Biological Control Of Aphids Research Articles

Biological Control of Aphids in China: Successes and Prospects.

Aphids are small, soft-bodied insects, and many are notorious pests of field crops, vegetables, fruit trees, ornamental plants, and trees. In China, there is an increasing emphasis on utilizing biological control agents, including aphidopathogenics, and selective pesticides for the management of aphids. In particular, preventive integrated pest management strategies with early interventions reduce the financial and environmental costs associated with treatments of outbreaks. Decades of progress have proved that biological control is a cost-effective and environmentally safe control option. Here, we review the history and progress of aphid control, with an emphasis on major natural enemies, mass-rearing, and conservation, and provide two successful cases, constraints, and future perspectives on aphid biological control in China.

The ATP-binding cassette transporter subfamily G member 4 mediates cuticular hydrocarbon transport to regulate drought tolerance in Acyrthosiphon pisum

ABC transporters are a highly conserved membrane protein class that promote the transport of substances across membranes. Under drought conditions, insects primarily regulate the content of cuticular hydrocarbon (CHC) to retain water and prevent evaporative loss. Involvement of ABC transporter protein G (ABCG) subfamily genes in insect CHC transport has been relatively understudied. In this study, we demonstrated that ABCG4 gene in Acyrthosiphon pisum (ApABCG4) is involved in CHC transport and affects drought tolerance by regulating CHC accumulation. ApABCG4 is strongly expressed in the abdominal cuticle and embryonic stages of A. pisum. Effective silencing of ApABCG4 was achieved using RNAi, and the silencing duration was analyzed. ApABCG4 silencing resulted in a significant decrease in the total and component contents of the CHC and cuticular waxy coatings of A. pisum. Nevertheless, the internal hydrocarbon content remained unchanged. The lack of cuticular hydrocarbons significantly reduced the drought tolerance of A. pisum, shortening its survival time under drought stress. Drought stress caused significant upregulation of ApABCG4. Molecular docking showed that ApABCG4 has a high binding affinity for nine n-alkanes of CHC through electrostatic interactions. These results indicate that ApABCG4 is a novel RNAi target with key applications in aphid biological control.

Through the green mosaic: Different tropical vegetation types have complementary effects on parasitoid diversity and biological control in organic agroecosystems

Land use change threaten global biodiversity, impacting ecosystem services, especially in diverse tropical regions. Yet, biodiversity conservation does not guarantee ecosystem services provision, given species' variable responses to local and landscape factors. Here, we evaluate how the landscape and local resources affect parasitoid diversity and aphid biological control in a tropical organic crop. Locally, we compared parasitoid communities within the crops and on adjacent non-crop plant strips and evaluated the effect of flower resource abundance on parasitoid diversity. At the landscape scale, we analyzed the effect of natural areas and their specific vegetational types on parasitoid diversity and the scale of these effects. Finally, we evaluated the relationship between biodiversity and biological control. Non-crop plant strips had higher parasitoid species richness and abundance than the crops, but similar species composition. Flower resource abundance in the non-crop strips negatively affected parasitoid richness. Natural areas in the landscape benefited parasitoid richness at a close range (0.42 km) and reduced parasitoid abundance at a wider scale (1.75 km). Forests and savannas increased parasitoid richness and reduced abundance, while grasslands drive parasitoid abundance and may disrupt species richness. Savannah areas, where trees and grasses coexist boosted the positive effects of forests on species richness and of grasslands on abundance. Parasitoid species richness benefited biological control exclusively in communities with intermediate and high number of parasitoid species. Our findings show that natural vegetation types with different wood densities have complementary effects in parasitoid diversity in tropical agroecosystems and represent a useful baseline for development of management and zoning plans.

Landscape structure and composition affect aphid biological control in alfalfa fields, but regional differences prevail

Landscape structure and composition affect aphid biological control in alfalfa fields, but regional differences prevail

A molecular approach to unravel trophic interactions between parasitoids and hyperparasitoids associated with pecan aphids.

