Research Article |
Corresponding author: Agustin Zarkani ( agustinzarkani@unib.ac.id ) Academic editor: Takumasa Kondo
© 2023 Agustin Zarkani, Ariffatchur Fauzi, Dwinardi Apriyanto, Mehmet Bora Kaydan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Zarkani A, Fauzi A, Apriyanto D, Bora Kaydan M (2023) Mealybugs (Hemiptera, Coccomorpha, Pseudococcidae) on parasitic plants (Loranthaceae) in Indonesia with description of a new species and a new country record. ZooKeys 1167: 199-210. https://doi.org/10.3897/zookeys.1167.106012
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Parasitic plants have been known to be attacked by insect pests since ancient times. However, little is known about the mealybug (Hemiptera, Coccomorpha, Pseudococcidae) fauna associated with them. A series of surveys of mealybugs found on Loranthaceae, a semi-parasitic plant family, was conducted in several places in Bengkulu Province, southern Sumatra, Indonesia. In the study, 55 mealybug specimens were collected, consisting of eight species belonging to five genera, namely Chorizococcus McKenzie (1 species), Dysmicoccus Ferris (2 species), Ferrisia Fullaway (1 species), Planococcus Ferris (3 species) and Pseudococcus Westwood (1 species). Chorizococcus ozeri Zarkani & Kaydan, sp. nov. is new to science, whilst Planococcus bagmaticus Williams represents the first record in Indonesia. In addition, the mealybugs Dysmicoccus lepelleyi (Betrem), Dysmicoccus zeynepae Zarkani & Kaydan, Ferrisia dasylirii (Cockerell), Planococcus lilacinus (Cockerell) and Pseudococcus jackbeardsleyi Gimpel & Miller are newly recorded from plants of the family Loranthaceae. Figures and illustrations of mealybug species with a taxonomic key to Asian Chorizococcus and a new country record based on morphological characters are also updated.
Biodiversity, identification key, new record, parasitic plant, pests, Sternorrhyncha, taxonomy
Loranthaceae is a primitive family of parasitic plants which are photosynthetic xylem feeders and cannot exist independently of the host plant (
Just as non-parasitic plants have been attacked by insect pests for many generations, parasitic plants have also been known to be attacked by insect pests since ancient times. However, little information about the mealybug fauna (Hemiptera, Coccomorpha, Pseudococcidae) associated with parasitic plants is known. According to the scale insect database ScaleNet (url:scalenet.info/), 18 species of mealybugs (Hemiptera, Pseudococcidae) have been reported to be associated with Loranthaceae worldwide, namely Anisococcus parasitus Williams & Granara de Willink, Coccidohystrix insolita (Green), Dysmicoccus ambiguous (Morrison), Dysmicoccus debregeasiae (Green), Dysmicoccus viticis (Green), Erioides rimulae Green, Exallomochlus hispidus (Morrison), Macrocepicoccus loranthi Morrison, Nipaecoccus kosztaraborum Williams & Granara de Willink, Nipaecoccus nipae (Maskell), Paraputo loranthi (Matile-Ferraro), Planococcus bendovi Williams, Planococcus kenyae (Le Pelley), Porococcus coxatus Ferris, Porococcus pergandei Cockerell, Porococcus tinctorius Cockerell, Pseudococcus comstocki (Kuwana) and Pseudococcus viburni (Signoret) (
For decades, the study of parasitic plants focused mainly on genetic variability, chemical contents, and their impact on their host plants. In this study we report several species of mealybugs found on Loranthaceae in Indonesia and provide an updated list of parasitic plant-feeding scale insects in the world. These specialized pests could be evaluated as natural control agents of parasitic plants in the future.
Adult mealybug females were collected from a series of sampling occasions on leaves, trunk, and branches of Loranthaceae trees in Bengkulu Province, southern Sumatra, Indonesia from March to December 2022. The sampling sites are at an altitude of 0–1100 m above sea level. The specimens were mounted and preserved in slides and identified to genus level. The slide mounting was carried out under a binocular dissection microscope, LEICA EZ4HD by using the method described
Species identifications were made by observing the specific features of the mealybug species using a phase-contrast compound microscope (LEICA DM2700) and were identified using the keys in
A series of surveys carried out in southern Sumatra on Loranthaceae resulted in the collection of 55 mealybug specimens consisting of eight species belonging to five genera. The identified species belong to the genera Chorizococcus McKenzie (1 species), Dysmicoccus Ferris (2 species), Ferrisia Fullaway (1 species), Planococcus Ferris (3 species) and Pseudococcus Westwood (1 species). One species is new to science, Chorizococcus ozeri Zarkani & Kaydan, whilst another, Planococcus bagmaticus Williams is a newly recorded in Indonesia. In addition, this is the first report of the genus Chorizococcus attacking Loranthaceae worldwide. Furthermore, the mealybugs Dysmicoccus lepelleyi (Betrem), Dysmicoccus zeynepae Zarkani & Kaydan, Ferrisia dasylirii (Cockerell), Planococcus lilacinus (Cockerell) and Pseudococcus jackbeardsleyi Gimpel & Miller were found for the first time associated with Loranthaceae in the world.
