Predation by Coccinellidae on Glycaspis brimblecombei (Hemiptera: Aphalaridae) eggs

Predação de ovos de Glycaspis brimblecombei (Hemiptera: Aphalaridae) por Coccinellidae

Abstract

Exotic Eucalyptus spp. are the most planted trees species in forest cultivation in Brazil. The red gum lerp psyllid Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), an invasive exotic pest, reduces the development and wood production of Eucalyptus spp. plantations. The search for natural enemies targeting the egg life stage is beneficial for the integrated pest management of G. brimblecombei. The objective of this work was to test a range of Coccinellidae species that potentially prey on G. brimblecombei eggs. Cycloneda sanguinea Linnaeus, Eriopsis conexa Germar, Harmonia axyridis Pallas, Hippodamia convergens Guerin-Meneville, Jaguarita conjugata Mulsant and Olla v-nigrum Mulsant (Coleoptera: Coccinellidae), reported to be associated with G. brimblecombei infestations, were evaluated. Newly emerged adults of O. v-nigrum and J. conjugata preyed on G. brimblecombei eggs, unlike C. sanguinea, E. conexa, H. axyridis and H. convergens. Predation of eggs by O. v-nigrum was highest, with a mean of 1,016 in 24 hours. These results, evaluating a range of Coccinellidae as predators of G. brimblecombei eggs, confirm the high predation rate of G. brimblecombei eggs by O. v-nigrum and that this ladybug may be important in the integrated management of this pest.

Keywords:
biological control; ladybugs; natural enemies; Olla v-nigrum; red gum lerp psyllid

Resumo

O gênero Eucalyptus ocupa a maior área plantada no setor florestal brasileiro com alta produtividade. O psilídeo de concha Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), praga exótica, reduz o desenvolvimento e produção de madeira nesses plantios. A busca de inimigos naturais para a fase de ovos de G. brimblecombei é essencial para complementar o manejo integrado e quebrar o ciclo da praga. O objetivo deste trabalho foi avaliar a predação de ovos de G. brimblecombei por seis espécies de Coccinelidae. A predação de ovos de G. brimblecombei por Cycloneda sanguinea Linnaeus, Eriopsis conexa Germar, Harmonia axyridis Pallas, Hippodamia convergens Guerin-Meneville, Jaguarita conjugata Mulsant e Olla v-nigrum Mulsant (Coleoptera: Coccinellidae), comumente associadas com infestações por essa praga, foi avaliada. Adultos recém emergidos de O. v-nigrum e J. conjugata predaram ovos de G. brimblecombei, mas isto não foi observado para C. sanguinea, E. conexa, H. axyridis e H. convergens. A predação de ovos, dessa praga, por O. v-nigrum foi maior em todas as avaliações, com 1.016 após 24 horas. Estes resultados são pioneiros na utilização de coccinelídeos no manejo de pragas do eucalipto. A maior predação de ovos de G. brimblecombei por O. v-nigrum indica que este predador pode ser importante para complementar o manejo integrado dessa praga.

Palavras-chave:
controle biológico; joaninha; inimigos naturais; Olla v-nigrum; psilideo-de-concha

1. Introduction

The area planted with Eucalyptus species is the largest in Brazil and with high productivity (Duarte and Ribeiro, 2023). The red gum lerp psyllid Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), an exotic pest with high invasive potential, has been reported in different countries in high infestations (Barbosa et al., 2023). This sap-sucking insect reduces the photosynthetic area and causes dryness of pointers and reduction of the development and wood production of Eucalyptus plantations (Del-Piero et al., 2022).

The integrated management of third and fourth instar G. brimblecombei nymphs is carried out using the parasitoid Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) (Favoreto et al., 2021), and for nymphs and adults of this insect, the predatory bug Atopozelus opsimus Elkins (Hemiptera: Reduviidae) (Dias et al., 2012), entomopathogenic fungi (Domingues et al., 2022) and chemical control (AGROFIT, 2024) are employed. Genetic resistance has limitations in managing G. brimblecombei due to its high adaptability to different plant hosts, as this pest damages most commercial clones used in Brazil (Dal-Pogetto et al., 2024). Identifying and utilizing egg predators could further enhance the effectiveness of integrated management strategies for G. brimblecombei.

