Hyperparasitoids of Xenostigmus bifasciatus (Hymenoptera: Braconidae), parasitoid of Cinara spp. (Hemiptera: Aphididae), in Pinus plantations in BrazilAbstract
Hyperparasitoidism can reduce the biological control of Cinara spp. (Hemiptera: Aphididae) in Pinus (Gymnospermae: Pinaceae) plantations in Brazil. Cinara atlantica (Wilson, 1919) and Cinara pinivora (Wilson, 1919), introduced into Brazil in the 1990s, damage young Pinus plants. The primary parasitoid Xenostigmus bifasciatus (Ashmead, 1891) (Hymenoptera: Braconidae) was introduced and released between 2002 and 2004 in the states of Paraná, Santa Catarina, and São Paulo, Brazil. The dispersion of this biological control agent was extensive, with parasitoidism near 100%, stabilizing Cinara spp. populations for years, however, the population increase of these aphids in Pinus taeda (Linnaeus, 1753) plantations up to 2.5 years old between 2022 and 2025 suggests a reduction in the efficiency of biological control. Eight hundred and eighty-four mummies of Cinara spp. were collected from commercial plantations in Santa Catarina and reared in laboratory, from which 203 Hymenoptera specimens emerged, including 24 (11.82% of the total mummies collected) of X. bifasciatus and 179 (88.18%) of the hyperparasitoids Asaphes californicus Girault, 1917 (Hymenoptera: Chalcidoidea: incertae sedis) (55.17%); Dendrocerus carpenteri (Curtis, 1829) (Hymenoptera: Megaspilidae) (10.80%); D. ramicornis (Boheman, 1832) (Hymenoptera: Megaspilidae) (9.90%); and Euneura sopolis (Walker, 1844) (Hymenoptera: Pteromalidae) (12.31%). This is the first record of D. ramicornis and the four species associated with Cinara spp. in P. taeda in Brazil. The high incidence of hyperparasitoidism may be the main cause of the reduced efficiency of Cinara spp. biological control in Pinus plantations in southern Brazil by X. bifasciatus.
Keywords:
Asaphes californicus; biological control; Dendrocerus spp.; Euneura sopolis; hyperparasitoidism; Pinus taeda
Resumo
O hiperparasitoidismo pode reduzir o controle biológico de Cinara spp. (Hemiptera: Aphididae) em plantações de Pinus (Gymnospermae: Pinaceae) no Brasil. Cinara atlantica (Wilson, 1919) e Cinara pinivora (Wilson, 1919), introduzidas no Brasil na década de 1990, causam danos a plantas jovens de Pinus. O principal parasitoide, Xenostigmus bifasciatus (Ashmead, 1891) (Hymenoptera: Braconidae), foi introduzido e liberado entre 2002 e 2004 nos estados do Paraná, Santa Catarina e São Paulo, Brasil. A dispersão desse agente de controle biológico foi extensa, com parasitoidismo próximo a 100%, estabilizando as populações de Cinara spp. por anos, entretanto, o aumento populacional desses pulgões em plantações de Pinus taeda (Linnaeus, 1753) com até 2,5 anos de idade entre 2022 e 2025 sugere uma redução na eficiência do controle biológico. Oitocentas e oitenta e quatro múmias de Cinara spp. foram coletadas em plantações comerciais em Santa Catarina e criadas em laboratório, das quais emergiram 203 espécimes de Hymenoptera, incluindo 24 (11,82% do total de múmias coletadas) de X. bifasciatus e 179 (88,18%) dos hiperparasitoides Asaphes californicus Girault, 1917 (Hymenoptera: Chalcidoidea: incertae sedis) (55,17%); Dendrocerus carpenteri (Curtis, 1829) (Hymenoptera: Megaspilidae) (10,80%); D. ramicornis (Boheman, 1832) (Hymenoptera: Megaspilidae) (9,90%); e Euneura sopolis (Walker, 1844) (Hymenoptera: Pteromalidae) (12,31%). Este é o primeiro registro de D. ramicornis e das quatro espécies associadas a Cinara spp. em P. taeda no Brasil. A alta incidência de hiperparasitoidismo pode ser a principal causa da reduzida eficiência do controle biológico de Cinara spp. em plantações de Pinus no sul do Brasil por X. bifasciatus.
