Parasitic wasps of the genus Tamarixia represent important biological control agents of members of the true bug group, Psylloidea, and are host specific; therefore, they can be used to control insect pests. In this study we report, for the first time, the presence of the parasitoid Tamarixia dahlsteni in Mexico and its mitochondrial barcode region of the cytochrome oxidase I gene (COI). We also review the species diversity of the genus Tamarixia in Mexico.

Biological control, COI, eugenia psyllid, parasitic wasps

Biological control agents represent a sustainable pest management option that help to maintain pest populations under accepted levels (Wang et al. 2019; Al-Ani et al. 2020). Parasitic wasps from the family Eulophidae represent a very important group of biological control agents as they have a wide range of insect hosts with different degrees of specialization. The genus Tamarixia Mercet represents one example of parasitoids with a high degree of host specificity (Urbaneja-Bernat et al. 2019). Most species act as ectoparasitoids, but in some cases endoparasitism has been reported (Noyes 2022). Species of the genus Tamarixia parasitize free-living and gall-forming species of true bugs, Psylloidea. It was proposed that they reached this host restriction through a specialization on their host (LaSalle 1994), although the species has also been reported parasitizing aphids (Zuparko et al. 2011). According to the Universal Chalcidoidea database, the genus Tamarixia comprises 54 species to date, which are distributed worldwide (Noyes 2022).

In Mexico, five species (both native and exotic) of Tamarixia are found: Tamarixia aguacatensis Yefremova (Yefremova et al. 2014), Tamarixia leucaenae Boucek (McClay 1990), Tamarixia radiata (Waterston) (González-Hernández et al. 2009), Tamarixia schina Zuparko (Zuparko et al. 2011), and Tamarixia triozae (Burks) (Lomelí-Flores and Bueno 2002). Some of these species have already been part of integrated pest management strategies with remarkable results. For instance, T. triozae, the parasitoid of the potato psyllid Bactericera cockerelli, was introduced to New Zealand for the biological control of the psyllids that vector the bacterium Candidatus Liberibacter solanacearum (CLso) (Workman and Whiteman 2009). This bacterium has been linked to different diseases in plants of the nightshade family Solanaceae (Munyaneza et al. 2007). In Mexico, T. triozae was found naturally in tomato crops and, according to parasitism evaluation, the percentage of parasitism reached by T. triozae on B. cockerelli has been up to eighty percent when insecticides are not used to control the psyllid populations (Lomelí-Flores and Bueno 2002). Tamarixia triozae is commercially available in Mexico through Koppert Mexico, and several studies have been carried out on its biological cycle (Rojas et al. 2015), its release into the environment either individually or in combination with other natural enemies for the control of B. cockerelli (Cerón-González et al. 2014; Ramírez-Ahuja et al. 2017). Other examples of Tamarixia species used for biological control are T. schina, which was introduced in California for the control of Calophya schini Tuthill (Psyllidae: Calophyidae), T. dahlsteni Zuparko, which was introduced for the control of Trioza eugeniae Froggatt (Hemiptera: Triozidae) (Zuparko et al. 2011) and T. radiata. The latter is native to Pakistan (Chen and Stansly 2014), but has been introduced into countries such as Taiwan, the United States and France (Guadeloupe), to control populations of the psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae), a vector of the bacterium Candidatus Liberibacter asiaticus (Chien et al. 1989; Michaud 2002; De León and Sétamou 2010). In Texas, a reduction of more than ninety percent of D. citri populations has been observed in regions where T. radiata was released (Flores and Ciomperlik 2017). In Mexico, the parasitoid was reported as an accidentally introduced species (De León and Sétamou 2010).

Currently, DNA barcodes are important tools for species identification with potential for bio-surveillance programs in agriculture (Ashfaq and Hebert 2016). DNA barcodes have been useful to identify important arthropod pests even at immature stages (Ashfaq and Hebert 2016). The common barcoding method used for animal identification is based on the sequencing of a part of the mitochondrial gene cytochrome oxidase subunit I (COI). COI has been used to create universal and public databases of sequences, such as the Barcode of Life Data System (BOLD), which includes agriculturally important insect sequences (Hebert et al. 2003). In this regard, here we report the occurrence of T. dahlsteni in Mexico for the first time, and the first mitochondrial cytochrome oxidase subunit one (COI) sequences for this species. We also discuss the potential of additional species of Tamarixia in Mexico.

