Biological control of wheat aphids: a historical contribution

Controlling a pest by biological means requires knowing its role in trophic networks and using and manipulating the organisms that make up this network in order to reduce its population.

The population growth of living beings is determined by the biotic potential, maximum reproduction under favorable conditions, and by the resistance of the environment resulting from physical and biological factors that act to reduce population growth. In agricultural systems, the population density of pests is regulated on the one hand by the availability of food and, on the other, by the action of natural enemies (Figure 1). Abiotic factors, such as meteorological conditions, act on these components of the trophic webs and their interactions define the rate of the processes involved in the biological cycles.

Phytophagous insects introduced into a new region can benefit from the abundance of food sources and the absence of efficient natural enemies. From 1965 to 1979, the area cultivated with wheat increased from 354.680 to 4.104.144 hectares in Brazil. This rapid expansion of the wheat cultivation area in the subtropical region of South America, associated with the low effectiveness of natural biological control, led to a population surge of introduced aphids, generating imbalance in the agroecosystem and requiring the intensive use of insecticides (Figure 2).

Aphids on cereals and their damage

Cereal aphids from the Palearctic region (Europe, North Africa, much of Arabia and Asia north of the Himalayas) have been introduced into the Neotropics (Central America, the Caribbean islands and South America). The first species established in South America was the green cereal aphid, Schizaphis graminum, recorded in 1914 in Argentina and, later, in Brazil, Chile, Colombia, Paraguay, Peru, Uruguay and Venezuela. Another species with reports between 1930 and 1970 was the corn aphid, Rhopalosiphum maidis, with observations in Argentina, Brazil, Colombia, Uruguay and Venezuela, but being uncommon in wheat.

Since the 1960s, the corn aphid, Sitobion avenae, the leaf aphid, Metopolophium dirhodum, and the oat aphid, Rhopalosiphum padi, were reported for the first time in the region (Figure 2). S. avenae e M. dirhodum became the two most important species in South American wheat crops. Between 1970 and 1980, population densities reached more than 100 individuals of S. avenae per ear and around 200 individuals of M. dirhodum per plant. Considering all aphid species, levels close to 250-300 aphids per plant were reached. Consequently, damage to wheat production became frequent. In plots without aphid control, grain yield damages exceeding 50% were often recorded. Overall, in the period 1967-1972, it was estimated that damage caused by aphids in wheat production in southern Brazil was above 20%.

Chemical control has become a common practice to prevent losses. In Brazil, in 1977, 98,6% of wheat crops in the states of Rio Grande do Sul and Paraná were sprayed once or twice, and in many cases, three to four sprays were necessary to control aphids. The use of chemical insecticides also occurred in other countries in the region. In Argentina, before 1979, aphids M. dirhodum, S. graminum e S. avenae could only be controlled by insecticides. This intensive use of insecticides affected the few endemic natural enemies, creating a vicious cycle that made wheat production totally dependent on this practice.

natural enemies

The population growth of aphids is affected by the action of parasitoids, predators and entomopathogenic microorganisms. Parasitoids are microhymenoptera, small wasps, mostly belonging to the families Braconidae (subfamily Aphidiinae) and Aphelinidae. The female lays an egg inside the aphid, where the larval development of the parasitoid occurs, which kills its host shortly before pupation, forming a “mummy” that protects the parasitoid until the adult emerges. The main predators of aphids are coccinellids (Coleoptera, Coccinellidae), lacewings (Neuroptera: Chrysopidae) and syrphids (Diptera: Syrphidae). These insects consume several aphids during their development, some of them during their larval phase and others also in the adult phase.

Before the reports of M. dirhodum e S. avenae In Brazil, records of natural enemies of wheat aphids were restricted to S. graminum. Since the leaf aphid and the corn aphid developed large populations, their biological control was considered inefficient. In the south-central region of Paraná, in the 1970s, high populations of these species and a very low level of parasitism were reported. There was also a significant, albeit late, incidence of the entomopathogen entomophthora sp. and the abundant presence of aphid-predatory syrphids before the population peak. However, this did not prevent the damage caused by aphids to grain productivity.

The aphid parasitoid fauna in Latin America is characterized by the prevalence of Aphidius platensis, Diaeretiella rapae e Lysiphlebus testaceipes. These were the only parasitoids reported in Brazil and Chile before the introduction of other species by biological control programs. A. platensis e D. rapae are of Palearctic origin and were probably accidentally introduced into South America along with their aphid hosts. L. testaceipes, of Nearctic origin, may have been accidentally introduced or migrated naturally from North America to South America. In Argentina, aphid parasitoid species Aphelinus asychis, A. abdominalis e Praon volucre were also reported on wheat aphids and may have been accidentally introduced into that country along with their aphid hosts.

Biological control program

The biological control program for aphids in winter cereals in South America, mainly through the importation and introduction of aphid parasitoids, can be considered one of the most successful biological control cases in the world. Aphid control programs for winter cereals have been launched in Argentina, Brazil and Chile.

These programs followed the scheme described by Van den Bosch and Messenger (1973), with the introduction, mass rearing and release of natural enemies, characterizing the so-called classical method of biological control. The hypothesis was that the population imbalance of aphids in wheat could be at least partially reversed by natural enemies that coevolved with these insects. The introduction of natural enemies would allow some to adapt to the ecological conditions of the humid subtropical region of South America, establishing themselves and multiplying in wheat aphids, helping to control the populations of these pests.

Introduction of parasitoids

Specific biological control programs for wheat aphids introduced six species of aphid parasitoids into Argentina, eight into Chile and 12 into Brazil (Table 1). These parasitoids originated from the USA and countries in Europe and the Middle East.

