Soursop, Annona muricata L. (Annonaceae), is native to the tropical regions of the Americas and the Caribbean, and is considered the most important species of the family. The principal use of this fruit is fresh consumption; however, it has a variety of medicinal and industrial uses (Coto & Saunders 2001; Jiménez et al. 2017). According to Hernández et al. (2013), Mexico is the principal producer of soursop in the world. Production currently is about 23,715 metric tons per yr, with a commercial value of around 159,856 million pesos (US $8,295,632). Most of the production is concentrated in the state of Nayarit, with a planted area of 1,990 ha, distributed in the municipalities of Compostela (1,912 ha), San Blas (52.4 ha), Bahía de Banderas (12 ha), Tepic (7.16 ha), and Xalisco (6.54 ha) (SIAP 2016).

The crop has several phytosanitary problems that considerably affect the production of fruit. At least 296 species of arthropods associated with the genus Annona are known from tropical countries; insects in the families Coccidae (Hemiptera), Noctuidae (Lepidoptera), Oecophoridae (Lepidoptera), and Eurytomidae (Hymenoptera) are most common (Vidal et al. 2014). In Costa Rica, Coto and Saunders (2001) recorded 10 species of insects that affect soursop cultivation and cause decreases in the yield and quality of the fruit.

In Mexico, several species of insect pests have been associated with A. muricata, including Optatus palmaris Pascoe (Coleoptera: Curculionidae), Euphoria sepulcralis (Fabricius) (= E. leucographa [Gory & Percheron]) (Coleoptera: Melolonthidae), Anastrepha ludens (Loew) (Diptera: Tephritidae), Saissetia nigra (Nietner) (Hemiptera: Coccidae), Acanthocephala femorata F. (Hemiptera: Coreidae), Membracis mexicana Guérin-Méneville (Hemiptera: Membracidae), Vanduzea segmentata (Fowler) (Hemiptera: Membracidae), Dysmicoccus brevipes (Cockerell) (Hemiptera: Pseudococcidae), Ferrisia virgata (Cockerell) (Hemiptera: Pseudococcidae), Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), Planococcus citri Risso (Hemiptera: Pseudococcidae), Corythucha gossypii F. (Hemiptera: Tingidae), Bephratelloides cubensis Ashmead (Hymenoptera: Eurytomidae), Oenomaus ortygnus Cramer (Lepidoptera: Lycaenidae), Gonodonta pyrgo Cramer (Lepidoptera: Noctuidae), Cerconota anonella Sepp (Lepidoptera: Oecophoridae), and unspecified specimens of Lonchaeidae (Diptera) and Pyralidae (Lepidoptera) (MacGregor & Gutiérrez 1983; Sánchez & Franco 2001; Ruiz et al. 2014; Vidal et al. 2014; Hernández et al. 2013, 2015; Cambero et al. 2017).

Chemical control is the method most used by producers for the management of these pests, although in Mexico there are no pesticides authorized for use in soursop by the Federal Commission for Protection against Health Risks (COFEPRIS 2018). Hernández et al. (2008) evaluated the insecticides dimethoate, malathion, chlorpyrifos-ethyl, cypermethrin, endosulfan, and azadirachtin for control of the seed borer B. cubensis in soursop, and reported that dimethoate was the most effective. A promising, sustainable, and ecological alternative for this problem is the use of beneficial organisms such as predators and parasitoids. Beneficial insects have the potential to regulate pest populations due to the dense-dependent relationship they establish, and they generally are considered to be harmless to humans and safe for the environment (Gutiérrez et al. 2013). Identification of the pest and beneficial insects associated with soursop cultivation in the state of Nayarit is of great importance, because this information will be important in identifying future actions for phytosanitary management of this crop. However, we undertook a survey of the insects associated with soursop cultivation in the principal producing municipalities of the state of Nayarit, Mexico.

Materials and Methods

The biological material (insect pests, parasitoids, predators, and insects associated with the crop) was obtained through biweekly sampling from Nov 2016 to Dec 2017 in 13 commercial soursop orchards, 7 located in the municipality of Compostela, and 6 in the municipality of San Blas, Nayarit, Mexico (Table 1).

Insect pest collections were carried out on 10 soursop trees selected randomly in each of the orchards, where 4 cardinal points of each tree were visually inspected for insects or their indicators (damage). Biological materials collected (insects, leaves, fruits, and seeds), were taken to the Laboratory of Agricultural Parasitology of the Multidisciplinary Center of Scientific Research 03 of the Autonomous University of Nayarit, where the insect specimens were separated and deposited in 50 mL clear plastic bottles with 70% ethyl alcohol for preservation prior to identification.

