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Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.7 no.2 Texcoco feb./mar. 2016

 

Articles

Chrysopidae species associated with Diaphorina citri Kuwayama in citrus and predation capacity of Sinaloa, Mexico

Edgardo Cortez-Mondaca1 

J. Isabel López-Arroyo2 

Luis Rodríguez-Ruíz3 

Mara P. Partida-Valenzuela4 

Jesús Pérez-Márquez5  § 

1INIFAP-C. E. Valle del Fuerte, 1609. Carretera México-Nogales, km Juan José Ríos, Sinaloa, México. (cortez.edgardo@inifap.gob.mx).

2INIFAP-C. E. General Terán. General Terán, Nuevo León, México. (lopez.jose@inifap.gob.mx).

3Junta Local de Sanidad Vegetal del Valle del Carrizo. Villa Díaz Ordaz, Sinaloa, México. (insectosbeneficosjlvc@hotmail.com).

4Universidad Autónoma de Sinaloa- Facultad de Agronomía. Carretera Culiacán-Eldorado, Culiacán, km17.5, Sin, México. (mapaval_1411@hotmail.com).

5INIFAP-C. E. Valle de Culiacán. Carretera Culiacán-El Dorado, km 17.0, Culiacán, Sin., México. (marquez.jesus@inifap.gob.mx).


Abstract

The study objectives were to determine species associated Chrysopidae Asian citrus psyllid Diaphorina citri Kuwayama in commercial orchards in the state of Sinaloa, Mexico, and evaluate the ability of predation on eggs and nymphs of D. citri. Five species of Chrysopidae were identified in orange orchards and Mexican lime in different regions of the state of Sinaloa; Chrysoperla comanche (Banks), Chrysoperla rufilabris (Burmeister), Chrysoperla carnea s. lat., Ceraeochrysa valid (Banks) and Ceraeochrysa Claveri (Navas). Ch. Comanche and Ceraechrysa valida were the most abundant species (p< 0.0004); Ch. comanche and Ch. rufilabris and showed greater capacity for predation immature eggs, nymphs girls (nymph 1 and nymph 2) and large nymphs (nymph 4 and nymph 5) to D. citri during the first six hours of exposure prey to predator. However, in the last reading of predation, at 24 h, all species of lacewing consumption had almost similar (p> 0.05), about 100 specimens per predator. Egg consumption and nymph girl was greater than that of large nymphs. These results support the use of Ch. comanche for biological control of D. citri in the state of Sinaloa.

Keywords: Chrysoperla comanche; Ch. rufilabris; Ch. carnea; Ceraeochrysa valida; C. Claveri; biological control

Resumen

Los objetivos del estudio fueron determinar especies de Chrysopidae asociadas al psílido asiático de los cítricos Diaphorina citri Kuwayama, en huertas comerciales en el estado de Sinaloa, México, y evaluar la capacidad de depredación sobre huevo y ninfas de D. citri. Se identificaron cinco especies de Chrysopidae en huertas de naranja y limón mexicano en diferentes regiones del estado de Sinaloa; Chrysoperla comanche (Banks), Chrysoperla rufilabris (Burmeister), Chrysoperla carnea s. lat., Ceraeochrysa valida (Banks) y Ceraeochrysa claveri (Navás). Ch. comanche y Ceraechrysa valida fueron las especies más abundantes (p< 0.0004); Ch. comanche y Ch. rufilabris mostraron mayor capacidad de depredación de estados inmaduros: huevos, ninfas chicas (ninfa 1 y ninfa 2) y ninfas grandes (ninfa 4 y ninfa 5) de D. citri durante las primeras seis horas de exposición de las presas al depredador. Sin embargo, en la última lectura de depredación, a las 24 h, todas las especies de crisopa presentaron un consumo prácticamente similar (p> 0.05), de alrededor de 100 especímenes por depredador. El consumo de huevo y ninfa chica fue mayor que el de ninfas grandes. Estos resultados sustentan el empleo de Ch. comanche para el control biológico de D. citri en el estado de Sinaloa.