Palavras-chave:
Asaphes californicus; controle biológico; Dendrocerus spp.; Euneura sopolis; hiperparasitoidismo; Pinus taeda
1. Introduction
The giant conifer aphids, Cinara pinivora (Wilson, 1919) and Cinara atlantica (Wilson, 1919) (Hemiptera: Aphididae), were first recorded in Brazil in 1996 and 1998, respectively, damaging Pinus spp. plants (Penteado et al., 2000, Lazzari et al., 2004; Oliveira et al., 2004, Oliveira et al., 2025). These aphids, native to the United States and Canada, are not considered pests in those countries (Lemes and Zanuncio, 2021).
The management of C. atlantica and C. pinivora in Pinus spp. plantations in Brazil was based on different strategies, mainly the introduction and release of the parasitoid Xenostigmus bifasciatus (Ashmead, 1891) (Hymenoptera: Braconidae). Between 2002 and 2004, from the southeastern United States in Pinus plantations in the states of Paraná, Santa Catarina, and São Paulo, Brazil (Reis Filho et al., 2004; Penteado, 2007; Cunha et al., 2016). One year after release, X. bifasciatus was detected in all areas of its introduction, with dispersal up to 80 km from the release sites and parasitism rates of up to 100%, effectively reducing Cinara populations (Reis Filho et al., 2004).
Cinara spp. populations increased in P. taeda plantations up to 2.5 years old in the states of Santa Catarina and Paraná between 2022 and 2025, two decades after the release of X. bifasciatus (Personal communication: Klabin technical team).
The objective was to evaluate the parasitism rates of C. atlantica by X. bifasciatus and the occurrence of hyperparasitoids in P. taeda plantations in the state of Santa Catarina, Brazil.
2. Materials and Methods
The study was conducted in October and November 2025 in commercial P. taeda plantations in municipalities of the state of Santa Catarina, Brazil (Table 1).
Total emergence (TE) of the parasitoid Xenostigmus bifasciatus (Hymenoptera: Braconidae) (Xb) and hyperparasitoids Asaphes californicus (Hymenoptera: Chalcidoidea: incertae sedis) (Ac), Dendrocerus carpenteri (Hymenoptera: Megaspilidae) (Dc), Dendrocerus ramicornis (Hymenoptera: Megaspilidae) (Dr) and Euneura sopolis (Es) (Hymenoptera: Pteromalidae) from mummies of Cinara spp. (Cspp) collected in Pinus taeda plantations in different municipalities of the state of Santa Catarina, Brazil. Oct-Nov, 2025.
Laboratory analyses and specimen rearing were carried out at the Forest Protection Laboratory of the Center for Agroveterinary Sciences (CAV), Santa Catarina State University (UDESC), in Lages, Santa Catarina, Brazil.
Eight hundred and eighty-four mummies of the giant conifer aphids, Cinara spp., were collected. Sampling was distributed at a ratio of one point per 300 hectares, covering plantations aged between eight and thirty months. Twenty plants were evaluated at each sampling point, with the complete removal of all mummies found. This age range was selected because it represents the period of greatest vulnerability of Pinus spp. plants to attack by Cinara spp. (Fox and Griffith, 1977; Penteado et al., 2000).
Needles bearing these mummies were placed in plastic containers covered with mesh/voil, kept in a climate-controlled chamber (BOD) at a constant temperature of 25 ± 1 °C, and checked daily for parasitoid emergence.
Live aphid specimens were preserved in 70% ethanol and identified (Blackman and Eastop, 1994).