Coccinellidae species prey on a wide range of pests (Zazycki et al., 2015; Li et al., 2021). Species of this family have been reported associated to native psyllids such as Triozoida sp. (Barbosa et al., 2003) and Psylla sp. (Hemiptera: Psyliidae) (Ferreira and Almeida, 2000), as well as to exotic species like Diaphorina citri Kuwayama (Hemiptera: Liviidae) (Michaud, 2001) and G. brimblecombei with Cycloneda sanguinea Linnaeus and Harmonia axyridis Pallas (Rodas-Ávalos et al., 2021). Given their association with G. brimblecombei and other similar pests, understanding their role in targeting specific developmental stages, such as eggs, is critical to enhance integrated pest management strategies. The objective of this study was to evaluate the predation of G. brimblecombei eggs by Coccinellidae species.

2. Materials and Methods

2.1. Glycaspis brimblecombei rearing

Glycaspis brimblecombei was reared on Eucalyptus urophylla saplings planted in 1-liter pots, housed in standardized cages with two plants each (40 cm × 45 cm × 80 cm), to collect its eggs (Wilcken et al., 2010). The rearing conditions included a controlled temperature of 25 ± 2 °C, relative humidity of 60 ± 10%, and a 13-hour photophase. Each cage received 80 to 100 G. brimblecombei adults, and saplings were replaced per cycle of this insect. Daily irrigation was performed using a 500 ml laboratory wash bottle (Domingues et al., 2022 adapted).

2.2. Predation assay of Glycaspis brimblecombei eggs by Coccinellidae

The predation of G. brimblecombei eggs was evaluated by the coccinellid species: Cycloneda sanguinea Linnaeus, Eriopsis conexa Germar, Harmonia axyridis Pallas, Hippodamia convergens Guérin-Méneville, Jaguarita conjugata Mulsant and Olla v-nigrum Mulsant (Coleoptera: Coccinellidae) was evaluated (Figure 1).

Figure 1
Adults of Cycloneda sanguinea (a), Eriopsis conexa (b), Harmonia axyridis (c), Hippodamia convergens (d), Jaguarita conjugata (e), Olla v-nigrum (f) (Coleoptera: Coccinellidae) evaluated for predation on Glycaspis brimblecombei (Hemiptera: Aphalaridae) eggs.

Branches of Eucalyptus urophylla, infested by G. brimblecombei and with coccinellid pupae, were collected in Suzano plantations in the Mato Grosso do Sul state, Brazil, and placed in standard rearing cages. The ladybug species were identified using identification keys (Vandenberg, 2002; Celli et al., 2021). Adults of these Coccinellidae were collected immediately after completing the pupal stage, identified, and individually placed in Petri dishes with ten replications (25 ± 2 °C, relative humidity of 60 ± 10%, and a 12-hour photophase), without sex separation.

Eucalyptus urophylla leaves, cut into disks with a diameter of 4 cm and with a known number of G. brimblecombei eggs (around 100 eggs) collected from a laboratory rearing, were provided in each dish, and the eggs were counted using a stereoscopic microscope. The leaves with G. brimblecombei eggs were replaced according to the predation by these insects. The number of eggs preyed was counted after one, two, three, four, five, six, seven and 24 hours. The data were subjected to ANOVA using the F-test and the means compared using Tukey's test (P≤0.05), all performed with the Minitab software (version 19) (Minitab, 2010).

3. Results

Newly emerged adults of O. v-nigrum and J. conjugata preyed on eggs of G. brimblecombei, unlike C. sanguinea, E. conexa, H. axyridis, and H. convergens. The predation of G. brimblecombei eggs by O. v-nigrum was higher in all evaluations (F = 375.47, p < 0.001), with an average of 1,016 eggs after 24 hours, while predation by J. conjugata started after four hours of evaluation (Table 1, Figure 2).