Fruits, seeds, and leaves with the presence of insects or signs of damage were placed in 1.8 L black plastic containers with a perforation in the middle, where a 50 mL clear plastic bottle was attached in order to use attraction to light as a means to obtain adult parasitoids associated with the principal soursop insect pests. These containers were maintained at a temperature of 25 ± 2 °C, and the material was systematically examined every 24 h.

Table 1.

Orchards studied to obtain the insects associated with soursop cultivation in Nayarit, México.

The predators detected in action on insect pests of interest were collected directly from the leaves, branches, flowers, and fruits. When no predatory action was recorded directly in the field, putative predators and different stages of insect pests were collected with the help of an entomological aspirator and were taken to the laboratory, where they were placed with potential prey in 90 mm diam Petri dishes to observe their acceptance or rejection.

Representative insect pests, parasitoids, and predators were preserved in 70% alcohol for identification using Motic® SMZ 168 stereoscopic (Motic Inc., LTD, Hong Kong, China) and LEICA™ DME compound microscopes (Leica Microsystems, Wetzlar, Germany), both purchased in Mexico, and the use of taxonomic keys of Slater and Baranowski (1978), Gordon (1985), Williams and Watson (1988, 1990), Williams and Granara de Willink (1992), Gibson et al. (1997), Blackman and Eastop (2000), Strange (2000), Godoy et al. (2006), and Valencia et al. (2006) for insect pests, parasitoids, and predators, as well as those of Blake (1933), Blackwelder (1944), Curran (1965), and Lasoń and Przewoźny (2009) for other insects associated with the crop. Confirmation of the species was made by specialists of the Entomology and Acarology Laboratory of the National Phytosanitary Reference Center. The identified specimens were deposited in the Insect Collection of the Agricultural Parasitology Laboratory, Autonomous University of Nayarit.

Results

In this study, 3,674 insect specimens were collected, of which 3,103 were phytophagous, 353 were parasitoids, 92 were predators, and 126 were insects with different eating habits (Table 2).

In our study of the phytophagous species, 2,809 specimens were in the order Hemiptera, 165 in Hymenoptera, 84 in Coleoptera, and 45 in Lepidoptera; M. hirsutus was the most abundant species with 356 specimens, even though it was found in only 8 of the 13 orchards. Second in abundance was Aphis spiraecola Patch (Hemiptera: Aphididae) with 338 specimens from 5 orchards, but with a collection of 202 specimens in the “Altavista 2″ orchard, the largest number of phytophagous insects collected by orchard. Bephratelloides cubensis is the only species that appeared in all orchards. “Chacala 1,” “Chacala 3,” and “El Llano” are the orchards from which we collected the lowest number of species (3). “Altavista 1″ recorded the highest number of species (19), although with fewer specimens (523) than “Palmas 1,” where there were (18) species and 613 specimens. When comparing soursop pests recorded in Mexico by different authors (MacGregor & Gutiérrez 1983; Sánchez & Franco 2001; Ruiz et al. 2014; Vidal et al. 2014; Hernández et al. 2013, 2015; Cambero et al. 2017), in this study we recorded an additional 9 species as new records of phytophagous pests. Orchard altitude did not seem to affect the number of pests or the number of specimens captured.

Table 2.

Number of specimens collected of phytophagous insect species associated with soursop cultivation in orchards of the municipalities of Compostela (39–437 masl) and San Blas (183–382 masl), Nayarit, Mexico.

In the municipality of Compostela, 1,727 specimens from 20 species of phytophagous insects, and 10 families of 4 orders were observed. The order with greatest abundance and diversity was Hemiptera, with 1,587 specimens of 16 species, followed by Hymenoptera with 82 specimens of 1 species, Lepidoptera with 30 specimens of 1 species, and Coleoptera with 28 specimens of 2 species. The most abundant species was M. hirsutus with 280 individuals, followed by Pinnaspis sp. (272) and A. spiraecola (246). The orchard with the highest number of insects collected was “Altavista 1″ (523), whereas the orchard with the lowest number was “Chacala 1″ (82).