In Brazil, the program was conducted by Embrapa Trigo (National Wheat Research Center) with support from FAO and the University of California. Parasitoids were the key insects in this program, constituting the logo of the biological control program in Brazil (Figure 2). After the introduction and quarantine process, large-scale rearing of parasitoids was carried out in the insectary of Embrapa Trigo. This facility, built in 1978, was named after Robert Van den Bosch, in honor of his contribution to the program and pioneering work in the biological control of insect pests in general.

The releases of parasitoids in wheat crops, carried out by the Embrapa team in Brazil in all wheat-growing regions of Rio Grande do Sul, were systematic and frequent. Sporadic releases were also carried out in the states of Santa Catarina, Paraná and Mato Grosso do Sul. After the releases, the sites were monitored to assess the establishment of the species and the levels of parasitism in wheat aphids.

From 1982 to 1992, with some species already established, releases continued at a lower intensity and were carried out directly by farmers using parasitoids supplied by Embrapa. The objective was to consolidate the technology and maintain motivation for the rational use of insecticides. During the period 1978-1992, approximately 20 million parasitoids were produced and released.

Program results

In Brazil, in the early 1980s, A. rhopalosiphi, A. uzbekistanicus e P. volume were considered established and subsequently, A. Ervi. Established parasitoids have developed adaptive mechanisms to successfully survive and parasitize grass aphid species, maintaining themselves during the wheat off-season on wild grasses and other crops. Following introductions, parasitism in S. avenae e M. dirhodum gradually increased. In different locations evaluated, parasitism in S. avenae ranged from 46 to 62% in 1980 and from 30 to 64% in 1981.

High and increasing parasitism levels continued to be recorded, while hyperparasitism was low and did not significantly affect parasitoid action. Another significant result was the synchrony in the parasitoid-host relationship, with parasitism starting early in the first aphids in autumn and winter. Population levels and damage of S. avenae e M. dirhodum were drastically reduced. In 1979-1981, the maximum aphid density/tiller ranged from 6,4 to 15,0 for S. avenae and from 4,7 to 9,0 for M. dirhodum. Parasitism in 1980 and 1981 kept the density of these species below the economic level.

No major aphid outbreaks occurred in the years following the introduction of parasitoids in Brazil. The use of insecticides fell dramatically. Furthermore, biological control was naturally extended to other winter cereals, such as barley, oats and triticale.

Current parasitoid guild and parasitism levels

Of the 12 exotic species of parasitoids introduced, three (A. uzbekistanicus, A. rhopalosiphi e A. Ervi) are still present in southern Brazil. A. colemani e L. testaceipes already occurred in the region; therefore, it is not possible to know whether the current population is composed of descendants of preexisting populations, introduced populations or a mixture of both. In the case of A. colemani, specimens collected during the biological control program (1978 to 1982), previously identified as Aphidius colemani, are in fact A. platensis.

Currently, in the guild of aphid parasitoids of winter cereals, the dominant species has been A. platensis. In a recent eight-year time series (2011–2018) in Coxilha (RS) were found A. platensis (61,4%), A. uzbekistanicus (7,3%), A. Ervi (1,6%), A. rhopalosiphi (6,8%), D. rapae (18,6%) and L. testaceipes (1,3%).

The population dynamics of parasitoids have been seasonal with a peak in winter and another in the winter-spring transition. For example, A. platensis e D. rapae peak in mid-winter, while A. uzbekistanicus e A. rhopalosiphi peak in late winter and early spring. High levels of parasitism in early winter may explain the drastic reduction in aphid populations in spring. Recent surveys during the wheat harvest indicated that in the early stages of the crop (vegetative period) levels of parasitism between 60 and 85% occurred.

From their center of distribution in the subtropical region, the parasitoids have spread to tropical regions, becoming important not only in the biological control of cereal aphids, but also in other agricultural crops.

Perspectives on biological control of winter cereal aphids

With the expansion of winter cereals into the tropical region (Brazilian Cerrado), it is important to assess the contribution of established parasitoids to the balance of agricultural systems. Some parasitoid species are established in the tropical region, but higher temperatures in the tropics may limit the ecological services of parasitoids.

With the confirmation of the establishment of these parasitoids in South American conditions, it is essential to develop, evaluate and encourage the adoption of management practices to conserve and increase the populations of natural enemies. Structuring the agroecosystem for the benefit of conservationist biological control is an approach that requires knowledge and transformation of the agricultural landscape. Conservation biocontrol acts in the long term and is more stable and less expensive than chemical control.

After the introduction of parasitoids to control wheat aphids in South America, there was a significant quantitative and qualitative change in the population patterns of the different aphid species, showing that more than 40 years later, this biological control project continues to bring positive results. Considering that the management of insect pests adopted by wheat producers is mainly based on chemical control, the use of control practices that reduce the negative effect of insecticides on the population of natural enemies becomes mandatory. The adoption of insect pest monitoring procedures that support insect control decisions based on action thresholds should be encouraged. These practices associated with the use of selective insecticides can favor the current situation for the biological control of aphids pests of winter cereals.

By Douglas Lau (Embrapa Wheat); Marcus Vinicius Sampaio (UFU); José Roberto Salvadori (Embrapa Wheat); Paulo Roberto Valle da Silva Pereira (Embrapa Forests); Carlos Diego Ribeiro dos Santos (UFRGS); Eduardo Engel (Esalq); Antonio Ricardo Panizzi e Alberto Luiz Marsaro Júnior (Embrapa Wheat)

Article published in issue 289 of Cultivar Grandes Culturas Magazine