Advances in molecular ecology can overcome many challenges in understanding host-parasitoid interactions. Genetic characterization of the key-players in systems helps to confirm species and identify trophic linkages essential for ecological service delivery by biological control agents; however, relatively few agroecosystems have been explored using this approach. Pecan production consists of a large tree perennial system containing an assortment of seasonal pests and natural enemies. As a first step to characterizing host-parasitoid associations in pecan food webs, we focus on aphid species and their parasitoids. Based on DNA barcoding of field-collected and reared specimens, we confirmed the presence of 3 species of aphid, one family of primary parasitoids, and 5 species of hyperparasitoids. By applying metabarcoding to field-collected aphid mummies, we were able to identify multiple species within each aphid mummy to unravel a complex food web of 3 aphids, 2 primary parasitoids, and upward of 8 hyperparasitoid species. The results of this study demonstrate that multiple hyperparasitoid species attack a single primary parasitoid of pecan aphids, which may have negative consequences for successful aphid biological control. Although further research is needed on a broader spatial scale, our results suggest multiple species exist in this system and may suggest a complex set of interactions between parasitoids, hyperparasitoids, and the 3 aphid species. This was the first time that many of these species have been characterized and demonstrates the application of novel approaches to analyze the aphid-parasitoid food webs in pecans and other tree crop systems.

Flowering areas enhance insect pollinators and biological control agents in wheat intensive agro‐ecosystems

Abstract This 4‐year study (2018–2021) aimed at investigating the effects of flowering areas inserted at the margin of soft wheat fields (Triticum aestivum L.) in comparison with spontaneous field margins. The action formed part of a multidisciplinary initiative promoted by the Barilla food company, aimed at promoting the sustainable production of soft wheat. Specific aims were to study the effects of flowering areas on (i) the abundance and species richness of insect pollinators, including wild bees, syrphids and butterflies; (ii) the levels of wheat aphid and bug infestations and (iii) the assemblages of biological control agents of aphids (coccinellids and aphid mummies as a result of parasitization). Insect surveys were carried out on 61 wheat‐growing farms located in Northern Italy. Insect pollinators were sampled on all farms, whereas wheat aphids, wheat bugs and aphid biological control agents were investigated in a sub‐sample of 20 farms. Results generally indicated a positive impact of flowering areas on multiple taxa in comparison with spontaneous field margins. The abundance of pollinators and coccinellids was significantly enhanced by the flowering areas. Aphid mummies showed an interaction between strategies and distances with more mummies at 5 m in wheat plots close to flowering areas and at 50 m in the plots close to spontaneous field margin (control). Flowering areas were validated as an important tool for promoting beneficial taxa in agro‐ecosystems. However, the successful establishment of this ecological infrastructure was suggested to rely on several factors, which included both the selection of suitable flowering plant species and the implementation of appropriate management practices.

The right banker plant for the right application: Comparison of three candidates for aphid biocontrol, barley (Hordeum vulgare L.), corn (Zea mays L.), and finger millet (Eleusine coracana (L.) Gaertn).

In temperate regions, aphid biological control in greenhouses is mostly achieved by the regular release of biocontrol agents. Due to the rapid growth rate of the aphid population, biocontrol agents must be released frequently in order to be present before pest outbreaks and to act rapidly to prevent exceeding the economic threshold. Banker plants reduce these numerous releases by providing natural enemies with a high-quality environment to develop and reproduce. Optimally, banker plants should be easy to produce, resistant to environmental conditions, provide a large amount of suitable banker prey in order to produce a high number of biocontrol agents, and resist the herbivory pressure of the banker prey. The present study aimed to compare the value of three banker plant candidates of the Poaceae family under laboratory and greenhouse conditions: barley (Hordeum vulgare L.), finger millet (Eleusine coracana (L.) Gaertn), and corn (Zea mays L.). Our results show that the three plants were suitable for different contexts. Finger millet yielded the biggest fresh plant biomass, supported the highest load of banker prey, and resisted aphid feeding longer than the other plant species. Corn was the cheapest to produce, and barley was the fastest to grow. Overall, finger millet could be more fitted for long crop cycles, pests with rapid population growth rates, and voracious or fast-reproducing biocontrol agents. Meanwhile, barley and corn may be better suited for rapid crop cycles, pests with slow population growth rates, and biocontrol agents that are not too voracious or have low reproductive rates. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Landscape simplification, urbanization, biological invasions, and climate change: a review of the major threats to native coccinellids in Central Chile

