Intro
The wheat aphids biological control program in Brazil was designed by the National Center of Wheat Research, unit of Brazilian Agricultural Research Corporation (Embrapa), targeting aphid species whose population levels and damage to culture have become alarming in the 1970s. The program started in 1978 with the support of FAO and the University of California - Berkeley, USA and collaboration of many others national and international institutions. At the time, the control of wheat aphids was done without the integrated management criteria, through the intensive use of chemical insecticides with negative consequences to the environment and human health.
Objective of the practice
The program followed the protocol described by Van den Bosch & Messenger (1973), with introduction, mass rearing and release of natural enemies (classic method of biological control). The hypothesis was that the imbalance of aphids in wheat crop could be at least partially reversed by the biological control, presuming that the introduction of several species would allow the adaptation of some of these species to ecological conditions at southern Brazil. Then they would establish themselves and multiply freely in the wheat aphids, helping to control the populations of pests. The targets of the program were M. dirhodum and S. avenae, species of major economic importance at that time. The stated objective was to achieve levels of parasitism to contribute 10-15% of aphid mortality).
Partners
The entire wheat production chain has benefited. In an environment of high populations of aphids, even the intense use of insecticides does not prevent infection by transmitted viruses. Consequently, there is a reduction of the productive level which can lead to economically unviable productivities. Even today, with balanced populations it is estimated that without the application of insecticide there is a residual damage of 20%. Another notable effect was on the environment and human health. For example, producers in the 1970s report fish mortality in rivers as common facts.
Implementation of the Project/Activity
After the visit of consultants / experts from research centers in various parts of the world, the collection and introduction of natural enemies in the wheat growing of Brazil was planned. At least fourteen species of micro-parasitic Hymenoptera of wheat aphids originating mainly from countries of Europe and the Middle East were introduced. After the introduction and the quarantine process, the species of parasitoids were created in large scale in the laboratories of Embrapa Wheat and released in crops, mainly wheat. Initially the releases were systematic and numerous, conducted by Embrapa's own staff, directed to all the wheat producing regions of Rio Grande do Sul. 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 evaluate the establishment of species and parasitism in wheat aphids. At the same time, studies on biology, population dynamics and aphid damage and on the selectivity of insecticides were carried out in order to develop complementary knowledge and technologies of pest management that would help to preserve biological control agents and reverse the imbalance. From 1982 to 1992, with several species already established, the releases continued less intense, made directly by the Embrapa parasitoid producers, in order to consolidate the technology and maintain the motivation for the rational use of insecticides. During the period 1978-92 about 20 million parasitoids were produced and released.
Results/Outputs/Impacts
Some introduced species of parasitoids established and parasitism of aphids in wheat crop exceeded the program target. The species Aphidius rhopalosiphi, Aphidius uzbekistanicus and Praon volucre were considered established and Aphidius ervi, Ephedrus plagiator and Praon gallicum were consistently recovered. The established parasitoids developed adaptive mechanisms that allowed them to survive and successfully parasitize cereal aphids species, going to act in the survival of local and aphid multiplication in wheat dry season in spontaneous grasses and other crops. After the introductions, the parasitism of S. avenae and M. dirhodum, the participation of various parasitoid species and instars spectrum of parasitized hosts were gradually increasing. In the evaluated sites (Espumoso, RS, for example), parasitism in S. avenae reached 61.9%, 46.4% and 55.6% in 1980 and 63.6%, 44.4% and 30.0 % in 1981, in wingless individuals of 4th instar, wingless adults and winged adults, respectively; in M. dirhodum in 1980, the parasitism rate was 64.3%, 16.7% and 25.0%, for these same morphological types. High and increasing parasitism levels continued to be registered, while the hiperparasitism proved to be small and not significantly impaired the action of parasitoids. Another significant result, related to the quality of parasitism, was the evolution regarding the timing in parasitoid-host relationship, with parasitism manifesting early, within the first weed aphids in autumn and winter. Population levels of aphids S. avenae and M. dirhodum and the damage they cause, extremely high in the 1970s, were reduced drastically after the biological control program for wheat aphids. In 1979-81, the maximum density found ranged from 6.4 to 15.0 aphids/tiller (S. avenae) and 4.7 to 9.0 aphids/tiller (M. dirhodum); the parasitism in 1980 and 81 were enough to keep the density of these species well below the thresholds of economic damages. Even under favorable environmental conditions and lack of other natural enemies (predators and pathogens), no more aphids outbreaks occurred in the years following the introductions. Similarly, in contrast to what happened before, there was not the same response to insect control, in terms of grain yield of wheat crop in subsequent years, due to low population levels that began to occur in crops. Although not a direct measure of biological control and other causes may be involved, the use of chemical insecticides for aphid control in wheat decreased gradually. In 1981, in Rio Grande do Sul, this practice was carried out in less than 5% of the area cultivated with wheat, providing a reduction of approximately 855,000 liters/year in the volume of insecticides applied in a period where consumption of pesticides in Brazilian crops grew significantly. In addition, the biological control of aphids was naturally extended to barley crops, oats and triticale.
