The citrus blackfly, Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae), has been present in the Americas since 1913 after being reported in Jamaica (Ashby 1915). Citrus blackfly is a polyphagic pest that has more than 300 hosts, particularly citrus fruits, whose development is favored by temperatures ranging from 28 to 32 °C, and relative humidity between 70% and 80%. This pest does not survive at temperatures higher than 40 °C and feeds on plant sap, causing plant weakening and withering. In addition, excretion of sugary substances favors fungi development (mostly sooty mold) on leaves and fruits, damaging surfaces, which decreases their quality, resulting in higher economic losses (Nguyen & Hamon 1993).

Mexico grows 589,758 ha of citrus fruits, distributed in 24 states, with an estimated production of 8.2 million tons (SIAP-SADER 2017). It is the fifth largest citrus fruit producer in the world, representing a value of around USD $1,167 billion annually (SENASICA 2020). Citrus blackfly originally was found in the state of Sinaloa, Mexico, in 1935 (Myartseva 2005), where it is considered a secondary pest because it is found in population levels that do not represent economic distress due to introduced biological control agents, including the citrus blackfly parasitoid Encarsia opulenta (Silvestri) (Hymenoptera: Aphelinidae). This parasitoid originally was released in Mexico in 1971, in addition to the tiny parasitic wasp Amitus hesperidium (Silvestri) (Hymenoptera: Platygastridae), released earlier in Mexico (around the 1960s) (Smith et al. 1964; SENASICA 1999). However, populations of this insect pest increase or decrease due to climatic factors (Velázquez 1984) as well as indiscriminate application of chemical insecticides (Smith et al. 1964) that also affect parasitoid populations.

Amitus hesperidium was reported in 13 Mexican states (SENASICA 2020) in the mid-1920s. A report by SENASICA (2019) provided similar results for citrus blackfly control in Oaxaca, Chiapas, and Morelos states. After applying Moelleriella libera (formally known as Aschersonia cf. aleyrodis Webber) (teleomorph: Hypocrella libera) (Clavicipitaceae: Hypocreales) (Liu et al. 2006) in combination with the parasitoid wasps Encarsia perplexa Huang & Polaszek (Hymenoptera: Aphelinidae) and A. hesperidium, the citrus blackfly population was significantly reduced. The aim of the present study was to apply a simple technique to increase Aschersonia sp. distribution in orchards by collecting and spraying its conidia on citrus that are heavily infested with citrus blackfly nymphs to assess its potential for control in 1 Quintana Roo location.

In Aug 2018, after chemical application to control the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), the blackfly population increased among citrus orchards in high humidity areas of the Jose Maria Morelos locality in Quintana Roo, Mexico (19.7500°N, 88.7000°W) (Fig. 1a). Furthermore, in some orchards the entomopathogenic fungus Aschersonia sp. was detected along with this insect infecting citrus blackfly nymphs. Fungus conidia were collected from Aschersonia sp. infected nymphs (Fig. 1b) in a Petri dish, detaching the conidia from the cuticle with a previously sterilized needle (Fig. 1c) and transferring them to a 0.1% Tween 80 solution (Fig. 1d). To homogenize the conidia suspension, it was manually and vigorously shaken for 5 to 10 min. This conidia suspension was sprayed onto some shoots infested with uninfected citrus blackfly. For this, collected conidia were suspended in a 0.1% Tween solution at a concentration of about 1.0 × 10⁸ conidia per mL and sprayed on citrus blackfly nymphs uninfected by Aschersonia sp. (Fig. 1e). This suspension was applied manually by spraying with a portable backpack sprayer (Lola 15 L, Torke S.A. de C.V., Mexico City, Mexico) on 30 leaves infested with citrus blackfly nymphs until moist when relative humidity was about 95%. Tween (1%) solution was used as a control.

Between Oct and Nov 2018, and after detecting citrus blackfly population infesting other citrus orchards from the same region, we used the same technique to treat nymphs, collecting conidia from infected nymphs and spraying them with a motorized sprayer (Honda Wjr4025, Gx35, 1.0 kw, 4.0 mpa, ARISA Maquinaria S.A. de C.V., Mexico City, Mexico), where a single application of about 1.0 × 10⁸ conidia per mL was applied in 30 ha of a Jose Maria Morelos location in Quintana Roo until moist. During the application period, the average temperature was 23 °C with ≤ 95% relative humidity. In 2019, fungus conidia were not applied because we did not find a citrus blackfly pest population.

Fig. 1.