Parasitoids, immediately after emergence, were preserved in 70% ethanol, mounted, and identified as Asaphes californicus Girault, 1917 (Hymenoptera: Chalcidoidea: incertae sedis) (Gibson and Vikberg, 1998; Li et al., 2024); Dendrocerus carpenteri (Curtis, 1829) and D. ramicornis (Boheman, 1832) (Hymenoptera: Megaspilidae) (Dessart, 1999; Pezzini et al., 2014); and Euneura sopolis (Walker, 1844) (Hymenoptera: Pteromalidae) (Ko et al., 2018; Lee et al., 2019).
Voucher specimens of aphids and parasitoids are deposited, respectively, in the Entomological Collection of Santa Catarina State University (Lages, SC) and in the Entomological Collection of the Federal University of Espírito Santo (Vitória, ES).
3. Results
Two hundred and three Hymenoptera specimens emerged from aphid mummies (Table 1).
Twenty-four (11.82%) of the specimens emerged from the mummies were X. bifasciatus, a primary and solitary parasitoid of Cinara spp. The individuals emerged from the remaining 179 (88.18%) mummies belonged to four species of aphid Hymenoptera hyperparasitoids, namely 112 (55.17%) specimens of A. californicus; 22 (10.80%) of D. carpenteri; 20 (9.90%) D. ramicornis; and 25 (12.31%) of E. sopolis (Table 1).
4. Discussion
The maintenance temperature of Cinara spp. mummies (25 ± 1 °C) may have affected the emergence of the different species because the development of Asaphes spp. and Dendrocerus spp. is better under milder thermal conditions (De Boer et al., 2019). Besides, thermal stress reduces the biological fitness of Dendrocerus spp., directly affecting fecundity (Buitenhuis et al., 2017; Mitsunaga et al., 2014), with reports of a 50% reduction in the progeny of D. carpenteri from different hosts between 19 °C and 20 °C (Walker and Cameron, 1981).
Asaphes californicus (Figure 1) is a generalist hyperparasitoid of primary aphid parasitoids, such as Aphidiinae (Braconidae) and Aphelinidae species. The distribution of this species extends along the west coast of North America, South America, and China. Its females oviposit on the bodies of late-instar larvae, prepupae or pupae of primary aphid parasitoids and develop as ectophagous and solitary pseudohyperparasitoids (Gibson and Vikberg, 1998).
The sampled specimens treated as A. californicus sensu (Gibson and Vikberg, 1998) is because its diagnostic features are similar to those of A. vulgaris (Walker, 1834) and A. suspensus (Nees, 1834) (Hymenoptera: Chalcidoidea: incertae sedis), such as yellow hind trochanters and darkened tibiae in females, and the outer surface part of the antennal scape of males bears a subbasal, ovoid to elongate-lanceolate, microsetose sensory region (Gibson and Vikberg, 1998). Furthermore, all Asaphes specimens collected in South America (Argentina, Bolivia, Chile, Colombia, Ecuador, Uruguay, and Venezuela) are A. californicus; therefore, previous records of A. vulgaris for South America refer to the former species (Gibson and Vikberg, 1998). Records of A. vulgaris in Brazil (De Santis, 1960) should also be treated as A. californicus, indicating that this species was already present in Brazil before 1968.
The genus Dendrocerus is cosmopolitan, comprising about 120 species, some of which are ectophagous aphid hyperparasitoids, including D. carpenteri, (Figure 2 a, c, d) recorded on all continents except Antarctica (Fergusson, 1980). This species has been recorded in Brazil and Chile (Dessart, 1975; Tavares, 1996) as a pseudohyperparasitoid of aphids (it lays eggs on the primary host after the aphid has been consumed) and has been associated with many aphid species and their primary and secondary parasitoids, including Asaphes and Pachymeuron (Hymenoptera: Pteromalidae) (Fergusson, 1980; Masner, 2006). The distribution of D. ramicornis (Figure 2 b, d and f) is Holarctic and associated with Lachininae aphids (Hemiptera: Aphididae), mainly species of Cinara and Lachnus (Fergusson, 1980). Dendrocerus carpenteri and D. ramicornis differ in the shape of antennae (mainly in males) and of the notaulices (both sexes). Males of D. carpenteri present the five basal flagellomeres triangular in profile (Figure 2 c), as in a serrate antennae. In D. ramicornis, males present each of the five basal flagellomeres with a long process dorsally (Figure 2 d) and all process of similar length. The notauli of the former species are distinctly convergent posteriorly and meet each other at the mesoscutal margin (Figure 2 e), but in D. ramicornis notauli are slightly convergent and reach the mesoscutal margin far from it other (Figure 2 f).