AbstractCoccinellids (Coleoptera) are important natural enemies of pests in agroecosystems. However, worldwide, native species face several threats, including landscape simplification, biological invasions, and climate change. In Central Chile, one of the global biodiversity hotspots, coccinellid communities are very diverse and are composed mostly of native species, which are most common in less disturbed habitats. In alfalfa fields, native coccinellids play a crucial role in the biological control of aphids, even when they are less abundant than exotics. However, in the last 2 decades, native species in this crop have declined in abundance and diversity. Our long‐lasting field and laboratory studies have shown that this decline is associated with: (1) the invasion of Harmonia axyridis (Pallas), which has superior competitive abilities and escapes more from parasitism; (2) the simplification of agricultural landscapes, loss of natural habitats, and urbanization; and (3) increasing environmental temperatures and decreasing precipitation. The decline in native coccinellid populations has resulted in a loss of taxonomic and functional diversity of assemblages, which may jeopardize biological control. Alfalfa fields and natural and semi‐natural habitats may offer an opportunity for the conservation of native coccinellids in agricultural landscapes. Such conservation might be achieved with better management of alfalfa fields and surrounding areas.

No evidence for competition over floral resources between winter-active parasitoids and pollinators in agroecosystems

Warming temperate winters are resulting in increased insect winter activity. With modern agroecosystems largely homogenous, characterised by low floral diversity, competitive interactions may arise between flower-visiting species, with potential implications for the ecosystem services they provide (e.g. biological control and pollination). Flower strips may be implemented during winter months to support flower-visiting insects and enhance ecosystem service provision. Employing field trials conducted in Brittany, France between 2019 and 2021 and laboratory cage experiments, the current study examined the impact of winter flower strips on aphid biological control performed by parasitoid wasps and the potential for competitive interactions between winter-active parasitoids and pollinators. Results revealed that parasitism rate was not enhanced by the presence of winter flower strips. This lack of effect was not the consequence of pollinator presence, and the current study found no effect of pollinator abundance on parasitism rate. Flower strips may thus be implemented during winter months to support nectar-feeding insects when floral resources are scarce, with no evidence of exploitative competition between pollinators and parasitoids, nor a detrimental impact on biological control provision.

Overview of the current status of Charipinae (Hymenoptera, Cynipoidea, Figitidae): taxonomy, distribution, and diversity.

The subfamily Charipinae (Hymenoptera: Cynipoidea: Figitidae) has had a problematic taxonomic history as many species have been described without comprehensive revisions being undertaken. Reliably identifying these species based on morphological assessment has been almost impossible. Recently, the types of all species have been re-examined and photographed, resulting in numerous taxonomic corrections that have been published elsewhere. Consequently, a summary checklist of all species that have ever been described within the Charipinae is provided with their current accepted status, including all associated references dealing with the historical nomenclatural changes and synonymy. We also provide up-to-date information on the diversity and distribution patterns of Charipinae to assist researchers working on these species in aphid biological control programs.

Aphid biological control in arable crops via flower strips: The predominant role of food resources over diversity effects

Abstract Plant taxonomic and functional diversity promotes interactions at higher trophic levels, but the contribution of functional diversity effects to multitrophic interactions and ecosystem functioning remains unclear. In agroecosystems, flower strips can be sown to promote biodiversity and associated services, but their plant composition is poorly considered from a functional diversity perspective so as to promote multitrophic interactions. In a field experiment, aphid biological control was compared across contrasting flower strip mixtures, over a 4‐year arable crop rotation. The effects of plants providing food resources, that is nectar and legumes supporting alternative hosts and prey, and the effects of plant species richness and functional dispersion were investigated on the biological control of aphid populations. In general, increases in the percentage of plant cover providing nectar and alternative prey (Fabaceae) to natural enemies increased predator–prey ratios and aphid parasitism and decreased aphid population growth rates. These effects however depended on the crop species. Species richness and the functional dispersion of traits involved in plant–arthropod interactions were of lesser importance, and the directions of their effects were crop‐specific. Synthesis and applications. These findings provide useful insight for designing perennial plant mixtures for creating or restoring habitats supporting aphid regulation. It is not adequate to sow any mixture containing simply flowering plants. Plant mixtures should comprise a large proportion of plant species supporting alternative prey, like legumes, and species producing nectar being easily accessible to natural enemies (corollas with nondeep nectar). To be efficient over a crop rotation, with aphids being present at different seasons, these nectar resources should be provided throughout the year thanks to a diversity of plant flowering periods.

