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Revista mexicana de ciencias agrícolas

Print version ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.8 n.4 Texcoco Jun./Jul. 2017 


Natural enemies associated with woolly aphid in apple orchards with different pest management

María Fátima Ordoñez Beltrán1 

Juan Luis Jacobo Cuéllar1  § 

Ernesto Quintana López2 

Rafael Ángel Parra Quezada1 

Víctor Manuel Guerrero Prieto1 

Claudio Ríos Velasco3 

1Facultad de Ciencias Agrotecnológicas, Extensión Cuauhtémoc-Universidad Autónoma de Chihuahua. Av. Presa de la Amistad núm. 201. Cuauhtémoc, Chihuahua, México. CP. 31510. Tel. (01) 625 5826825. (;;

2Grupo de Especialidades y Desarrollo Agronómico, S. A. de C. V. Carretera Cuauhtémoc-Álvaro Obregón, km 3.5, núm. 2015. Cuauhtémoc, Chihuahua, México. CP. 31604. (

3Centro de Investigación en Alimentación y Desarrollo, A. C. Unidad Cuauhtémoc, Chihuahua. Av. Río Conchos S/N Parque Industrial. Cuauhtémoc, Chihuahua, México. CP. 31570. (


The woolly aphid (Eriosoma lanigerum Hausmann) is a phytophagous disease affecting apple orchards [Malus sylvestris (L.) Mill. var domestica (Borkh) Mansf.] established in Chihuahua state. In order to fight them it has been privileged the use of conventional insecticides, incurring in extemporaneous applications that possibly have repercussions in the low occurrence of natural enemies. Based on the above and the reduced information on natural enemies of woolly aphid in México, during the years 2011 and 2012 the present research was carried out with the purpose of identifying the incidence of predators and parasitoids associated with colonies of woolly aphid in apple orchards with different pest management. By orchard management, 38 and 35 individuals were detected in orchards without management and with integrated pest management, values that were statistically equal to each other and different from the 12 individuals detected in the orchard with conventional management. The species of predators associated with colonies of woolly aphid in Chihuahua were: Hippodamia convergens, Chrysopa nigricornis, Chrysopa oculata, Chrysoperla rufilabris, Chrysoperla comanche, Chrysopa spp., Allograpta obliqua, Sirphus sp. and Toxomerus sp., whereas as parasitoids only Aphelinus mali was detected.

Keywords: Malus sylvestris var domestica; Eriosoma lanigerum; predators; parasitoids


El pulgón lanígero (Eriosoma lanigerum Hausmann) es un fitófago que incide en huertos de manzano [Malus sylvestris (L.) Mill. var domestica (Borkh) Mansf.] establecidos en el estado de Chihuahua. Para su combate se ha privilegiado el uso de insecticidas convencionales, incurriendo en aplicaciones extemporáneas que posiblemente repercuten en la baja ocurrencia de enemigos naturales. Con base en lo anterior y la reducida información sobre enemigos naturales del pulgón lanígero del manzano en México, durante los años 2011 y 2012 se realizó el presente trabajo con la finalidad de identificar la incidencia de depredadores y parasitoides asociados a colonias de pulgón lanígero en huertos de manzano con diferente manejo de plagas. Por manejo del huerto, se detectaron 38 y 35 ejemplares para los huertos sin manejo y con manejo integrado de plagas, valores que fueron estadísticamente iguales entre sí y diferentes a los 12 ejemplares detectados en el huerto con manejo convencional. Las especies de depredadores asociadas a colonias de pulgón lanígero en Chihuahua fueron: Hippodamia convergens, Chrysopa nigricornis, Chrysopa oculata, Chrysoperla rufilabris, Chrysoperla comanche, Chrysopa spp., Allograpta obliqua, Sirphus sp. y Toxomerus sp., mientras que como parasitoides se detectó solo a Aphelinus mali.

Palabras clave: Malus sylvestris var domestica; Eriosoma lanigerum; depredadores; parasitoides


Within the phytophagous complex affecting apple, the woolly aphid has increased during the last years, possibly due to the increase of maximum temperatures, low precipitation (Ramírez et al., 2011) and the reduction of natural biological control agents (Gontijo et al., 2012) that are often decimated by the use of insecticides (Penman and Chapman, 1980). The insect when feeding causes hypertrophy and tissue rupture in roots and shoots of apple trees (Brown et al., 1991), which can reduce sap flow and favor the entry of phytopathogenic fungi (Weber and Brown, 1988). High and recurrent populations of the phytophagous can reduce vigor, tree productivity and fruit quality by occupying spaces within the stylus canal and seed loci (Brown et al., 1995).