Palabras clave: Chrysoperla comanche; Ch. rufilabris; Ch. carnea; Ceraeochrysa valida. C. claveri; control biológico

Introduction

The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) vector Huanglongbing (HLB) caused by the bacterium Candidatus Liberibacter spp., the worst disease of citrus worldwide. In heavy infestations can kill the psyllid vegetative buds of growing plants or cause leaf abscission (Michaud, 2004). Also cause direct damage to the foliage, which facilitates the deformation of leaves and affects yield potential. The HLB management should be based on the timely removal of infected trees, use of healthy plants from certified nurseries and protected in the management of vector populations D. citri (da Graca, 1991; Chiou, 1998; da Graca y Korsten, 2004; Bové, 2006; National Research Council, 2010).

In Mexico, it has driven the integrated management of insect through the implementation of a regional plan, the scheme provides for chemical control to reduce or eliminate vector populations and biological control through massive release of parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae), considered the main natural enemy of D. citri (Chien et al., 2001; Etienne et al., 2001; McFarland and Hoy, 2001; Aubert, 2008). At home there are two breeding centers parasitoid and while maintaining a considerable production thereof is insufficient to meet the requirement of the citrus regions where they are produced (Yucatán's peninsula and region the Pacífico's lemon).

Moreover, there are numerous predators attacking D. citri populations. Usually the most abundant are some species of lacewings Chrysoperla and Ceraeochrysa gender also coccinellid (Cortez-Mondaca et al., 2010; Lopez-Arroyo et al., 2010) as the gray ladybug Olla v-nigrum (Mulsant), which shows a high potential to suppress pest populations (Michaud, 2004). In Mexico there is at least one laboratory reproduction of beneficial insects in each entity in most of them playing some kind of Chrysoperla (Bahena, 2008, SENASICA, 2011).

This infrastructure and equipment can be utilized to reproduce some of the species associated with D. citri on citrus. This study was conducted in order to determine the species of Chrysopidae associated with the Asian citrus psyllid in commercial orchards, in the state of Sinaloa and evaluate the ability of predation in the stages of egg, girls nymphs and large Asian psyllid citrus.

Materials and methods

The study was conducted in two stages:

Stage I. Collection and identification of species associated Chrysopidae Asian citrus psyllid in commercial orchards. It was conducted under field conditions using pickings lacewing adults and reproduction of the species obtained was performed at the Laboratory Breeding Beneficial Insects of the Local Board of Plant Protection Carrizo Valley, located in Villa Diaz Ordaz, Sinaloa. During the months of july 2010 to september 2011.

Were performed 12 adult lacewing pickings with entomological net in six commercial orchards of orange Citrus sinensis Osbeck and lemon Mexican Citrus aurantifolia Swingle located in the north, in the town of Ahome; in the center, in the town of Mocorito; east, in the municipality of Sinaloa de Leyva; and in the south, in the town of La Cruz de Elota, the state of Sinaloa, in July 2010, March 2011, August 2011 and September 2011 (Table 1). Lacewing adults captured by three to five hours hits an entomological net in different parts of each citrus orchard in each sampling date, they were confined in cages and transported to the laboratory breeding of beneficial insects The Local Board Plant health Carrizo Valley, where they were given food and waited for them to reproduce (F1), third instar larvae were identified to species based on the taxonomic keys Lopez-Arroyo et al. (2008) and Tauber and Leon (2001), using a stereoscopic microscope.

Table 1 Number of lacewing adults captured in commercial citrus orchards in the state of Sinaloa, Mexico. 