Currently, a total of 18 mealybug species (Hemiptera, Pseudococcidae) have been reported on plants of the family Loranthaceae worldwide (
Chorizococcus wilkeyi McKenzie, by original designation.
(adapted from Williams, 2004). Body of adult female membranous, varying in shape from elongate oval with almost parallel sides, to broadly oval. With 1–5 pairs of cerarii present on posterior segments of abdomen and sometimes a pair on head also, each cerarius bearing 2 conical setae; auxiliary setae absent from cerarii anterior to anal lobe pair. Oral rim ducts, sometimes of 2 sizes, present on dorsum and frequently also on venter. Oral collar tubular ducts usually present, at least on venter; if present on dorsum, then restricted to margins. Antennae each normally with 7 or 8 segments. Legs well developed, with translucent pores usually present, at least on hind coxae. Claw normally stout, without a denticle. Tarsal digitules minutely knobbed. Multilocular disc pores present on venter, rarely found on dorsum. Circulus present or absent, when present usually divided by an intersegmental line. Anal ring normal, bearing 6 setae. Anterior and posterior ostioles present.
(all deposited at MMUB). Holotype. Adult female, left label: AZ1204, 13.vii.2022, Indonesia, Sumatra, Bengkulu, ex Loranthus sp., 03°45'10″S, 102°16'59″E, 120 m a.s.l.; right label: Chorizococcus ozeri Zarkani & Kaydan, 3 ♀♀, coll. A. Zarkani, det. M.B. Kaydan. The holotype specimen is ringed with red ink on the coverslip. Paratypes. 3 ♀♀, Indonesia: (AZ1205), same data as holotype; 3 ♀♀, AZ206, Sumatra, Bengkulu on semi-parasitic plant, Loranthus sp. (Loranthaceae), living on avocado (Persea americana Mill.), 03°45'10″S, 102°16'59″E, 13.vii.2022, coll. A. Zarkani.
Appearance in life
(Fig.
Slide-mounted adult female
(based on the holotype and 3 paratypes) (Fig.
Dorsum. Derm membranous, with 13 pairs of cerarii around body margin, each cerarius with enlarged conical setae set up in 2 rows and each with 1 auxiliary setae. Each anal lobe cerarius set on membranous cuticle and containing 2 enlarged conical setae, each 15–25 μm long, plus 8–10 trilocular pores and 2–3 hair-like auxiliary setae, each about 10–12 μm long. Dorsal setae conical, thinner than most cerarian setae, each 5.0–7.5 μm long, median setae 10.0–12.5 μm long, scattered throughout dorsum. Trilocular pores, each 2.5–3.8 μm in diameter, scattered. Multilocular disc pores and tubular ducts absent.
Venter. Setae flagellate, each 87.5–122.5 μm long, longest setae located medially on head. Apical setae on anal lobes unusually short, each 125.0–127.5 μm long. Multilocular disc pores, each 6.25–7.5 μm in diameter, present on abdominal segments, distributed as follows (mean numbers): IV: 18, V: 42, VI: 44, VII: 28, and VIII: 18. Trilocular pores, each 2.5–3.8 μm across, scattered throughout venter. Oral collar tubular ducts with two types: large type each 7.5–10.0 μm long, 2.5–3.1 μm wide, present one on each marginal abdominal segments V–VIII and mesothorax, and more abundantly on mid areas of thorax.
Chorizococcus ozeri is most similar to Chorizococcus srinagaricus Williams in having no oral rim tubular ducts on the venter; dorsal rim tubular ducts few, present mainly either in medial areas or marginal areas. However, C. ozeri can be distinguished from C. srinagaricus in having (character states for C. srinagaricus given in parentheses): (i) oral rim tubular ducts present mainly in marginal areas of dorsum (mainly in medial areas of dorsum); (ii) oral collar tubular ducts absent on dorsum (present); (iii) ventral oral collar tubular ducts present around abdomen only (present on entire body surface); (iv) large discoidal pores absent from venter (present); and (v) translucent pores on hind coxa present (absent).
It is also similar to Chorizococcus sorgi Williams in lacking oral collar tubular ducts entirely from ventral margins of head and thorax; multilocular disc pores and oval collar tubular ducts absent from the area lateral to each first coxa. However, C. ozeri can be distinguished from C. sorgi in having (character states for C. sorgi given in parentheses): (i) cerarii confined to anal lobes only (present on at least 3 posterior cerarii); (ii) no oral rim tubular ducts on venter (oral rims present on venter); and (iii) multilocular disc pores in two rows on venter (in one row).
