Psyllaephagus brachiatus and Psyllaephagus sp. HH (Hymenoptera: Encyrtidae) in infestations of Glycaspis brimblecombei (Hemiptera: Aphalaridae) in Brazil

Psyllaephagus brachiatus e Psyllaephagus sp. HH (Hymenoptera: Encyrtidae) em infestações de Glycaspis brimblecombei (Hemiptera: Aphalaridae) no Brasil

Abstract

Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), a pest of Australian origin, has spread to many countries where it damages plants of the Eucalyptus genus. The parasitoid Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) is the most widely employed biological control strategy to manage this pest. The identification of Psyllaephagus species present in Brazil is essential, as they may compromise the effectiveness of the biological control of G. brimblecombei. The objective of this study was to report species of Psyllaephagus (Hymenoptera: Encyrtidae) in infestations of G. brimblecombei in Brazil. Psyllaephagus spp. adults were collected, identified, stored in 90% ethanol at -20°C, and identification verified by molecular methods. The DNA of the adult insects was extracted and amplified using the primers CP1 and CB2. The phylogenetic analysis confirmed the association of the parasitoid lineage found to Psyllaephagus brachiatus Riek and Psyllaephagus sp. HH (Hymenoptera: Encyrtidae) reported in Australia as heteronomous hyperparasitoids (autoparasitoids) with females developing in unparasitized psyllids and males in those parasitized by conspecific females or heterospecific parasitoids. The biology of these Psyllaephagus lineages and its impact as hyperparasitoids in their hosts in Brazil requires further studies. Psyllaephagus brachiatus and Psyllaephagus sp. HH, were identified for the first time in Brazil, and their detection in infestations of G. brimblecombei highlights the need to better understand their relationship with this pest and its parasitoid P. bliteus.

Keywords:
biological control; Eucalyptus; hyperparasitoids

Resumo

Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), uma praga de origem australiana, espalhou-se por diversos países onde causa danos às plantas do gênero Eucalyptus. O parasitoide Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) é a estratégia de controle biológico mais amplamente empregada para o manejo dessa praga. A identificação das espécies de Psyllaephagus presentes no Brasil é essencial, pois podem comprometer a eficácia do controle biológico de G. brimblecombei. O objetivo deste estudo foi relatar espécies de Psyllaephagus (Hymenoptera: Encyrtidae) em infestações de G. brimblecombei no Brasil. Adultos de Psyllaephagus spp. foram coletados, identificados, armazenados em etanol a 90% a -20 °C, e a identificação foi verificada por métodos moleculares. O DNA dos insetos adultos foi extraído e amplificado utilizando os primers CP1 e CB2. A análise filogenética confirmou a associação da linhagem de parasitoides encontrada a Psyllaephagus brachiatus Riek e Psyllaephagus sp. HH (Hymenoptera: Encyrtidae), relatados na Austrália como hiperparasitoides heterônomos (autoparasitoides), com fêmeas desenvolvendo-se em psilídeos não parasitados e machos naqueles parasitados por fêmeas coespecíficas ou por parasitoides heteroespecíficos. A biologia dessas linhagens de Psyllaephagus e seu impacto como hiperparasitoides em seus hospedeiros no Brasil requerem estudos adicionais. Psyllaephagus brachiatus e Psyllaephagus sp. HH foram identificados pela primeira vez no Brasil, e sua detecção em infestações de G. brimblecombei ressalta a necessidade de compreender melhor sua relação com essa praga e com o parasitoide P. bliteus.

Palavras-chave:
controle biológico; Eucalyptus; hiperparasitoides

1. Introduction

A wide variety of parasitoids are reported for Australian psyllids, including 245 valid species (Singh, 2016; Wu et al., 2021) of the cosmopolitan genus Psyllaephagus Ashmead (Steinbauer et al., 2014; Bush et al., 2020). In Australia, 57 Psyllaephagus species were identified as parasitoids or hyperparasitoids associated with psyllids only in Eucalyptus trees (Hollis, 2004). The structure of the antenna and head of males differentiates species of this genus, whereas females may be indistinguishable and difficult to identify. Therefore, in some cases, identification keys for these species are based on male characteristics (Riek, 1962; Myartseva et al., 2002). Psyllaephagus species can hyperparasitize primary species of the same genus (Trjapitzin, 1981; Berry, 2007; Hall et al., 2017).

Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), a pest of Australian origin, has spread to many countries where it damages plants of the Eucalyptus genus (Del-Piero et al., 2022). The parasitoid Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) is the most commonly used biological control agent to manage this pest (Favoreto et al., 2021; Cuello et al., 2021) and was detected parasitizing G. brimblecombei in Brazil in 2003, and considered as a fortuitous introduction (Berti-Filho et al., 2003); it was later intentionally introduced in 2006 (Wilcken et al., 2015). The identification of Psyllaephagus species present in Brazil is essential, as they may compromise the effectiveness of the biological control of G. brimblecombei. The objective of this study was to report species of Psyllaephagus (Hymenoptera: Encyrtidae) in infestations of G. brimblecombei in Brazil.

2. Materials and Methods

2.1. Collection and identification of Psyllaephagus sp.

Branches infested by G. brimblecombei from commercially grown eucalyptus trees were collected in plantations in the states of Mato Grosso do Sul, Minas Gerais, Paraná, and São Paulo Brazil (Table 1). These branches were taken to the laboratory and placed in pots with water in standard rearing cages until the emergence of insects. Adult Psyllaephagus sp. emerged from G. brimblecombei lerps were collected with the aid of a stereoscopic microscope, preserved in 90% ethanol at -20°C, and sent for molecular identification to the “Laboratório de Ecologia Molecular de Artrópodes, Departamento de Entomologia e Acarologia” of the Universidade de São Paulo (ESALQ/USP) in Piracicaba, São Paulo state, Brazil.

Table 1
Populations (Pop.), hosts, Eucalyptus grandis × Eucalyptus camaldulensis (E.g. × E.c.), E. grandis × Eucalyptus urophylla (E.g. × E.u.) and Eucalyptus urophylla (E.u.), latitude, longitude, place and year of collections (Year) of Psyllaephagus spp. (Hymenoptera: Encyrtidae) in the states of Mato Grosso do Sul (MS), Minas Gerais (MG), Paraná (PR) and São Paulo (SP) Brazil between 2018 and 2022.

Pop.	Hosts	Latitude	Longitude	Place	Year
1	E.g. x E.u.	-17.8164	-42.9006	Itamarandiba, MG	2018
2	E.g. x E.u.	-20.9999	-52.3514	Brasilândia, MS	2022
2	E.g. x E.u.	-21.0305	-51.9594	Três Lagoas, MS	2022
2	E.u.	-20.9792	-51.8647	Três Lagoas, MS	2022
2	E.u.	-20.6295	-51.6615	Três Lagoas, MS	2022
2	E.g. x E.u.	-21.0908	-51.9650	Três Lagoas, MS	2022
3	E.g. x E.c.	-23.7453	-50.7634	São Jerônimo da Serra, PR	2019
4	E.g. x E.u.	-22.4528	-48.9256	Agudos, SP	2019

2.2. Morphological identification

The males of Psyllaephagus of Mato Grosso do Sul state were identified, based on their morphology, and deposited in the “Coleção de Insetos Entomófagos “Oscar Monte” and in the Laboratório de Controle Biológico”, of the Instituto Biológico in Campinas, São Paulo state, Brazil, under the reference number IB-CBE-S-838. Morphological identification was performed only for insects from the Mato Grosso do Sul state lineage, using the key proposed by Riek (1962). Identification was performed in Brazil by the authors and confirmed by Dr. John S. Noyes through comparison with specimens at the Natural History Museum, London. The lineages collected from other states in 2018 and 2019 did not meet the necessary conditions for morphological identification.

