New Eucalyptus (Myrtaceae) species host of Blastopsylla occidentalis (Hemiptera: Aphalaridae) and its parasitism by Psyllaephagus blastopsyllae (Hymenoptera: Encyrtidae) in Indonesia

Species Eucalyptus (Myrtaceae) baru yang menjadi inang Blastopsylla occidentalis (Hemiptera: Aphalaridae) dan parasitismenya oleh Psyllaephagus blastopsylla (Hymenoptera: Encyrtidae) di Indonesia

Abstract

Blastopsylla occidentalis Taylor (Hemiptera: Aphalaridae), native to Australia, causes damage to an increasing number of Eucalyptus (Myrtaceae) species and their hybrids in a growing number of countries. This is partly because predatory insects and spiders have low potential to reduce B. occidentalis populations. The purpose of this study was to report a new host of B. occidentalis and the parasitism of this insect by Psyllaephagus blastopsyllae Tamesse, Soufo, Tchanatame, Dzokou, Gumovsky, & Coninck (Hymenoptera: Encyrtidae) in Indonesia. Blastopsylla occidentalis nymphs parasitized were collected from five Eucalyptus pellita F. Muell. trees on October 3^rd, 2023, in Senoni, East Kalimantan, Indonesia, and reared in a laboratory until their adults or P. blastopsyllae emerged. The adults recovered from this parasitoid were identified by morphological analysis of their bodies. Eucalyptus pellita is a new host for B. occidentalis. This is the first time in Asia (Indonesia) that P. blastopsyllae has been reported. This new insect-host association alerts the world to the need to develop management strategies for B. occidentalis on E. pellita plantations. The recovery of P. blastopsyllae also opens up new perspectives for the development of biological control programs in Indonesia.

INTRODUCTION

The eucalyptus shoot psyllid Blastopsylla occidentalis Taylor (Hemiptera: Aphalaridae), native to Australia, feeds on Eucalyptus L’Hér. (Myrtaceae) (Demetriou et al., 2022) This insect is geographically distributed in all regions of Brazil, on the islands of Kalimantan and Sumatra in Indonesia, and in the states of California and Florida in the United States of America. It has been also reported in Algeria, Burundi, Cameroon, Egypt, Kenya, South Africa (Africa), Argentina, Chile, Mexico, Nicaragua, Uruguay (America), China, Hong Kong, Israel, Philippines, Turkey, Yemen (Asia), Cyprus, Italy, Malta, Portugal, Spain (Europe), and New Zealand (Oceania) (Queiroz DL et al., 2018);(Saliba et al., 2019) Blastopsylla occidentalis is spread through infested Eucalyptus spp. materials, but the introduction of this insect into new areas can be prevented through organism identification work in borders, as reported by the identification, at a species level, of several psyllid species in a port of entry in South Korea (S-J & D-S, 2020).