In relation to the natural enemies of woolly aphid, coccinellidae species have been recorded: Adalia bipunctata (L.), Coccinella septempunctata L., Coccinella transversoguttata Brown, Harmonia axydiris Pallas, Hippodamia convergens Guérin-Méneville, Hippodamia tredecempunctata (L.); Syphids: Heringia calcarata (Loew), Syrphus opinatur Osten Sacken, Eupeodes fumipennis Thomson, E. americanus Wiedeman, Syritta pipiens (L.), Eumerus stigatus (Fallen), Melangyna umbellatarum (F.); Chrysopods: Chrysopa nigricornis Burmeister, Chrysoperla plorabunda (Fitch), Hemerobius spp.; dermapterae: Forficula auricularia L. and the parasitoid Aphelinus mali (Haldeman) (Asante, 1997; Mols and Boers, 1999; Nicholas et al., 2005; Mansilla and Pérez, 2006; Berg and Short, 2008; Beers et al., 2010, Moerkens et al., 2012; Gontijo et al., 2012; Dicu et al., 2013; Gontijo et al., 2015), with syphids showing the highest relative frequency 62.7%, followed by lacewings 23.6%, Coccinellids 8.9% and other predators including bedbugs, spiders and earwigs with 4.8% (Gontijo et al., 2015).

With regard to A. mali parasitoids, up to 90% of parasitism have been reported, especially in years with an early occurrence, or with the occurrence of better adapted biotypes to different temperature and precipitation conditions (Suckling et al., 1999). Wearing et al. (2010) studied the relationship between E. lanigerum fluctuation and its A. mali parasite in the transition from a conventional phytophagous combat program using broad spectrum insecticides and an integrated program based on selective insecticides. The incidence of woolly aphid remained very low in the site with conventional management due to the use of insecticides, while in the site in transition to the integrated management program there was an increase of the phytophagous and a low colonization by its natural enemies that took close to four years in reducing the population to acceptable levels.

The main natural enemy that achieved this was the A. mali parasitoid, along with predators such as the coffee willow Micromus tasmaniae (Walker) and the Forficula auricularia L. earwig. The concurrence of F. auricularia and A. mali in the reduction of woolly aphid was reported by Lordan et al. (2015). Based on the above, and considering the reduced information on natural enemies of apple aphid in México, this paper was based on the hypothesis: “conventional management of phytophagous species restricts the relative abundance and richness of natural enemies species associated with colonies of woolly aphid that affect apple orchards of Chihuahua state”; and the objective was to identify the incidence of predators and parasitoids associated with colonies of woolly aphids in apple orchards with different pest management.

Materials and methods

Location of the study

The research was carried out in Cuauhtémoc, Chihuahua, México, in apple orchards located between 28º 25՚ 58” and 28º 28՚ 19” north latitude and 106º 54՚ 25” and 106º 54’ 37” west longitude, with an average height of 2 042 masl; with maximum distance between orchards of 5 900 m.

Characteristics of apple orchards under study

Three orchards with the Golden Delicious cultivar on Franco rootstock were selected, which is susceptible to woolly aphid and were designated as: 1) orchard without pest management (with irrigation, without anti-hail mesh, with restriction of economic resources and without technical advice: SM); and 2) orchard with integrated pest management (with anti-hail mesh, irrigation, without economic resource constraints, with technical assistance, with use of sex pheromone to interrupt mating of the apple moth and combating phytophagous with low environmental impact insecticides and conventional ones: MIF) and 3) orchard with conventional pest management (with anti-hail mesh, irrigation, without economic resource constraints, with technical advice and application of conventional insecticides: MC). In each of the orchards five trees with similar vigor were marked, determined by the trunk cross-sectional area, as close as possible to each other and in the inner part of the orchard.

Determination of woolly aphid abundance

The number of woolly aphid colonies in the tree crown was counted with detailed visual inspections, checking around each tree, orchard, and year, once per week during April to September in the 2010 and 2011 years.

Species determination and abundance of natural enemies

During April to September of 2010 and 2011, weekly inspections were carried out for the collection of beneficial insects that affected the colonies of woolly aphid established in apple trees in each of the designated orchards. For immature stage predators the collection was done with dissecting forceps and with a striking net in the case of adults. The specimens captured by each review date and type orchard were placed in 30 ml containers with 70% ethyl alcohol for storage and transferred to the Entomology Laboratory of the Autonomous University of Chihuahua, Cuauhtémoc Unit. The identification of coccinélidos was made based on the keys of Gordon (1985); for genera and species of Chrysopidae the papers of Ramírez (2007); Valencia et al. (2006) were used and for Syrphidae the keys of Marinoni et al. (2007) were used.