2.3. Molecular analysis

DNA from a single adult male insect from the states of Mato Grosso do Sul, Minas Gerais, Paraná, and São Paulo Brazil was extracted using the Wizard Genomic DNA Purification Kit (Promega). A fragment of the mitochondrial cytochrome b (Cytb) gene was amplified using the primers CP1 (5’-GATGATGAAATTTTGGATC-3’) (Harry et al., 1998) and CB2 (5’-ATTACACCTCCTAATTATTAGGAAT-3’) (Jermiin and Crozier, 1994) via PCR with the following reagents: 0.8 µl dNTP (10 mM; Sinapse Inc.); 1.0 µl CP1 (5 µM); 1.0 µl CB2 (5 µM); 4.0 µl MgCl₂ (50 mM); 2.5 µl buffer (Mg²⁺ Free; Thermo Fisher Scientific); 10.5 µl milliQ water; 0.2 µl Taq polymerase (5 U/µl; Thermo Fisher Scientific); and 5 µl of individual DNA in a total volume of 25 µl per reaction. The PCR cycles consisted of initial denaturation at 95°C for three minutes; 35 cycles of denaturation at 95°C for 30 seconds, annealing at 47°C for 30 seconds, and extension at 72°C for two minutes; and a final extension at 72°C for 10 minutes. The PCR amplicons were visualized under ultraviolet light after electrophoresis using 5 µl of amplicon in a 1.5% v/v agarose gel. The amplified fragments were purified in the laboratory using Exo-Sap enzymes (Cellco Biotech) and sequenced bidirectionally by the Sanger method. The gene sequences were compared with the public database of the NCBI (National Center for Biotechnology Information). Evolutionary relationships between the sequenced specimens and database sequences were inferred using Bayesian phylogenetic analyses. The best-fitting evolutionary model was selected using MRMODELTEST v2.3 (Nylander, 2004). Bayesian phylogenetic trees were generated in MRBAYES using a 344 bp fragment of the cytochrome B gene from Psyllaephagus spp. lineages (Ronquist and Huelsenbeck, 2003). Four independent runs of 15 million generations were performed, each with one cold and three heated chains. The first 25% of sampled trees were discarded as burn-in, and a majority-rule consensus tree was constructed from the remaining trees, with nodes supported by posterior probabilities greater than 0.50.

3. Results

Specimens of the Mato Grosso do Sul (MS) lineage were morphologically identified as Psyllaephagus brachiatus Riek, 1962 (Hymenoptera: Encyrtidae) (Figure 1).

Figure 1
Male of Psyllaephagus brachiatus (Hymenoptera: Encyrtidae) associated with infestations of Glycaspis brimblecombei (Hemiptera: Aphalaridae) and identified using Riek's 1962 key.

The amplified and sequenced region from specimens of the Mato Grosso do Sul (MS) lineage was compared with the DNA barcoding database at NCBI. This analysis generated a consensus fragment of 699 bp showing 100% homology with the codes MN615707 and KU525267 of Psyllaephagus brachiatus (OQ718161). In contrast, specimens from Minas Gerais, Paraná, and São Paulo showed 100% homology with KU568437 of Psyllaephagus sp. HH (OQ789283, OQ789285, and OQ789266), a species yet to be formally described (Table 2).

Table 2
Population (Pop.), species, GenBank access code (AC), coverage (Cov.), identity (Ident.) and nearest GenBank access (Nearest AC) of Psyllaephagus brachiatus and Psyllaephagus sp. HH (Hymenoptera: Encyrtidae) collected in Glycaspis brimblecombei (Hemiptera: Aphalaridae) infestations in Mato Grosso do Sul (MS), Minas Gerais (MG), Paraná (PR) and São Paulo (SP) states, Brazil.

Pop.	Species	AC	Cov.	Ident.	Nearest AC
MS	Psyllaephagus brachiatus	OQ718160	46%	100%	KU525267
MS	Psyllaephagus brachiatus	OQ718161	45%	100%	KU525267
MS	Psyllaephagus brachiatus	OQ718162	60%	100%	KU525267
MG	Psyllaephagus sp. HH	OQ789283	88%	99,20%	KU568437
PR	Psyllaephagus sp. HH	OQ789285	88%	99,59%	KU568437
SP	Psyllaephagus sp. HH	OQ789266	88%	99,39%	KU568437

The phylogenetic analysis of a 344 bp fragment of the cytochrome B gene confirms the introduction of two species of Psyllaephagus in Brazil (Figure 2).