Blastopsylla occidentalis damages plants of all ages of Eucalyptus spp., with a greater number of individuals foraging on new leaves and the tips of younger ones, resulting in physical damage (distortion of leaves and tips) and loss of vigor (Floris et al., 2020) Infestation of Eucalyptus globulus Labill. by B. occidentalis reduces the growth and causes death of young plants in the nursery and field in African countries, including Cameroon (Soufo & Tamesse, 2015);(Dzokou et al., 2020) and Rwanda (Ivan & Takatoshi, 2019) This insect also makes Eucalyptus camaldulensis Dehnh. trees weaker and preferred by other psyllid species with greater damage potential, Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae) in Algeria(Kheddar et al., 2020) In addition, B. occidentalis reduces the wood productivity of Eucalyptus urophylla S.T. Blake and hybrids of E. urophylla × Eucalyptus grandis W. Hill. in areas with prolonged drought in Brazil due to an increase in the population of this insect (Burckhardt et al., 1999) In contrast, the infestation of Eucalyptus maidenii Muell. adult trees by B. occidentalis did not cause damage in Uruguay (Martínez et al., 2014) but reduced the production of Eucalyptus spp. inflorescences and seeds for genetic improvement programs and honey in the Mediterranean Basin (Floris et al., 2018) The hybrid E. urophylla × E. grandis and more than 10 Eucalyptus species have been reported as hosts of B. occidentalis, including E. camaldulensis, Eucalyptus forrestiana Diels, E. globulus, Eucalyptus gomphocephala DC., Eucalyptus microtheca F. Muell., Eucalyptus nichelii Maiden & Blakely, Eucalyptus oleosa F. Muell. ex Miq., Eucalyptus rudis Endl., and Eucalyptus spathulata Hook. (Soufo & Tamesse, 2015);(Joly et al., 2020) Blastopsylla occidentalis is controlled through different practices of integrated management such as the application of insecticides (Künast et al., 2020) and the conservation and/ or release of the parasitoid Psyllaephagus blastopsyllae Tamesse, Soufo, Tchanatame, Dzokou, Gumovsky, & Coninck (Hymenoptera: Encyrtidae) (Tamesse et al., 2014) This parasitoid lays its eggs on B. occidentalis nymphs, which become blackish as the host develops inside them; a new P. blastopsyllae adult emerges per nymph with potential to reduce the B. occidentalis population (Tamesse et al., 2014).

Psyllaephagus blastopsyllae has been reported in Algeria, Cameroon, Ethiopia, Rwanda, South Africa (Africa), and Brazil (America) (Tamesse et al., 2014); (Bush et al., 2016);(Adel-Sellami et al., 2020);(Künast et al., 2020) Although reports of P. blastopsyllae in Ethiopia and Rwanda do not refer to B. occidentalis (Ivan & Takatoshi, 2019);(Wondafrash et al., 2021) its occurrence is likely to occur in these countries. New reports confirming the presence of P. blastopsyllae in countries and host plants of B. occidentalis provide important information for the development of biological control programs and the selection of tolerant Eucalyptus clones, respectively (Joly et al., 2020);(Künast et al., 2021) The objective of this study was to report the first incidence of P. blastopsyllae in Asia and confirm the species name of its insect host. We also report a new species of Eucalyptus as a host for B. occidentalis.

METHODS

This study was conducted on a commercial plantation of Eucalyptus pellita F. Muell. and its hybrids in East Kalimantan, Indonesia at 00°16’56.57’’ to 00°39’10.78’’S, 116°24’59.00’’ to 117°00’18.92’’E, and an average of 70 m above sea level. Blastopsylla occidentalis was reported in this area for the first time in mid-2022, when it reached pest status (Burckhardt et al., 2024).

The collection of P. blastopsyllae to confirm its species identity was carried out as previously described. The three uppermost branches (around 50 cm long) of E. pellita were collected from five trees (around 1.70 m high) at 00°23’25.12’’S and 116°50’11.14’’E (tree 1), 00°23’25.24’’S and 116°50’11.52’’E (tree 2), 00°23’25.49’’S and 116°50’11.92’’E (tree 3), 00°23’25.75’’S and 116°51’52.27’’E (tree 4), and 00°23’25.91’’S × 116°52’11.01’’E (tree 5) within a 20-hectare stand on October 3 ^rd , 2023, in Senoni, East Kalimantan. This stand was planted for four days starting on May 17 ^th , 2023. Only plants with branches infested with at least one blackened (potentially parasitized) B. occidentalis nymph were selected. These branches collected were placed in 3 l capacity plastic bags filled with air and taken to a laboratory, where they were kept under incubation at 26.6 ± 4.0 °C and a 12:12 (L:D) h photoperiod until the emergence of B. occidentalis or parasitoids. Emerging parasitoids were collected from plastic bags using a brush and stored in 80% ethanol in Eppendorf ^® plastic vials (Hamburg, Germany).

