to examine the reasons for the lack of natural parasitism in the field by the range of parasitoids and to assess the value of biological control programs in Indonesia. It needs to be stated that the role of Trichogramma spp. egg parasitoids was not assessed due to the difficulty of encountering borer egg batches in the field. Furthermore, the calculated parasitism rates may slightly underestimate actual field rates. This is due to the latent mortality of a fraction of the collected larvae in the lab after collection. In addition, some larval parasitoids may be more attracted to a certain larval stage (i.e. medium or large), while percentage parasitism was calculated in proportion to the total number of obtained larvae.
Chemical or biological control may be most effective if deployed as borer populations begin to rise, which according to our study is between 50 -150 days after planting or time of harvest for C. sacchariphagus and S. excerptalis, and after 150 days for C. auricilius. It is not clear based on our study when the best time to release stage-specific natural enemies is, since all immature stages were abundant over an extended period of time through the duration of the crop. However, the population peak for S. excerptalis small, medium and large larval stages was observed 150, 200 and 250 days after planting, respectively, while this was evident 250 days after planting for C. sacchariphagus and 250 -300 days after planting for C. auricilius. This information will be useful in determining when to commence a parasitoid release program, which should be well before a population peak occurs. In addition, targeted field sampling when plants are between 50 -150 days of age will further assist in deciding on accurate timing of stage-specific parasitoid release.

CONCLUSION
Knowledge gained during this study will improve our understanding of the dynamics of these borer species in cane fields, and will enhance our quarantine measures accordingly. With sugarcane plantations expanding in South East Asia, it is in Australia's interest to maintain strong research and surveillance activities in that region. Australia's engagement in sugarcane research and development in South East Asia will benefit industries in this region and will also ensure a safe and secure sugarcane industry in Australia.