Figure 2
Bayesian phylogenetic tree for a 344 bp fragment of the cytochrome B gene from lineages of Psyllaephagus (Hymenoptera: Encyrtidae).

4. Discussion

The phylogenetic analysis indicated the introduction of two species of Psyllaephagus described as heteronomous hyperparasitoids in Brazil, with their biology not yet fully understood (Hall et al., 2017). The analysis confirmed the association of the lineage collected in Mato Grosso do Sul as P. brachiatus (Hall et al., 2017; Fromont, 2017) and those from Minas Gerais, São Paulo, and Paraná states as Psyllaephagus sp. HH, also described as heteronomous hyperparasitoids (Hall et al., 2017).

Psyllaephagus brachiatus, an Australian species, parasitizes Cardiaspina fiscella Taylor, 1962 on E. tereticornis and Glycaspis sp. on Eucalyptus spp. (Hemiptera: Aphalaridae) as a primary parasitoid (Riek, 1962; Hollis, 2004). In Australia, however, both P. brachiatus and Psyllaephagus sp. HH are reported as heteronomous hyperparasitoids, with females developing in unparasitized psyllids and males in psyllids previously parasitized by conspecific females or heterospecific species (Hunter and Kelly, 1998; Hall et al., 2017). In contrast, only two species of Psyllaephagus are considered typical hyperparasitoids: P. clarus and P. faustus (Hollis, 2004).

Psyllaephagus brachiatus was described in psyllids of the genera Cardiaspina and Spondyliaspis (Hall et al., 2017) and Mycopsylla (Fromont, 2017), indicating a generalist hyperparasitoid (Steinbauer et al., 2014). In Brazil, P. brachiatus is associated with the red gum lerp psyllid, G. brimblecombei, and P. bliteus, but also potentially native psyllid species due to its generalist habits.

The hyperparasitism reported in Australia for P. brachiatus and Psyllaephagus sp. HH (Hall et al., 2017) is similar to that reported for Coccophagus scutellaris Dalman (Hymenoptera: Aphelinidae) (Hunter and Woolley, 2001) and Encarsia pergandiella Howard (Hymenoptera: Aphelinidae) (Bográn and Heinz, 2002), as well as in some species of the families Encyrtidae and Ichneumonidae (Perevaryukha, 2020). The high competitiveness of heteronomous hyperparasitoids reduces the efficiency of primary parasitoids in classical biological control programs (Williams, 1996; Briggs and Collier, 2001; Bográn et al., 2002) in natural and agricultural environments (Tougeron and Tena, 2019), which underscores the importance of evaluating their impact on biological control and host organisms, including native species (Penagos and Williams, 1995; Loomans et al., 2002).

On the other hand, heteronomous hyperparasitoids are widely used in classical biological control programs due to their high potential to suppress pest populations when the efficiency of primary parasitoids is not adequate (Zhao et al., 2022). Understanding hyperparasitoid interactions is vital for sustainable pest control in Eucalyptus plantations. New Psyllaephagus species may reduce the effectiveness of managing G. brimblecombei, making it essential to study their relationship with this pest and its parasitoid P. bliteus.

Acknowledgements

To the Brazilian institutions “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Finance Code 001)”, “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)” and “Suzano S.A.” for financial support. To Prof. Alberto Soares Correa of the “Escola Superior de Agricultura “Luiz de Queiroz” of the Universidade de São Paulo” (USP)” and to Dr. John S. Noyes of the Natural History Museum, London, England for their assistance in identifying the Psyllaephagus species.

Data Availability Statement

The entire dataset supporting the results of this study was published in the article itself.

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• ZHAO, Y., ZHU, L., RAMIREZ-ROMERO, R., DAI, P., YANG, X., RUAN, C.C., DESNEUX, N. and ZANG, L.S., 2022. Mating status of an autoparasitoid and sex of the secondary host impact the outcome of heteronomous hyperparasitism. Entomologia Generalis, vol. 42, no. 1, pp. 87-99. https://doi.org/10.1127/entomologia/2021/1324
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Edited by

• Editor:
  Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  15 June 2026
• Date of issue
  2026

History

• Received
  30 Aug 2025
• Accepted
  27 Feb 2026