Dendrocerus capenteri (a, c, d) and D. ramicornis (b, d, f): habitus (a, b), antennae (c, d) and mesoscutum (e, f). The arrows indicate the notaulus.
Euneura sopolis (Figure 3), with records from Europe, Korea, and Japan, appears to have an original Palearctic distribution (Lee et al., 2019). This parasitoid has been recorded in southeastern Brazil (Cunha et al., 2016), associated with species of Pauesia Quillis, 1931 (Hymenoptera: Aphidiidae) and Xenostigmus (Garrido Torres and Nieves-Aldrey, 1999), which are primary parasitoids of aphids of the family Lachnidae (Cunha et al., 2016).
Several species of primary and secondary parasitoids of C. atlantica emerged during the quarantine process for the introduction of X. bifasciatus into Brazil, in 2002. The aphid mummies were shipped from the United States and the parasitoid emerged were: X. bifasciatus and Diaeretus sp. (Foerster, 1862) (Hymenoptera: Aphiididae); Alloxysta lachni (Ashmead, 1885) (Hymenoptera: Figitidae), Anastatus sp. Motshulsky (Hymenoptera: Eupelmidae); Asaphes suspensus (Hymenoptera: Chalcidoidea: incertae sedis); Dendrocerus sp. (Megaspilidae); Euneura lachni and E. sopolis (Pteromalidae); Syrphophagus sp. Ashmead (Hymenoptera: Encyrtidae); and Tetrastichus sp. Haliday, 1844 (Hymenoptera: Eulophidae). Specimens of contaminant species were destroyed during quarantine, and only X. bifasciatus was released, between 2002 and 2004, for the control of Cinara spp. in the states of São Paulo, Paraná, and Santa Catarina (Penteado et al., 2004).
Among the hyperparasitoid species obtained here, A. californicus and D. carpenteri were present in Brazil before the introduction of X. bifasciatus; E. sopolis was reported in the country more than 10 years after this introduction. D. ramicornis is here recorded for the first time. This suggests that these latter two hyperparasitoid species, like Cinara spp., were introduced accidentally. On the other hand, these hyperparasitoids may have been introduced by natural dispersal, since their aphid hosts have been recorded in countries neighbouring Brazil, such as Argentina and Uruguay (Penteado et al., 2000), and these aphids and their hyperparasitoids are native to or have long been present in North America (Gibson and Vikberg, 1998).
The low emergence rate of X. bifasciatus, the main biological control agent of Cinara spp., and the high emergence rate of hyperparasitoids apparently limit the effectiveness of classical biological control of these aphids in Pinus plantations in Brazil. Surveys on the occurrence of these hyperparasitoids should be conducted in the states of Paraná and São Paulo, as well as in neighboring countries, since the resurgence of giant conifer aphids as major pests in Pinus plantations in the coming years is likely.
5. Conclusion
This is the first report of the hyperparasitoids A. californicus, D. carpenteri, D. ramicornis, and E. sopolis associated to Cinara species in P. taeda plantations in Brazil and of D. ramicornis in South America.
Acknowledgements
The authors thank Klabin S/A for the technical support during material collection and “Programa Cooperativo sobre Proteção Florestal (PROTEF) of the Instituto de Pesquisas e Estudos Florestais (IPEF)” for financial assistance.
Data Availability Statement
The entire data set that supports the results of this study was published in the article itself.
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Editor:
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