In order to collect parasitoids, twigs with parasitized aphids were taken and placed in plastic containers with a capacity of 500 mL with a mesh cap to allow air flow, a cotton pad was placed in the container with distilled water to provide moisture and avoid dehydration of the phytophagus and possible parasitoid. The containers were transferred to the laboratory and placed with natural light and temperature from 18 to 25 oC where they were checked daily, the emerged parasitoids were collected and deposited in glass containers of 30 mL capacity with 70% alcohol for preservation. The identification of specimens was done with the keys of Gibson (1997); Graham (1976); Grissell and Schauff (1997); Noyes (2011); Prinsloo and Nester (1994); Woolley (1997).

The number of natural enemies per family, species, year and orchard management was recorded. In the family and species categories, the number of specimens represented the absolute frequency, then the relative frequency was obtained, product of the absolute frequency divided by the total number of detected specimens. The abundance (number of specimens) and richness (number of species) was obtained per year and phytophagous management, using the Sorensen coefficient of similarity, calculated with the equation Qs= 2s/(n1 + n2), where qs is the proportion of similarity, s is the number of shared species, n1 is the number of species of site 1 and n2 the number of species of site 2 (Magurran, 1988), to determine the similarity degree by common species among orchards with different pest management.

Statistical analysis

Mann-Whitney non-parametric test with 95% confidence was used to compare the number of airborne aphid colonies per year and management (Sprent and Smeeton, 2001). The statistical analyzes were performed using SAS (2003); while the incidence of natural enemies by family, species, abundance and richness per year and management was analyzed with the non-parametric test of X2 with a classification criterion divided into categories, with 95% confidence and with correction of Yates when it was necessary according to Sprent and Smeeton (2001).


Abundance of woolly aphid

The occurrence of aerial colonies of woolly aphid in apple trees per year was statistically different under the Mann-Whitney median comparison test with 95% confidence. During 2010, the median value of aerial colonies of woolly aphid was 1, while in 2011, the value was 52 (Table 1). The comparison of the median value of the number of colonies per orchard management was also statistically different with 95% confidence. The trees in the orchard with conventional management showed the lowest value with one colony of woolly aphid per tree. In trees with integrated pest management, the median number of colonies was 77 for 2010 and 52 for 2011, while for trees with no management, the highest variation was recorded with 1 colony per tree in 2010 and 254 colonies for 2011 (Table 1).

Table 1 Median number of aerial colonies of woolly aphid per year and orchard management. Cuauhtémoc, Chihuahua. 

SM= sin manejo; MIP= manejo integrado de plagas; MC= manejo convencional. Valores con misma letra en hileras y columnas significa igualdad estadística entre ellos con 95% de confianza y bajo la prueba no paramétrica de Mann-Whitney.

Abundance of natural enemies and species composition

During 2011, abundance (number of specimens of natural enemies) was 70, a value that was statistically different from 15 specimens detected in 2010. Values for richness (number of species) were four and 10 for the years 2010 and 2011 respectively, with no significant differences between them. In relation to the Sorensen coefficient, a similarity coefficient of 0.53 was obtained with the comparison between years, whereas with the comparison between orchard management, the greatest coincidence of natural enemies detected was for orchards without management and integrated management with value of 0.8.

Regarding the occurrence of natural enemies per orchard management, there was greater abundance and richness in the unmanaged orchard with values of 38 specimens and eight species respectively. In the orchard with integrated phytophagous management, there were intermediate registered values with 35 specimens and seven species, while in the orchard with conventional management the lowest values were detected with 12 specimens and four species for abundance and richness, respectively. The values for number of individuals (abundance) were statistically the same for orchards with no management and with integrated phytophagous management, while these were statistically different for abundance in the orchard with conventional management (Table 2).

Table 2 Abundance of woolly aphid in apple orchards with different pest management in Cuauhtémoc, Chihuahua, during 2010 and 2011. 

Valores en columna total por familia y en hilera total por manejo con misma letra, son estadísticamente iguales entre sí bajo la prueba no paramétrica de X2 con un criterio de clasificación dividido en categorías con corrección de Yates cuando se consideró necesario y con 95% de confianza.

The natural enemies associated with woolly aphid (Eriosoma lanigerum) colonies in apple trees in Chihuahua belonged to the Chrysopidae families with 27 specimens (Chrysopa nigricornis Burmeister, with 11 specimens as most frequent), Aphelinidae with 23 specimens (Aphelinus mali as a single species), Coccinellidae with 19 specimens (Hippodamia convergens Guerin-Meneville as a single species) and Syrphidae with 23 specimens (with Allograpta obliqua with 11 specimens as most frequent), with statistical equality for the number of specimens per family (Table 2). In species richness, the frequency reported in each orchard management was statistically the same, even though the maximum value for the orchard without management was eight species, while for the orchard with conventional management it was four (Table 2).