In the municipality of San Blas, 1,376 specimens from 18 species of phytophagous insects, and 9 families of 4 orders were observed. The order with the greatest abundance and diversity was Hemiptera, with 1,222 specimens of 14 species, followed by Hymenoptera with 83 specimens of 1 species, Coleoptera with 56 specimens of 2 species, and Lepidoptera with 15 specimens of 1 species. The most abundant species was Pinnaspis sp. with 309 individuals, followed by Aulacaspis sp. (129), P. citri (98), and M. mexicana (97). “Palmas 1″ was the orchard with the highest incidence of pests (613) and “El Llano” was the lowest (35).

Relative to parasitoids and predators (Table 3), more parasitoid specimens (353) than predators were collected (92). Five species of parasitoids were collected; the most abundant species was Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) with 93 specimens, followed by Aphytis sp. (75) and Gyranusoidea indica Shafee, Alam & Agarwal (Hymenoptera: Encyrtidae) (74). Parasitoids were collected from all the orchards of the 2 municipalities, although different species. In Compostela, a greater number was collected (242) than in San Blas (111); “Altavista 1″ is the orchard where the largest number of parasitoids was collected (79), and “El Llano” was the least (5). “Altavista 1,” “Tecuitata 1,” and “Palmas 1″ were the orchards with the greatest diversity (5 species), whereas in “Chacala 1,” “Chacala 3,” “Divisadero,” and “El Llano,” only 2 species were collected. Regarding the predators, 12 species were collected; the most abundant species was C. sanguinea with 36 specimens, followed by S. pinachi (14) and H. convergens (11). All the predators were collected from 6 orchards. In Compostela, a greater number of specimens was collected (47) than in San Blas (45), although in San Blas a greater number of predatory species was collected (8) than in Compostela (6). “Palmas 1″ was the orchard where the largest number of specimens (31) and 7 species were collected, followed by “Altavista 1″ with 28 specimens from 5 species; in the remaining orchards, 4 to 14 specimens and 1 to 4 species were collected per orchard. Stethorus pinachi was the most-collected species in a single orchard (11 specimens in “Altavista 1″).

In the municipality of Compostela, Aphytis sp., Coccophagus sp., Encarsia sp., A. kamali, and G. indica were detected parasitizing Pinnaspis sp., Saissetia nigra, Aulacaspis sp., and G. indica. The most-represented species was G. indica with 64 individuals, followed by A. kamali (58) and Aphytis sp. (53). As for the predators, of the ladybird beetles A. orbigera, C. sanguinea, S. pinachi, and the lacewings C. valida, Ceraeochrysa sp., and C. externa were detected. The ladybird beetle C. sanguinea was the most abundant with 22 specimens, followed by S. pinachi (12) and Ceraeochrysa sp. (5); the lacewings were collected only in the orchard “Altavista 1.” On the other hand, in the municipality of San Blas, the parasitoids Aphytis sp., Coccophagus sp., Encarsia sp., A. kamali, and G. indica were detected parasitizing Pinnaspis sp., S. nigra, Aulacaspis sp., and M. hirsutus. The parasitoid A. kamali was best represented with 35 individuals, followed by Coccophagus sp. (24) and Aphytis sp. (22). The species of predators recorded were Chilocorus sp., C. sanguinea, Cycloneda sp., H. convergens, O. v-nigrum, P. pallidula guticollis, and S. pinachi preying on aphids, and C. montrouzieri preying on M. hirsutus. Cycloneda sanguinea was the most abundant species with 14 specimens followed by H. convergens (11), and C. montrouzieri and Cycloneda sp. (6 each). Predators were collected in only 2 of the orchards (Palmas 1 and 2) and lacewings were not collected in this municipality.

In addition to the pests and natural enemies (parasitoids and predators), 126 specimens of insects with ‘other’ eating habits (e.g., fungi, honeydew, etc.) were detected: Disonycha glabrata F. (Coleoptera: Chrysomelidae), Chalcolepidius silbermanni Chevrolat (Coleoptera: Elateridae), Rhodobaenus 13-punctatus (Gyllenhal) (Coleoptera: Curculionidae), Lobiopa insularis Castelnau (Coleoptera: Nitidulidae), Agathon sp. (Diptera: Blephariceridae), Drosophila icteroscuta Wheeler (Diptera: Drosophilidae), Nephrocerus scutellatus (Macquart) (Diptera: Pipunculidae), Anasa armigera (Say) (Hemiptera: Coreidae), Ochrimnus lineoloides Slater (Hemiptera: Lygaeidae), and Kallitaxila granulata (Stål) (Hemiptera: Tropiduchidae), which were collected either directly from the soursop trees, or emerged from the decaying fruits (Table 4).

