Chrysopids (Neuroptera: Chrysopidae) Associated with Raoiella indica (Acari: Tenuipalpidae) in Colima, Mexico

Control of R. indica is largely through the application of chemical insecticide sprays, but given the height of some tree hosts and their presence in areas (e.g., tourist and residential zones) where this type of control raises environmental and public health issues, use of natural enemies is a promising alternative (Carrillo et al. 2014). We, therefore, performed periodic sampling to identify the naturally occurring chrysopids (Neuroptera: Chrysopidae) associated with this pest in Tecomán, Colima, Mexico.

At weekly intervals from 16 February to 21 October 2016, we observed and collected chrysopid larvae on coconut palms infested with R. indica. The trees were located on the El Real-Pascuales beachfront of Tecomán, Colima, Mexico (N 18°50′56.50″, W 103°57′15.40″). We used a 10× magnifying glass to observe larvae feeding on R. indica. Representative larvae were collected using a fine-hair brush, placed individually in 9-cm petri dishes, and transported to the Centro Nacional de Referencia de Control Biológico (CNRCB) in Tecomán, Colima, Mexico. Once in the laboratory, larvae were placed in 5-cm petri dishes, fed eggs of Sitotroga cereallela Olivier (Lepidoptera: Gelechidae), and allowed to develop at 25 ± 2°C until adulthood when they were placed in ethyl acetate and identified according to morphological characteristics.

Sex was identified using taxonomic key of Brooks and Barnard (1990, Bull. Brit. Mus. Nat. Hist. Entomol. 59: 117–286) and male and female genitalia descriptions of Tjeder (1971, Entomol. Scand. 2: 110–188). Species identification was performed using the keys of Tauber et al. (2000, Ann. Entomol. Soc. Am. 93: 1195–1221) for Ceraeochrysa and Brooks (1994, Bull. Brit. Mus. Nat. Hist. Entomol. 63: 137–210) for Chrysoperla.

We confirmed the identity of R. indica by using molecular analysis through the extraction of genomic DNA with the HotSHOT method (Truett et al. 2000, Biotech. 29: 52–54) and sequencing of the COI gene fragment. The identified specimens were placed in the Entomophagous Insect Collection (CIE) at CNRCB.

With each weekly sampling, we calculated the relative frequency by using the formula Fi = (n/N) × 100, where Fi is relative frequency; n is the number of samples in which the species appears; and N is the total number of samples collected. We assigned a relative frequency value by using the scale of Masson and Bryssnt (1974, J. Zool. 179: 289–302), with Fi > 30 = species occurs very frequently, Fi > 10 < 30 = species occurs frequently, and Fi < 10 = species occurs infrequently.

Based on morphological characters, we identified Ceraeochrysa cincta (Schneider), Ceraeochrysa claveri (Navás), Ceraeochrysa valida (Banks), Ceraeochrysa smithi (Navás), and Chrysoperla carnea sl. (Stephens) in these samples. In addition, we obtained and subsequently characterized a COI fragment of approximately 650 bp from specimens of Ch. carnea sl. because it is currently considered to be a complex including more than 15 cryptic species (Henry et al. 2013, Biol. Rev. 88: 787–808). Phylogenetic reconstruction of the COI mitochondrial region by using the neighbor-joining method for that sample showed evolutionary distances equal to those for members of species of the Ch. carnea complex from the GenBank database (Chrysoperla mohave [Banks], Chrysoperla johnsoni [Henry, Wells & Pupedis], Chrysoperla adamsi [Henry, Wells & Pupedis], Chrysoperla downesi [Smith]), thus supporting the conclusion that the specimen we collected belongs to the Ch. carnea sensu lato complex as per Henry et al. (2013). Canard and Thierry (2007, Ann. Museo Civico Stario Nat. Ferrara 8[2005]: 173–179) previously noted that the specific name Ch. carnea caused confusion and that species separation may be through analysis of mating calls of live insects of both sexes.

With the exception of Ch. carnea sl, the four species of Ceraeochrysa showed remnants of red mites on their dorsal surfaces. This is a behavior that enables the insect to transport residues from its prey and other organic materials to provide protection against its natural enemies (Adams 1982, Neur. Int. 2: 69–75).

A total of 713 chrysopid specimens were identified. Ceraeochrysa cincta and C. claveri were present during all 9 mo of the sampling. Ceraeochrysa cincta was collected most frequently (586 individuals), whereas 116 specimens of C. claveri were collected. Both species exhibited a high relative frequency value (Fi) (Table 1). These factors likely indicate adaptation of C. cincta to the coastal zone conditions in the state of Colima. To the contrary, only seven specimens of C. valida (Banks), three specimens of C. smithi (Náva), and one of Ch. carnea sl. were collected.

Table 1 Relative frequency of different species of chrysopids associated with R. indica in coconut palms of the El Real-Pascuales beach front in Tecomán, Colima, Mexico, from February to October 2016.

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Ceraeochrysa larvae feed on different agricultural pests, including mites (Tauber et al. 2000). In Mexico, species of this family have been observed preying on mites in fruit trees such as citrus, Citrus spp., and guava, Psidium guajava L., in the states of Colima, Michoacán, Nuevo León, and Tamaulipas (Tauber and de León 2001, Ann. Entomol. Soc. Am. 94: 197–209), in addition to coconut palm.

We found citations of only C. claveri, Chrysopodes collaris (Scheider), and Chrysopa cubana (Hagen) as preying on R. indica (González et al. 2013, Rev. Protección Veg. 28: 215–218; Carrillo et al. 2014). Thus, our study is the first report of natural predation of C. cincta, C. valida, C. smithi, and Ch. carnea sl. on R. indica. These chrysopid species, especially C. cincta and C. claveri that are the most abundant, might be considered for biological control agents of R. indica.