Psyllaephagus blastopsyllae was identified through a morphological analysis of its adult body, followed by a comparison with a description by (Tamesse et al., 2014) and deposited at the National Collection of Insects, Biosystematics Division, Agricultural Research Council in Pretoria, South Africa (accession number: HYMT07333).

The number of B. occidentalis nymphs (blackish color) parasitized per branch in each plant and emergence rate (%) were assessed. Non-parasitized and parasitized nymphs (blackish color), another with the exit hole of the adult parasitoid, and adult females of P. blastopsyllae (pinned and foraging on E. pellita branches) were photographed with an HDL camera attached to an Olympus SZ2-ILST stereomicroscope manufactured by Olympus Corporation, Tokyo, Japan. To provide a compiled list of B. occidentalis natural enemies, a literature review was performed to identify all species reported per region in different countries.

RESULTS AND DISCUSSION

The present study reports the first occurrence of P. blastopsyllae in Asia (Indonesia), and its host species (B. occidentalis) was confirmed through two analyses: first, previous information on the existence of two psyllid species in Senoni, B. occidentalis and Platyobria drepanoides Burckhardt (Hemiptera: Aphalaridae); second, the possibility of differentiating the nymphs of these two species by analyzing their antenna features (Burckhardt et al., 2024) The psyllid species whose mummies presented an exit hole from parasitoid emergence was confirmed as B. occidentalis after analysis of its antenna features (B. occidentalis antenna is longer than that of P. drepanoides) (Figure 1 A−C) Psyllaephagus blastopsyllae, recovered in Indonesia in the current study, has been reported as an endoparasitoid (Künast et al., 2020) of fourth- and fifth-instar nymphs of B. occidentalis (Soufo & Tamesse, 2015) The adults of this insect emerge from the hosts through an exit hole in the upper part of the second half of the abdomen, as first illustrated and described in Cameroon (Tamesse et al., 2014) The origin of both P. blastopsyllae and its host B. occidentalis is likely to be the same in Australia (Künast et al., 2020).

Psyllaephagus blastopsyllae is easily identified by the naked eye when foraging on E. pellita branches infested by B. occidentalis in the field due to its high body mobility, wing movement, and characteristic dark color body (Figure 1 D−E) The parasitized nymphs and mummies of this psyllid were also easily observed (Figure 1 B−C) facilitating the determination of parasitism rate percentages in plantations. The current report on P. blastopsyllae adds Indonesia as the sixth country with confirmed occurrence of this insect Table 1 The identification of P. blastopsyllae from a collection in Indonesia opens up possibilities for its release into this country in areas with B. occidentalis with a low number or absence of natural enemies. The first report of B. occidentalis parasitized by P. blastopsyllae was in Cameroon (Tamesse et al., 2014) followed by a study reporting the presence of this parasitoid in South Africa, with populations high enough to keep those of its host under the control level (Bush et al., 2016) Psyllaephagus blastopsyllae and Psyllaephagus viridis Prinsloo are similar, differing in that the former has a scutellum more densely covered in pubescence (covered with 55 to 60 setae or more), the position of the toruli being below the lower eye margins, females with a shorter antennal scape (only 3.5 to 4.0 times longer than broad), and males with a shorter antennal scape (close by twice as long as broad) (Tamesse et al., 2014).

Figure 1.Nymphs of Blastopsylla occidentalis (Hemiptera: Aphalaridae) non-parasitized (A) and parasitized (B), parasitoid exit hole (C), and adult females of Psyllaephagus blastopsyllae (Hymenoptera: Encyrtidae), mounted (D) and foraging on Eucalyptus pellita (Myrtaceae) branches in the field (E).