Discussion

The diversity of species with phytophagous habits recorded in this study surpass those found by Hernández et al. (2013), who reported 9 species associated with the cultivation of soursop, among which B. cubensis, C. anonella, and O. ortygnus are considered pests of economic importance in Mexico. Ruíz et al. (2014) reported that the species Neosilba spp. (Diptera: Lonchaeidae), B. cubensis, and C. anonella were the most abundant phytophagous species in the state of Veracruz, whereas Sánchez and Franco (2001) and Hernández et al. (2006) recorded B. cubensis in soursop plantations in the states of Tabasco and Nayarit, respectively. It should be mentioned that the species with the greatest abundance in this study were Pinnaspis sp., M. hirsutus, Aulacaspis sp., A. spiraecola, and B. cubensis, and their presence in the production zones in the state broadens the range of organisms that could be considered part of the important soursop pest complex.

Among the secondary species (those of lesser abundance), E. leucographa, O. palmaris, and G. pyrgo were observed. Ruiz et al. (2014) and Cambero et al. (2017) also reported E. leucographa feeding on the soursop fruit, without mentioning the level of damage, in the states of Veracruz and Nayarit, respectively. On the other hand, Vidal et al. (2014) reported that O. palmaris uses Annona squamosa L. (Annonaceae) as a host, whereas Castañeda (2011) reported the occurrence of O. palmaris on A. muricata during the mo of Nov and Dec in the municipality of Compostela, Nayarit, quantifying the resulting damage. Hernández et al. (2015) mentioned that G. pyrgo could be abundant and cause up to 40% of defoliation in mature trees, which causes a reduction in the quality and production of soursop fruits in the state of Nayarit.

In the soursop-producing areas in this study, Aphytis sp., Coccophagus sp., Encarsia sp., A. kamali, and G. indica occurred as parasitoids of Pinnaspis sp., S. nigra, Aulacaspis sp., and M. hirsutus. Hernández et al. (2013) and Ceballos et al. (2016) mentioned that the parasitoids A. kamali and G. indica are used in the biological control programs of the pink hibiscus mealybug in Mexico and Cuba, respectively. On the other hand, Gaona et al. (2006) noted that the species of the genus Anagyrus, Aphytis, Coccophagus, and Encarsia, have the ability to exercise a natural control over the Coccoidea in Ciudad Victoria, Tamaulipas, and could be used as an alternative to biological control in ornamental and fruit plants of that state.

Table 3.

Number of specimens collected of parasitoids and predators associated with insect pests in soursop cultivation in orchards of the municipalities of Compostela and San Blas, Nayarit, Mexico.

Table 4.

Number of insect specimens collected in association with soursop cultivation in orchards of the municipalities of Compostela and San Blas, Nayarit, Mexico.

With respect to predators, 9 species of ladybug and 3 species of lacewing were observed, among which C. sanguinea, H. convergens, and S. pinachi (Coccinellidae) and Ceraeochrysa sp. (Chrysopidae) were the most abundant. These results are similar to what was recorded by Rodríguez et al. (2017), who reported the presence of these species in the jackfruit plantations in the municipalities of Compostela and San Blas, Nayarit, Mexico.

In this study, the ladybird beetle P. pallidula guticolli Mulsant was recorded for the first time in the state of Nayarit. Previously it had been recorded in the states of Puebla and Veracruz (as Cycloneda rubida L.) (Coleoptera: Coccinellidae) by Gorham (1887–1899) and later by Trejo and Néstor (2012) for the state of Morelos. It is also noteworthy that 9 species were observed feeding on soursop in Mexico for the first time, because they are not included in the lists of previous authors (MacGregor & Gutiérrez 1983; Sánchez & Franco 2001; Ruiz et al. 2014; Vidal et al. 2014; Hernández et al. 2013, 2015; Cambero et al. 2017).

The entomofauna associated with soursop cultivation in the principal production area of Nayarit, Mexico, is very diverse, having a large number of phytophagous insects (20), as well as natural enemies such as parasitoids (5 species) and predators (12 species) that have the potential to naturally regulate the pest organisms associated with the crop. However, these natural enemies should be given more attention, because they could be part of biological control programs implemented for the management of the soursop pests.