Plant volatiles mediate Aphis gossypii settling but not predator foraging in intercropped cotton.

The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae) is an important pest of cotton and horticultural crops globally. In China, smallholder farmers regularly intercrop cotton with garlic or onion. Aside from higher farm-level revenue, cotton intercrops are typified by lower Aphis gossypii abundance than monocrops. So far, the mechanistic basis of this lowered pest pressure has not been empirically assessed. Field trials showed that Aphis gossypii abundance is lower and (relative) abundance of aphid predators higher in early-season cotton intercrops than in monocrops. Cage trials and Y-tube olfactometer tests further indicated that garlic and onion volatiles repel Aphis gossypii alates. Electrophysiological bioassays and gas chromatography-mass spectrometry (GC-MS) identified two physiologically active volatiles, that is, diallyl disulfide and propyl disulfide from garlic and onion respectively. Next, behavioral tests confirmed that both sulfur compounds exert a repellent effect on alate Aphis gossypii. Garlic and onion volatiles interfere with Aphis gossypii settling, but do not affect its main (ladybird) predators. Meanwhile, early-season cotton/onion intercrops bear higher numbers of Aphis gossypii predators and fewer aphids. By thus unveiling the ecological underpinnings of aphid biological control in diversified cropping systems, our work advances non-chemical management of a globally-important crop pest. © 2023 Society of Chemical Industry.

Hoverflies provide pollination and biological pest control in greenhouse-grown horticultural crops.

Beneficial insects provide pollination and biological control in natural and man-made settings. Those ecosystem services (ES) are especially important for high-value fruits and vegetables, including those grown under greenhouse conditions. The hoverfly Eupeodes corollae (Diptera: Syrphidae) delivers both ES, given that its larvae prey upon aphid pests and its adults pollinate crops. In this study, we investigated this dual role of E. corollae in three insect-pollinated and aphid-affected horticultural crops i.e., tomato, melon and strawberry within greenhouses in Hebei province (China). Augmentative releases of E. corollae increased fruit set and fruit weight of all three crops, and affected population dynamics of the cotton aphid Aphis gossypii (Hemiptera: Aphididae). On melon and strawberry, E. corollae suppressed A. gossypii populations by 54-99% and 50-70% respectively. In tomato, weekly releases of 240 E. corollae individuals/100 m2led to 95% fruit set. Meanwhile, releases of 160 hoverfly individuals per 100 m2led to 100% fruit set in melon. Also, at hoverfly/aphid release rates of 1:500 in spring and 1:150 in autumn, aphid populations were reduced by more than 95% on melon. Lastly, on strawberry, optimum levels of pollination and aphid biological control were attained at E. corollae release rates of 640 individuals/100 m2. Overall, our work shows how augmentative releases of laboratory-reared hoverflies E. corollae can enhance yields of multiple horticultural crops while securing effective, non-chemical control of resident aphid pests.

Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards

To date, direct interactions between pests and natural enemies are often considered in biocontrol programs. Recently there has been an increase of evidence for the importance of third-party mediated indirect interactions in determining the population dynamics of insects. Predicting the strength of such interactions remains a central challenge in biocontrol assessments. Here, two field experiments were performed in two years to investigate to which extent Dysaphis plantaginea Passerini, Aphis pomi De Geer, and Myzus cerasi Fabricius might indirectly interact through shared natural enemies and ants. We first studied the population dynamics of target insects in isolated orchards of apples and cherries. Secondly, we investigated how the spatial coexistence of aphid-infested cherries can indirectly affect the population dynamics of apple aphids via natural enemies and ants. In the first experiment, nine parasitoid species were recorded on apple and cherry aphids, among them were three species in common. Six predatory families were found on cherry and apple aphids, while only one ant species, Lasius niger L., was found associating with these aphids. In the second experiment, temporal variation in the natural enemy-mediated apparent competition between M. cerasi and apple aphids was found. The cherry aphid is likely to be an important source of natural enemies that attack apple aphids early in the season. Significantly reduced numbers of ants associating with apple aphids in the intercropping habitat were found. Our results emphasize the importance of considering indirect interactions in the designing of pest management strategies.