This study also reports the first case of B. occidentalis hosted in E. pellita. All B. occidentalis stages (eggs, instar nymphs, and adults) and feeding were clearly observed on the plants. Psyllaephagus blastopsyllae is the only parasitoid of B. occidentalis reported to date. However, six groups of predators of this insect have been reported in Brazil, and one in Cameroon Table 2 The first report of B. occidentalis on E. pellita raises an alert for Eucalyptus spp. forest growers, as this plant species is one of the most planted in Indonesia, in addition to being used as a pollen source in genetic selection programs(Sinulingga et al., 2021) Psyllaephagus blastopsyllae recovered from B. occidentalis in seven countries was the main natural enemy of this psyllid because other natural enemies are generalist predators with a low potential to keep this psyllid population under control levels. These predators prefer to attack soft-bodied insects (aphids, mealybugs, thrips, whiteflies, etc.) rather than B. occidentalis when they occur simultaneously on the same Eucalyptusplant (Q & D, 2007);(Saliba et al., 2019).

Table 1.Reports of the natural parasitism of Blastopsylla occidentalis (Hemiptera: Aphalaridae) by Psyllaephagus blastopsyllae (Hymenoptera: Encyrtidae) per region in different countries

Country	Region	References
Algeria	Oued Smar, Algiers	(Adel-Sellami et al., 2020)
Brazil	Três Lagoas, Mato Grosso	(Künast et al., 2020)
	Mato Grosso do Sul
	Minas Gerais
	São Paulo
Cameroon	Yaounde	(Tamesse et al., 2014)
Ethiopia	-	(Wondafrash et al., 2021)
Indonesia	East Kalimantan	Present study
Rwanda	Bugesera, Gasabo and Rubavu Districts	(Ivan & Takatoshi, 2019) (Wondafrash et al., 2021)
South Africa	Buffelspoort, West of Pretoria	(Bush et al., 2016)

Table 2.Organisms reported as predators of Blastopsylla occidentalis (Hemiptera: Aphalaridae) per country

Predatory organisms	Order, Family	Country	References
Hover flies, including Allograpta exotica , Pseudodorus clavatus and Syrphus phaeostigma	Diptera, Syrphidae	Brazil	(Q & D, 2007)
Lacewings, including Chrysoperla spp.	Neuroptera, Chrysopidae	Brazil	(Q & D, 2007)
Ladybugs, including Cycloneda sanguinea , Eriopis connexa , Harmonia axyridis , Hippodamia convergens , and Olla v-nigrum	Coleoptera, Coccinellidae	Brazil, Cameroon	(Q & D, 2007) ;(Soufo & Tamesse, 2015)
Long-legged flies	Diptera, Dolichopodidae	Brazil	(Q & D, 2007)
Minute pirate bugs, including Anthocoris sp.	Hemiptera, Anthocoridae	Brazil	(Q & D, 2007)
Spiders	Araneae	Brazil	(Q & D, 2007)

Table 3. Mean (M) and total (T) of Blastopsylla occidentalis (Hemiptera: Aphalaridae) nymphs (N) parasitized by Psyllaephagus blastopsyllae (Hymenoptera: Encyrtidae) per branch (B) in a commercial stand of Eucalyptus pellita (Myrtaceae) in East Kalimantan, Indonesia

	Tree 1			Tree 2			Tree 3			Tree 4			Tree 5
	B 1	B 1	B 3	B 1	B 2	B 3	B 1	B 2	B 3	B 1	B 2	B 3	B 1	B 2	B 3
N	2	3	2	1	2	2	2	1	2	3	1	2	2	1	1
M	2.3			1.7			1.7			2.0			1.3
T	7			5			5			6			4

The number of B. occidentalis nymphs parasitized per tree was low at the collection time Table 3 but sufficient to obtain P. blastopsyllae parasitoid adults for species identity confirmation. The emergence rate was 100%, with 40% and 60% of the parasitoid individuals emerging within one or two days after field collection, respectively.

The occurrence of B. occidentalis in E. pellita alerts planted forest growers to implement integrated programs to control this insect. The report of nymphs of this insect parasitized by P. blastopsyllae in Indonesia opens up new perspectives for developing biological control activity initiatives.

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