Fecha Sitio Coordenadas Adultos capturados Cultivo
05/07/2010 CLARVI, Ahorne 25°47'51.54";108°56'18.38" 100 Limón mexicano
06/07/2010 Dolores Hidalgo, Ahorne 26°21'11.55";109°00'20.05" 52 Naranja
07/07/2010 Agua Nueva, Ahorne 25°51'22.35";109°05Ό4.74" 127 Naranja
08/07/2010 Dolores Hidalgo, Ahorne 26°21'11.55";109°00'20.05" 150 Naranja
09/07/2010 Agua Nueva, Ahorne 25°51'22.35";109°05Ό4.74" 125 Naranja
10/07/2010 CLARVI^^ 25°47'51.54";108°56'18.38" 220 Limón mexicano
13/07/2010 Dolores Hidalgo, Ahorne 25°47'51.54";108°56'18.38" 158 Naranja
15/07/2010 Dolores Hidalgo, Ahorne 25°47'51.54";108°56'18.38" 208 Naranja
16/03/2011 Caimanera, Mocorito 24°57Ό8.71";107°44'36.06" 190 Naranja
17/03/2011 La Guamuchilera, Mocorito 24°56'14.64";107°43'47.46" 130 Naranja
25/03/2011 Caimanera, Mocorito 24°57Ό8.71";107°44'36.06" 400 Naranja
26/08/2011 Genaro Estrada, Sinaloa de Leyva 25°55'38.89";108°23Ό4.02" 120 Limón mexicano
07/09/2011 Ejido El Bolillo, La Cruz de Elota 24°01Ί7.29";106°49Ό4.76" 212 Naranja
12/09/2011 Ejido El Tecuyo, La Cruz de Elota 24°54Ό1.40";106°43'30.03" 145 Naranja
Total Ocho sitios 2 337 Dos especies

In 3520 larvae obtained in the first generation (F1) was randomly identified 550 larvae (15.6%), product screenshots July 2010; 300 larvae of 653 (45.9%), 300 larvae of 387 (77.5%) and 604 larvae 1 573 (38.4%) of each of the three sacks in March 2011; Larvae produced 233 233 (100%) of the capture of august 2011; and 718 larvae, product of two catches september 2011, the total (100%) were inspected.

The results of the samplings were separately subjected to a one-way ANOVA, considering the sampling dates as repetition. The average obtained for each species was applied the Tukey test (5%) (SAS, 2009), the relative abundance of each species of lacewing obtained (Magurran, 1988) was calculated and graphic results were formulated. In the laboratory of CEVAF reference specimens are preserved.

Stage II. Capacity assessment predation Ch. Carnea Stephens, Ch. Rufilabris, Ch. Comanche and C. valida on some of the immature stages of D. citri. This stage was carried out under laboratory conditions at the National Institute of Agricultural and Livestock Forestry Research (INIFAP) -Campo Experimental Valle del Fuerte (CEVAF), seven tests were conducted predation, four eggs, one with girls nymphs (first and second instar) and two large nymphs (fourth and fifth instar) during july and august 2011.

Predators. second instar larvae of the green lacewing species existing laboratory breeding of beneficial insects, the Local Board of Plant Protection Carrizo Valley, at the time of each test were evaluated. Evaluated lacewing larvae adults obtained corresponded to identify species Chrisopidae (Cortez-Mondaca et al., 2011).

Preys. For testing highly infested seedlings with D. citri were collected from five to 10 cm in length for commercial trees citrus groves and backyard trees, usually Mexican lime for immature stages of the Asian citrus psyllid and they were counted, to establish a certain number of them in each outbreak. With an entomological needle is removed from each outbreak different development states the purpose of evaluation, only specimens of age who wanted to assess in each event were left. Outbreaks usually containing 100 copies of D. citri, were placed in a plastic petri dish of 13 cm in diameter and 2 cm, and exposed to a second instar larva, previously isolated and subjected to fasting for 24 h (Cortez et al., 2002). The larva fasting was placed directly on containing outbreaks dams; then shoots were examined at different intervals of time, for counting the number of surviving specimens, eggs, nymphs or large nymphs girls. The difference between before and after the inspection was the number of prey consumed.

For each kind of larva stage of the dam and four replications of the test were performed. The results were subjected to a one-way ANOVA; the averages were applied Tukey test (5%) (SAS, 2009).

Results

Stage I. Determination of the number of species associated Chrysopidae the Asian citrus psyllid. A total catch of 2 337 adult lacewing commercial citrus orchards in the state of Sinaloa, Mexico was obtained. The number of adults captured by orchard and date of capture, was variable, from 52 specimens in Dolores Hidalgo, Ahome, on July 6, 2010, 400 specimens from Orchard Caimanero Mocorito on 25 March 2011. Generally the number of catches by date and orchard were about 150 adults (Table 1).