Table 1
Number of Glycaspis brimblecombei (Hemiptera: Aphalaridae) eggs preyed by Cycloneda sanguinea (Cs), Eriopsis conexa (Ec), Harmonia axyridis (Ha), Hippodamia convergens (Hc), Jaguarita conjugata (Jc) and Olla v-nigrum (Ov) (Coleoptera: Coccinellidae) during 24 hours after the emergence of adults of these predators.

Period (h)	Ov	Jc	Cs	Ec	Ha	Hc
1	39.0 ± 7.6	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
2	86.2 ± 11.5	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
3	131.1 ± 9.6	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
4	182.5 ± 12.6a	1.9 ± 1.3b	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
5	257.0 ± 14.6a	6.9 ± 4.6b	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
6	352.5 ± 21.0a	12.2 ± 8.1b	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
7	428.3 ± 26.6a	33.2 ± 14.4b	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0
24	1,016.0 ± 29.4a	167.7 ± 32.4b	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0	0.0 ± 0.0

• Means followed by the same lower-case letter, per line, do not differ by the Tukey test (p≤ 0.05).

Figure 2
Eucalyptus leaf before (a) and after (b) predation of Glycaspis brimblecombei (Hemiptera: Aphalaridae) eggs by Olla v-nigrum (Coleoptera: Coccinellidae).

4. Discussion

The reproductive system of newly emerged Coccinellidae adults is not fully mature, making feeding during the early life stages crucial. The predation rate during this period is essential for prey association and ovarian development, directly impacting future reproductive fitness (Osawa, 2005). This increases the importance of feeding for the ovarian development of these natural enemies (Hatt and Osawa, 2021).

The predation of G. brimblecombei eggs by O. v-nigrum and J. conjugata confirms reports of these natural enemies in infestations of native psyllids on Caesalpinia peltophoroides plants in Brazil (Machado, 1982) and that the eggs of these pests may be part of their diet in the field. Furthermore, O. v-nigrum has been reported in several South American regions, including some in Brazil (Silva et al., 2013), and even North America (Maffei et al., 2001). This is important and demonstrates that the insect is present naturally in different regions, making it possible to breed and release them in forest areas, as a biological control strategy, within Integrated Pest Management.

The lack of predation by C. sanguinea, E. conexa, H. axyridis, and H. convergens on G. brimblecombei eggs is related to these natural enemies preferring other prey, such as mites and aphids (Sarmento et al., 2007; Milléo et al., 2019; Rodríguez-Palomera et al., 2019). Their presence in G. brimblecombei infestations may be associated with other stages of this insect or other pests in the same area (Evans and England, 1996).

The reduced predation of G. brimblecombei eggs by J. conjugata, starting after four hours of evaluation, may be related to this food source not being ideal for the ovarian development of this natural enemy (Lima et al., 2020), and this resource may be secondary to maintaining the survival of this predator until finding suitable prey (Mercer et al., 2020).

The higher predation of G. brimblecombei eggs by adults of O. v-nigrum explains the frequent presence of this natural enemy in infestations of this pest (Sanchez-Martinez et al., 2005; Oliveira et al., 2010; Rodas-Ávalos et al., 2021), and this resource may be primary for the development of this predator, similar to what has been reported for Psylla sp. (Kato et al., 1999). Therefore, this natural enemy is important to reduce G. brimblecombei populations (Hoy, 2019). The development, oviposition, and viability of these natural enemies vary with the quality of prey, making them potential secondary sources for the maintenance of some Coccinellidae species.

5. Conclusions

The high predation of G. brimblecombei eggs by Olla v-nigrum indicates that this natural enemy is a promising alternative for the integrated management of this pest.

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.”.

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Publication Dates

• Publication in this collection
  12 May 2025
• Date of issue
  2025

History

• Received
  26 Aug 2024
• Accepted
  18 Mar 2025