Several natural enemies affect the aerial colonies of woolly aphids and although its relevance varies according to the latitude and orchard management (Lordan et al., 2015), the joint occurrence of predators and parasitoids can mean better control of this pest (Gotinjo et al., 2015). The most frequently mentioned woolly aphid predators are: syrphids, coccinellidae, lacewings, bedbugs and earwigs (Walker, 1985; Asols, 1997; Mols and Boers, 1999; Short and Bergh, 2004), A. mali has been mentioned as a specific parasitoid with the capacity to significantly reduce its incidence in some areas (Gotinjo et al., 2012). In apple orchards established in Chihuahua were detected predatory syrphids, coccinellidae and chrysophos. Less species diversity was observed than those reported by Gotinjo et al. (2015), not detecting bedbugs and spiders. In the case of European earwigs (F. auricularia), reported as a soil inhabitant or places qualified for its protection and with cosmopolitan distribution (Asante, 1997; Nicholas et al., 2005, Lordan et al., 2015), its absence could have been due to the fact that the search for natural enemies was directed to aerial colonies of woolly aphid. A. mali was not detected in the orchard with conventional management, possibly due to its susceptibility to broad spectrum insecticides used in the pest control programs of this fruit (Cohen et al., 1996).

The detection of natural enemies of woolly aphid in apple trees should be strengthened with functional response tests to enable the implementation of a stable biological combat program, a desirable alternative to the restriction of organophosphate insecticides use and the public demand for sustainable strategies in the fight against pests (Altieri and Nicholls, 2012). Irrespective of the relative importance of natural enemies of woolly aphid detected in Chihuahua, the orchard management must include measures for its conservation with the manipulation of the implicit habitat to favor the increase in the diversity, the population of beneficial organisms and consequently, the phytophagous suppression (Fiedler et al., 2008).

Phytophagous diseases affecting apple orchards established in the western of Chihuahua state, México, are commonly fought with broad-spectrum insecticides, despite undesirable recognition of their use (Luckman and Metcalf, 1994). In this conventional phytophagous management, insecticides such as Carbaryl, Azinphos methyl, Dimethoate, Chlorpyrifos and Fosmet (Ramírez and Jacobo, 2002) are applied, and some of them are toxic to natural enemies (Cohen et al., 1996). There is an incipient knowledge that fruit growers have on phytophagous integrated management on apple trees and as a consequence, chemical combat is privileged to the point that it has been determined that of every eight agrochemicals sprays, only three of them have technical justification (Ramírez and Jacobo, 2002).

The conventional phytophagous management that is regularly practiced in the western Chihuahua state, should change if it is intended to be successful in the reduction of woolly aphid. The idea is inferred based on the results presented by Gontijo et al. (2012); Nicholas et al. (2005), in which they indicate the populations increase of woolly aphid by the continuous use of wide spectrum insecticides and in spite of the reduced detected number of aerial colonies of woolly aphid in the orchard with conventional management in this research. Therefore, the control of the woolly aphid could be satisfactory with the design of commercially viable integrated phytophagous management strategies (Nicholas et al., 2003).

Additionally, during the 2009-2010 winter for the apple orchards region of Cuauhtémoc, Chihuahua, there was a cold winter accumulation (based on the Richardson et al., 1974 procedure) of 621 cold units, while for the 2010- 2011 winter the accumulation of cold was 429 units. The lower accumulation of winter cold (benign winter) and later the occurrence of higher maximum temperatures and lower precipitation, coincided with the highest number of woolly aphid colonies and their natural enemies detected during 2011. The above, agrees with what was reported by Laštůvka (2009); Moerkens et al. (2012); Nicholas et al. (2005), who emphasized the winter temperature as one of the important factors of insect mortality. With respect to the occurrence of detected natural enemies, the bibliographic information of the effect of extreme temperatures on its survival is scarce, a possible explanation could be the way in which some of them winter (New, 1984; Honek, 1985; Cánepa et al., 2015).


The use of broad-spectrum insecticides in the orchard with conventional management reduced the incidence of aerial colonies of woolly aphid in apple trees and caused a reduction in the frequency of predators and absence of parasitism by A. mali, this evidence validates the raised hypothesis.

In apple orchards established in western of Chihuahua state, there are several natural enemies of woolly aphids that could be considered in the design of integrated management strategies once their functional response has been determined.

The low precipitation, benign winter, and subsequently the occurrence of higher maximum temperatures during the evaluation period may have influenced the incidence of woolly aphid colonies in apple trees and consequently in the abundance and richness of their natural enemies.

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Received: March 2017; Accepted: May 2017

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