Differential Susceptibility of Coleomegilla maculata and Scymnus creperus Larvae to Aggression by Solenopsis invicta Workers.

The biological control of aphids by aphidophagous coccinellids is often hampered by aphid-tending ants or aggressive, invasive ants foraging for food. Aggressive species such as the imported fire ant Solenopsis invicta Buren may attack and kill coccinellid larvae. This study tested the hypothesis that wax-secreting Scymnus creperus Mulsant larvae are less susceptible than non-wax-secreting Coleomegilla maculata (DeGeer) larvae to S. invicta aggression. Laboratory experiments were set up using bird cherry-oat aphid Rhopalosiphum padi (L.) nymphs and adults (as prey for coccinellids) on barley leaves in arenas with either coccinellid species and with or without S. invicta workers. The presence of S. invicta reduced aphid predation by C. maculata but not Sc. creperus. The frequency of S. invicta attack was greater for C. maculata than Sc. creperus; mortality was significantly greater for C. maculata than Sc. creperus. The wax covering on Sc. creperus reduced S. invicta aggression. Unexpectedly, Sc. creperus larvae with the wax cover removed did not suffer more S. invicta attacks or increased mortality. In conclusion, the wax cover and, perhaps, the volatile or non-volatile compounds in the wax and on the integument of Sc. creperus larvae reduce S. invicta aggression. Further research could identify the wax compounds and determine their functionality as semiochemicals against S. invicta.

Diversity of endosymbiotic bacteria in the pea aphid (Acyrthosiphon pisum) on alfalfa in Chile

Facultative bacterial endosymbionts are prevalent in aphid pest species and key organisms for the rapid adaptation to changing environment conditions under agricultural management. Facultative endosymbiont interactions allow beneficial phenotypes of insect hosts, providing resistance against natural enemies, fungal infections as well as enhanced resistance to thermal conditions, among others. These interactions have been highlighted as important modulators in the evolution of aphid defenses, being a key aspect for the invasive potential of aphids as pests. In this study, we have examined the bacterial community diversity associated to the pea aphid Acyrthosiphon pisum on alfalfa (Medicago sativa L.) crops in Central Chile by determining the presence and abundance of the seven most common facultative endosymbionts reported for aphid species, including: Hamiltonella defensa, Regiella insecticola, Serratia symbiotica, Spiroplasma sp., Rickettsia sp., Rickettsiella viridis and Fukatsuia symbiotica (or pea aphid X-type symbiont’ PAXS), using a PCR-based approach across species-specific primers, in 16 alfalfa fields during the Chilean spring in the Maule Region. We reported six of the seven endosymbiont species studied, observing a high frequency of infected aphids being the endosymbiont H. defensa, the most predominant among the aphid populations in the different alfalfa fields studied. As H. defensa has been extensively studied in its defensive role to parasitoids, we discuss implications for biological control of this aphid pests. We also discuss the absence of a relevant defensive endosymbiont such as F. symbiotica in the Chilean pea aphid populations and potential implications for the success of the pea aphid biological control program.

Historical andContemporary Perspectives ontheBiological Control ofAphids onWinter Cereals byParasitoids inSouth America.

Aphids are worldwide pests, and in South America, they harm many crops including winter cereals. In the 1970s, the rapid expansion of the wheat crop area in the subtropical region of South America led to growth of aphid populations. The wide availability of food, associated with the low effectiveness of natural biological control, put the aphid populations out of balance, requiring intensive use of insecticides. At the end of the decade, biological control programs of aphids were initiated in Argentina, Brazil, and Chile, including the importation of natural enemies (mainly parasitoids), followed by their laboratory rearing and field release. With decreased use of highly hazardous pesticides, biological control by introduced and already-present parasitoid species was enhanced. The program was very successful and aphid populations have been kept at low levels. This review article explores the history of this program and its current status. In modern day agriculture, with intense multiple cropping systems, adoption of several conservation practices, and increased cultivation of wheat in tropical regions, we discuss ways to keep this program effective to maintain aphid populations on cereal crops at low acceptable levels through employing biological control agents.