Enabling factors and constraints
The conditions that allowed the successful introduction of biological control of aphids in Brazil were: 1) extensive international cooperation; 2) the creation by the Brazilian government of a research company with a qualified technical staff and physical structure necessary to carry out the activities; 3) available and flexible financial resources to be used in the implementation of the program; 4) agility in the quarantine process and introduction of the species.
Sustainability and replicability
Starý et al (1993) state that the successful establishment and continuity of good efficiency levels in the control of aphids in wheat are favored by diverse array of cultures and habitats commonly associated with the production of wheat in the different regions where this cereal is cultivated in South America. According to these authors, such cultures and habitats serve as a natural refuge and also as a source of aphids as alternative hosts to the parasitoids. The adaptation of introduced parasitoid species to Brazilian conditions can be confirmed by recent results obtained in surveys conducted in 2002 (Medianeira), 2008 and 2009 (Ibiporã, Londrina and Rolândia) in northern state of Paraná and in 2006 (Augusto Pestana) in the northwest of Rio Grande do Sul. In these works were found the species A. colemani, A. uzbekistanicus, A. ervi, A. rhopalosiphi, D. rapae and L. testa-ceipes parasitizing aphids R. padi, S. avenae and M. dirhodum (Alves et al 2005, Zanini et al 2006, Bortolotto et al 2012, Machado & Santos 2013). The structuring of the agro-ecosystem to benefit the conservative biological control is an approach that requires knowledge and the possible trans-formation of the agricultural landscape. But, probably, it is the most apropriate pest control strategy regarding environmental conservation and also, in the long term, more stable and less expensive (Boivin et al 2012). Different studies on this subject show that the complexity of environments does not influence the diversity or abundance of aphid parasitoids in winter cereals, indicating that these insects can get the resources for their survival even in less complex environments (e.g. areas with high percent-age of agricultural use). However, parasitism levels tend to decrease with the increase in distance from the crop edges, showing a strong dependence of these parasitoids to resources associated with the diversity of vegetation in the farm level (Tscharntke et al 2005, Brewer et al 2008, Hol-land et al 2008, Vollhardt et al 2008, Caballero López et al 2012) and demonstrating, in this way, the importance and benefits of maintaining conservation areas, however small. The importance of these areas of greatest diversity in the agricultural landscape is related to the provision of alternative hosts for the maintenance of parasitoids, especially in periods when the wheat is not in the field. Starý et al (2007), in a survey con-ducted to verify parasitoid association with biological control in Brazil, confirmed this fact in reporting the occurrence of A. colemani, A. ervi, D. rapae, P. gallicum and P. volucre parasitizing different aphid species that are not associated with winter cereals and, in this way, responsible for the maintenance of these parasitoid populations, for example, in the summer periods. Although relatively simple, the different techniques that can be used to help the conservative biological control need to be assessed under the conditions of Brazilian agro-ecosystems for further adoption by producers.
Conclusions
After the introduction of parasitoids to control aphid wheat pests in Brazil there was a significant quantitative and qualitative change in population patterns of the different aphid species, showing that more than forty-five years later, the biological control project continues to bring positive results. The absurdly large population levels of aphids causing significant direct damage to wheat have not been repeated and parasitism remains active. Aphid species that previously had major pest status, as M. dirhodum and S. avenae, today are detected sporadically and only occasionally reach population levels that need chemical control, fact considered normal within the biological control process that is dynamic and is based in natural balance between involved species. Nowadays there is a closer balance between aphid populations and their natural enemies, es-pecially parasitoids. According to Joshi et al (2010), the biological offers numerous advantages, especially when compared with chemical control. This method is non-polluting, non-toxic and is self-perpetuating. Although the initial cost may be high, subsequent expenses do not occur and the results are usually permanent.
Other sources of information
• Revista Brasileira de Entomologia
• Print version ISSN 0085-5626On-line version ISSN 1806-9665
• Rev. Bras. entomol. vol.51 no.1 São Paulo Jan./Mar. 2007
•
http://dx.doi.org/10.1590/S0085-56262007000100018
• BIOLOGICAL CONTROL AND PLANT PROTECTION
• Aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their associations related to biological control in Brazil
• Natural biological control of aphids (Hemiptera: Aphididae) in a wheat field by parasitoids (Hymenoptera, Aphidiinae) in Medianeira, PR, Brazil
• Luis Francisco Angeli Alves, Tânia M.V. Prestes, Agostinho Zanini, Maria F. Dalmolin, Ayres de O. Menezes Junior
•
http://dx.doi.org/10.5433/1679-0359.2005v26n2p155
• J Insect Sci. 2015; 15(1): 40.
• Published online 2015 Apr 5. doi: 10.1093/jisesa/iev027
• PMCID: PMC4535473
• PMID: 25843593
• Aphidophagous Parasitoids can Forage Wheat Crops Before Aphid Infestation, Parana State, Brazil