(a) Aschersonia sp. conidia application site, Jose Maria Morelos, Quintana Roo, Mexico; (b) selection of citrus blackfly nymphs infected with Aschersonia sp. from citrus leaves; (c) conidia extraction with a needle from infected nymphs; (d) conidia suspension; (e) selected citrus leaves with citrus blackfly nymphs uninfected with Aschersonia sp. for conidia application; (f) citrus blackfly nymph infection by Aschersonia sp. and mycelia development after fungus application in 30 leaves infested with citrus blackfly nymphs in Jose Maria Morelos locality at 7 d after application; (g) at about 55 d after application. Photographs provided by Cipriano Villarreal-Rizo.

Following application of fungal conidia in Aug 2018, citrus blackfly control was achieved by late Sep 2018, about 55 d after application, where fungi were disseminated to other individuals of this species present along untreated shoots (Fig. 1f & 1g). After the application of fungi in 30 ha in Jose Maria Morelos, Quintana Roo, an epizootic of citrus blackfly nymphs infected with Aschersonia sp. was detected, and this pest control method was assessed (Fig. 2a). The following year (2019), rain was scarce and the average relative humidity in this location was lower than 60%. We did not detect the pest nor the fungi. In Sep 2020, temperatures averaged 30 °C and relative humidity was about 80%, which increased the citrus blackfly population. We did not apply conidia despite detection of Aschersonia sp. Citrus blackfly biocontrol actually was achieved as in 2018, resulting in an epizootic, without further control application (Fig. 2b). Citrus blackfly adults and nymphs are phloem feeders, which cause direct damage to plants. In addition, indirect damage is caused by the presence of sooty mold on leaves, branches, and fruits. Damage affecting plants and fruits causes great economic losses.

Integrated pest management is a sustainable ecosystem-based approach for pest control that combines different management strategies to minimize chemical pesticide application and grow eco-friendlier crops (FAO 2020). The use of parasitoid wasps is a common procedure for citrus blackfly biological control (Hart et al. 1978; Nguyen et al. 1983; Huang & Polaszek 1998; Meagher & French 2004; White et al. 2005; SENASICA 2019). The entomopathogenic fungi Aschersonia cf. aleyrodis and Aegerita webberi Fawcett have been associated with citrus blackfly (Vieira Lima et al. 2017) but their application for biological control in the field is rare.

Aschersonia sp. conidia collection from infected nymphs, to be sprayed in citrus orchards to achieve citrus blackfly infection and control, represents a simple and inexpensive technique to reduce this pest population. By 2013, the citrus blackfly population significantly decreased in the Mexican states of Morelos (92% reduction), Oaxaca (77% reduction), and Chiapas (45% reduction) by using the parasitoids E. perplexa and A. hesperidium in combination with the fungus Aschersonia aleyrodis from orchards where they were present (SENASICA 2019).

In our study, we did not release any parasitoids but the pest population was significantly reduced after conidia application in field, where Aschersonia sp. led to an epizootic on citrus blackfly in 2018. In 2019, Aschersonia sp. conidia were not applied because the citrus blackfly population was rather low, probably due to environmental factors where the recorded temperature increased (higher than 35 °C) and the relative humidity decreased (lower than 60%). In 2020, after the citrus blackfly population recurred at higher numbers, when environmental conditions temperatures averaged 30 °C and relative humidity was higher than 80%, a second Aschersonia sp. epizootic infection of citrus blackfly nymphs was recorded at the same location of previously applied conidia. Based on the results reported for the region in 2020, fungus was still present in the sprayed area and became active again after citrus blackfly numbers increased. In summary, field results showed that it is possible to control citrus blackfly nymphs using a simple technique found to naturally control pests that may be used by citrus producers and biological control agents.

Fig. 2.

(a) Epizootic caused by Aschersonia sp. on citrus blackfly nymphs after conidia application on 30 ha in Jose Maria Morelos, Quintana Roo, Mexico (late Nov 2018); (b) presence of Aschersonia sp. on citrus blackfly nymphs (Sep to Nov 2020) without conidia application in Jose Maria Morelos, Quintana Roo, Mexico. Photographs provided by Cipriano Villarreal-Rizo.

We thank CONACYT-MEXICO for grant A1-S-33091 to OP-G. We also thank the Sistema Nacional de Investigadores (SNI-Conacyt, Mexico) for financial support through SNI-16614 to PT-G, SNI-9942 to RG-F, and SNI-73211 to OP-G compensations. Authors thank the technical support provided by Jorge Omar Uicab-Santos, Alberto Chan-Dzul, and David Joel Góngora-Xool from the State Committee for Plant Health (CESAVE) of Quintana Roo, Mexico, and for providing facilities and access to citrus orchards sampling and treatment.