According to the literature, seven of the 54 existing species of Tamarixia are reported from the Nearctic and Neotropical regions (Noyes 2022). Mexico spans both regions and, following this study, the number of Tamarixia species was updated to six. In addition, our phylogenetic analysis suggested the COI barcoding region to be a useful molecular marker for the distinction of Tamarixia species. The phylogeny obtained suggested intraspecific genetic structure for some of the species, which unveils the necessity of robust and wider phylogenetic analysis at the genus level.

The host for T. dahlsteni is the eugenia psyllid Trioza eugeniae. Both species were found in Australia associated with the ornamental tree Syzygium paniculatum, and in 1988 the psyllid was found for the first time in California, USA. The damage caused by the psyllid on S. paniculatum trees prompted a search for its natural enemies in Australia. As a result, the wasp T. dahlsteni was identified as the primary parasitoid of T. eugeniae and was later imported to the USA to control eugenia psyllid populations (Dahlsten et al. 1993). A similar case is the one of Tamarixia schina. The wasp was reported as a natural enemy of the exotic psyllid Calophya rubra (Blanchard) which feeds on Schinus molle trees (Álvarez-Zagoya and Cibrián-Tovar 1999). According to Zuparko et al. (2011), new undescribed Tamarixia species were found in both California and Florida, USA, parasitizing psyllid species which have potential distribution in Mexico.

In biological research, names of species are essential to ensure comparable results when working with model organisms (Pante et al. 2015), and in agriculture they are also required for biosecurity and quarantine concerns (Lyal et al. 2008). Notwithstanding, in some cases species identification is not an easy task and deep taxonomic studies are needed. For instance, in 2019 the misidentification of the eugenia psyllid T. eugeniae was uncovered by Taylor and Martoni (2020), who indicated that the true name of the species should be Trioza adventicia Tuthill. Taylor and Martoni mentioned that the two exotic species resemble each other, and only a detailed study based on a series of morphological characters and DNA barcoding supported the separation and validity of both species.

As already mentioned, psyllids are main hosts for the Tamarixia species and because of their possible broad dietary tolerance some species might migrate and disperse to new geographic regions (Percy et al. 2012). This might also promote the introduction and dispersion of exotic or new species of parasitoids in countries like Mexico. For example, T. schina apparently migrated to Mexico from California (Yefremova et al. 2014). According to the study by Percy et al. (2012), in the same region (California, USA), different species of psyllids attacked by some unidentified Tamarixia species exist, hosted by plants with potential distribution in Mexico. Moreover, in this country more than 114 species of psyllids (Méndez-Tobar 2015) exist, which may also represent possible hosts for exotic Tamarixia species. Therefore, the diversity of this genus might be currently underestimated in Mexico.

In agriculture, species identification protocols based on DNA represent powerful tools for the success of early detection programs, or monitoring of species (Lyal et al. 2008; Boykin et al. 2012; Poland and Rassati 2019). However, for some groups of insects, the lack of reference barcodes, errors in databases, scarcity of voucher specimens and presence of cryptic species represent strong limitations. As an example, recently a new Tamarixia species (T. aguacatensis) was described based on morphological characters, but because their sampling seems to be seasonally restricted (Yefremova et al. 2014), the generation of barcodes for further studies on their biology and phylogeny represents a challenge.

Besides reporting the presence of Tamarixia dahlsteni in Mexico, we also provided barcodes that may be employed as a reference for further monitoring programs or studies about this economically important group of wasps. Moreover, our phylogenetic analysis suggests the need for a deeper and wider taxonomic revision of the genus.

The authors are grateful to Dave Burns and Laurie Jo Elliot for providing English editing of the manuscript.