Species identification. In the first three dates grouped catches, august 7, 2010, 16 and 17 march 2011, Ch. Comanche was the predominant species (Figure 1), while the dates of march 25 and august 26, and on september 7, 2011, C. valid was the most abundant. Ch. Carnea and C. Claveri were the rarest species, the first one occasion captured on the first sample and the second in the last two dates and places of capture. The results of the ANOVA showed significant difference in the prevalence of C. valid and Ch. Comanche about Ch. Rufilabris, C. Claveri and Ch. Carnea (p< 0.0004). Whereas in the calculation of the relative abundance of each species, C. validates showed nearly half of the total captured specimens (0.495), followed closely by C. Comanche (0447), together accounted for 0.942 of relative abundance; all other species in total amounted to only 0.057 (Figure 2).

Figure 1 Number of specimens Crhysopidae identified to species, adult captured in citrus orchards in Sinaloa, Mexico. 

Figure 2 Relative abundance of species Chrysopidae in commercial orchards of orange and Mexican lime in Sinaloa, Mexico. 

Stage II. Capacity assessment predation Ch. carnea, Ch. rufilabris, Ch. comanche and C. valida. In four tests predation on eggs of D. citri no significant difference between treatments (p> 0.05) was detected; however, in all tests Ch. rufilabris showed increased consumption of dams in the early hours of exposure, after five or six hours had consumed 90% or more of the available eggs. In the second test, Ch. Comanche consumed more than Ch. Carnea in the first four readings predation (Figure 4). In the third evaluation Ch. Carnea consumed more egg in the first three readings of predation compared to Ch. Comanche (Figure 5). In the latest assessment of egg predation Ch. Comanche, it predated C. valid only in the first five readings (Figure 6). Lacewing evaluated species consumed nearly all of D. citri eggs before or 24 h exposure (Figures 4, 5 and 6).

Figures 3, 4, 5 and 6 Consumption of eggs Diaphorina citri lacewing species of broodstock from citrus groves. 

The only assessment girls nymphs (first and second instar) with Ch. rufilabris, Ch. comanche and C. valida, significant difference (p< 0.001) was obtained in the first five readings of predation. Girl consumption D. citri nymphs was significantly different between Ch. comanche and Ch. valid in the first five readings mortality.; and about Ch. comanche and Ch. rufilabris significant difference in consumption of nymphs in the first and third reading predation. Ch. comanche consume 99 specimen of D. citri to four hours of exposure (third reading) of dams The three species preyed nymphs girls total 24 h of exposure (Figure 7).

Figure 7 Consumption small Diaphorina citri nymphs lacewing species of broodstock from citrus groves. 

In the first test of predation capacity Ch. Rufilabris, Ch. Comanche and Ch. Carnea on large nymphs (fourth and fifth instar) of D. citri, no significant difference between the readings of predation (p< 0.001) was detected. The consumption of prey by Ch. rufilabris was higher in the first four readings (1, 2, 3 and 5 h), but at 24 h Ch. comanche consumption exceeded the other two species. Among Ch. comanche and Ch. carnea the difference in consumption was reduced in the four readings prumras predation, but all readings was higher for the former species. After 24 h of exposure, all species consumed more than 90 large nymphs of D. citri on average (Figure 8). In the second test, with evaluation of Ch. rufilabris, Ch. comanche, Ch. carnea and C. valid, significant difference between treatments (p< 0.001) was observed Ch. comanche concerning C. valida and Ch. carnea, but compared to Ch. rufilabris at first reading (a one hour exposure prey-predator). In other readings predation no significant difference between treatments was determined even though the average values of predation is different (Figure 9), protruding Ch. Comanche readings 5, 6 and 7 h exposure. C. valida showed the lowest consumption of prey, especially in the first three readings of predation, in other consumption was close to that of Ch. carnea (Figure 9).

Figure 8 and 9. Consumption of large nymphs Diaphorina citri lacewing species of broodstock from citrus groves. 

Discussion

Species abundance and diversity

In other regions of the country indicated the presence in the various species of citrus species Chrysopidae of the gender Ceraeochrysa, Chrysopa, Chrysoperla, Eremochrysa and Leucochrysa, mainly (López-Arroyo, 2000; López-Arroyo et al., 2010). In the citrus area of Sinaloa, only species Chrysoperla and Ceraeochrysa were found, which shows a lack of diversity of this important group of predators. This could be even more critical, because in at least two areas were released commercially species C. valida and Ch. comanche.