Functional analysis of odorant-binding proteins for the parasitic host location to implicate convergent evolution between the grain aphid and its parasitoid Aphidius gifuensis

(E)-β-farnesene (EBF) is a typical and ecologically important infochemical in tri-trophic level interactions among plant-aphid-natural enemies. However, the molecular mechanisms by which parasitoids recognize and utilize EBF are unclear. In this study, we functionally characterized 8 AgifOBPs in Aphidifus gifuensis, one dominant endo-parasitoid of wheat aphid as well as peach aphid in China. Among which, AgifOBP6 was the only OBP upregulated by various doses of EBF, and it showed a strong binding affinity to EBF in vitro. The lack of homology between AgifOBP6 and EBF-binding proteins from aphids or from other aphid natural enemies supported that this was a convergent evolution among insects from different orders driven by EBF. Molecular docking of AgifOBP6 with EBF revealed key interacting residues and hydrophobic forces as the main forces. AgifOBP6 is widely expressed among various antennal sensilla. Furthermore, two bioassays indicated that trace EBF may promote the biological control efficiency of A. gifuensis, especially on winged aphids. In summary, this study reveals an OBP (AgifOBP6) that may play a leading role in aphid alarm pheromone detection by parasitoids and offers a new perspective on aphid biological control by using EBF. These results will improve our understanding of tri-trophic level interactions among plant-aphid-natural enemies.

Licorice strips enhance predator-mediated biological control in China's cotton crop.

Habitat management such as field- or farm-level diversification can conserve arthropod natural enemies, enhance biological pest control and lower (or suspend) insecticide use in agricultural crops. These approaches however have been underexploited to manage the aphid Aphis gossypii in cotton cropping systems of Xinjiang, China. In this study, we investigated whether the presence of licorice (Glycyrrhiza uralensis) at the field edge benefits generalist predator abundance and aphid biological control in local cotton crops. Field trials during 2020 and 2021 showed that licorice strips enhanced the in-field abundance of generalist predators (primarily ladybeetles) 2.2-4.3 fold during early season, i.e. initial growth before A. gossypii peak infestation pressure. During peak outbreak conditions in July, treatment fields with licorice strips experienced a respective 17.5-61.2% lowered aphid density and 12.3-14.6-fold higher predator-to-aphid abundance ratio (PAR) than control fields. In late season (aphid decline phase) of either year, cotton fields with licorice strips also attained a respective 4.7-9.9 fold higher PAR. Exclusion cage assays quantitatively assessed predator-mediated A. gossypii biological control and the relative contribution of licorice strips. The biocontrol services index (BSI) was 2.8 times (2020) and 1.4 times (2021) higher at 5m distances from the licorice strip as compared to control fields. Licorice strips in the immediate vicinity of cotton fields benefit generalist arthropod predators and improve aphid biological control throughout the cotton cropping season. These findings help to integrate habitat management within integrated pest management (IPM) frameworks in the biggest cotton production region of China. © 2022 Society of Chemical Industry.

Thermal development of the endoparasitoid Aphelinus maculatus Yasnosh (Hymenoptera: Aphelinidae) parasitizing Myzus persicae Sulzer (Homoptera: Aphididae).

The aphid parasitoid, Aphelinus maculatus Yasnosh, was first documented in China in 2016. It is important to make clear of the effects of temperatures on the development of this aphid parasitoid for the future using as a aphid biological control agent. So the thermal requirements, lower developmental threshold (t), thermal constant (K), upper developmental threshold (Tm) and optimum developmental temperature (To) for the egg-mummy, mummy-adult and egg-adult periods of A. maculatus were established under the laboratory conditions. The studies were conducted at five constant temperatures (13, 18, 23, 28, and 33°C) and with a 16L: 8D photoperiod. Lower developmental threshold (t) and thermal constant (K) were estimated by fitting linear model. Upper developmental threshold (Tm) and optimal developmental temperature (To) were estimated by fitting Logan I non-linear model. The results turned out that the lower (t) and the upper developmental thresholds (Tm) for egg-adult period were 5.59°C and 28.17°C, respectively. The thermal constants (K) for egg-mummy, mummy-adult, and egg-adult periods were estimated at 121.51, 127.88, and 243.90 degree-days, respectively. The optimal developmental temperature (To) for egg-adult period was 27.45°C calculated by the model, but the survival rate was only 40.68% at the temperature of 28°C. The highest survival rate was 74.32% at temperature of 23°C, implying that A. maculatus preferentially developed at the temperate regions of temperature.