In the orchard of Caimanero prior to sampling capture march 16, 2011 (Table 1), four releases of 10 000 eggs must Ch. comanche, controlling D. citri at intervals of 15 days, were performed it follows that their dominance was influenced in part by releases. While in the orchard of Sinaloa de Leyva, where species were captured C. valida and C. claveri, releases were made Ch. comanche and to C. valida, at the same intervals and doses mentioned earlier, in the period october 2010 to january 2011, and later, during August 2011 was released twice by Ch. carnea, standing breeding arable crops. However, no adult latter species were recovered. The reduced presence of Ch. carnea in citrus trees could be associated with the preference of the species for arable habitats, while the other species are listed as being of arboreal (Brooks y Barnard, 1990; Brooks, 1994; Albuquerque et al., 2001).

In the state of Sinaloa, is dominated by a warm and semi-arid climate with some variation in relation to the presence of vegetation, which differ in abundance and diversity, being relatively higher in the south central part of the state; the average temperature in the winter months (november to march) ranges from 19 °C to 22 °C and, while in the summer months 8 may to september, fluctuates between 24 °C and 28 °C. The citrus orchards in the capture adult Chrysopidae was conducted are located in agricultural valleys, where a lesser or greater degree extensive use of pesticides and agrochemicals in general, especially in horticultural crops, takes place during the months october to april. With regard to the above, in all orchards specimens of C. valida only in an orchard We obtained specimens were obtained C. comanche and two orchards not obtained Ch. rufilabris. While Ch. carnea was obtained only in orchards in northern Sinaloa and C. claveri was obtained in two locations in the town of orchards La Cruz de Elota and Sinaloa de Leyva. Unknown factor that determined the production of different species orchard, but as already mentioned, in the orchard of Caimanero and Sinaloa de Leyva releases C. valida and C. comanche. were performed.

This study is the first report of identification of species associated Chrysopidae Asian citrus psyllid in Sinaloa.

Predation: Chrysopidae species evaluated showed the same ability to predation; however, C. rufilabris showed more greed in the early hours of exposure of the dams. The species evaluated consumed nearly all of dams exposed 24 h or before the end of the evaluation period. Small nymphs significant difference (p< 0.001) was obtained in the first five readings exposure. C. comanche demonstrated greater predation, followed by C. rufilabris. However, at 24 h the three species generally consumed the dams 100 exposed.

With large nymphs significant difference (p< 0.001), Ch. Ccomanche and Ch. rufilabris was obtained showed significant difference in prey consumption compared to C. valida in the first reading of prey consumption (24 h). As usual, the consumption of large nymphs of D. citri was lower than that of eggs and nymphs girls. It is necessary to determine the total required dams D. citri, different stages of development, each kind of Chrisopidae first, second and third instar, to estimate the total consumption capacity.

Implications for the biological control of D. citri. The decision to use any kind of these predators for biological control rising against the Asian citrus psyllid, depend on the adaptation reflected their predominance in a given environment (Cortez-Mondaca et al., 2008); the predatory capacity on the psyllid in question (Tauber et al., 2000) and the feasibility of production of each, this attribute should include the ability to reproduce and the cycle of life, because they influence the cost of investment by specimen reproduced. For feasibility of reproduction, the difference between Chrysoperla species evaluated is reduced; while species "load dump" C. valida and C. claveri and have a higher larval life cycle in 3-4 days and periods preovisposición differing in 3-9 days, which involves a period greater power and maintenance laboratory ; however, these factors may be advantages in the field, as it would have a predator active for a longer time (López-Arroyo et al., 1999; Albuquerque et al., 2001; López-Arroyo and De León, 2002).

Lacewings playback is possible, since each institution in the country have at least one laboratory reproduction of beneficial insects and most played some kind of Chrysoperla (Bahena, 2008, SENASICA, 2010).

Conclusions

The higher prevalence of C. comanche in citrus, combined with the ability to prey consumption suggest that Ch. comanche may have greater chance of success against the Asian citrus psyllid in Sinaloa, Mexico.

The use of lacewing is proposed as an alternative that would reduce exclusive dependence on chemical control for controlling D. citri. Also, avoid the risks inherent in the use of toxics environment.

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Received: December 2015; Accepted: February 2016

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