This species is named after Emin Ozer (Business Sustainability Lead Turkiye, Syngenta Tarim San. ve Tic. A.Ş., Yeni Mahalle 87071 Sk. Bozkurtlar Rezidans No: 52 K/D:12/25, Seyhan – Adana / TURKIYE), one of the best partners and mentor of the Kaydan’s Laboratory.
Loranthus sp. (Loranthaceae) (Fig.
Indonesia (Sumatra, Bengkulu Province).
1(0) | Cerarii confined to anal lobes only | 2 |
– | Cerarii present on at least 3 posterior segments of abdomen and sometimes on head | 5 |
2(1) | Oral rim tubular ducts of 2 sizes present on venter, in considerable number around margins and submarginal areas | C. kandyensis (Green) |
– | Oral rim tubular ducts of 1 size only, either absent from venter or present in small number only, on margins and medial areas | 3 |
3(2) | Ventral oral rim tubular ducts present, scattered on head, thorax and abdomen. Dorsal oral rim tubular ducts numerous laterally, relatively few present medially | C. graminis Khalid & Shafee |
– | Ventral oral rim tubular ducts absent. Dorsal oral rim tubular ducts few, present mainly either in medial areas or margin areas | 4 |
4(1) | Dorsal oral rim tubular ducts present mainly in medial areas. Dorsal and ventral oral collar tubular ducts present throughout dorsum and venter. Large discoidal pores, some almost as large as multilocular disc pores, present on venter. Translucent pores on hind coxa apparently absent | C. srinagaricus Williams |
– | Dorsal oral rim tubular ducts present mainly in margin areas. Dorsal oral collar tubular ducts absent. Ventral oral collar tubular ducts present around abdomen only. Large discoidal pores absent from venter. Translucent pores on hind coxa present | C. ozeri Zarkani & Kaydan |
5(1) | Ventral multilocular disc pores present around vulva only, numbering 2–4 | C. alami Khalid & Shafee |
– | Ventral multilocular disc pores present across abdominal segments, at least as far forward as abdominal segment IV, numbering more than 10 | 6 |
6(5) | Oral collar tubular ducts present on ventral margins of head and thorax; a group of tubular ducts associated with 1 or 2 multilocular disc pores situated lateral to each first coxa | C. irretitus Williams |
– | Oral collar tubular ducts absent entirely from ventral margins of head and thorax; multilocular disc pores and oval collar tubular ducts absent from lateral to each first coxa | C. sorgi Williams |
Indonesia, Sumatra, Bengkulu Province, North Bengkulu District, Kemumu, on Loranthus sp. (Loranthaceae), living on cacao (Theobroma cacao L.), 600 m a.s.l, 03°26'00″S, 102°15'15″E, 11.v.2022, coll. A. Zarkani (AZ983-984), 6 ♀♀.
The species is polyphagous on 25 plant genera within 17 families: Anacardiaceae, Annonaceae, Arecaceae, Asparagaceae, Clusiaceae, Euphorbiaceae, Fagaceae, Malvaceae, Meliaceae, Moraceae, Musaceae, Myrtaceae, Rubiaceae, Rutaceae, Sapindaceae, Sapotaceae, and Zingiberaceae (
Indonesia, Sumatra, Bengkulu Province, Seluma District, Napal Jungur, on Loranthus sp. (Loranthaceae), living on Jengkol (Pithecellobium lobatum Benth), 205 m a.s.l., 03°57'12″S, 102°30'09″E, 5.iii.2023, coll. A. Zarkani (AZ1248), 3 ♀♀.
Dysmicoccus zeynepae is a polyphagous species found on ornamental plants and tropical fruits such as Durio zibethinus Murray (Malvaceae), Lansium parasiticum Corrêa (Meliaceae), Manilkara zapota Linnaeus (Sapotaceae) and Coffea robusta Lindl. ex de williamson (Rubiaceae) (
Indonesia, Sumatra, Bengkulu Province, Bengkulu City, Teluk Segara, on Loranthus sp. (Loranthaceae), living on cucumber tree (Averrhoa bilimbi L.), 30 m a.s.l., 03°47'18″S, 102°15'15″E, 12.vi.2022, coll. A. Zarkani (ΑΖ1080-1081), 3 ♀♀.
The species is polyphagous on ornamental plants and fruits belonging to 30 plant families and 54 genera. It is cosmopolitan, being found in 24 countries; in Indonesia it was first recorded from Bengkulu Province, Southern Sumatra on Durio zibethinus Murray (Malvaceae), Gliricidia sepium (Jacq.) (Fabaceae), Hibiscus spp. (Malvaceae), Psidium guajava L. (Myrtaceae), Solanum torvum Swartz (Solanaceae) and Theobroma cacao L. (Malvaceae) (
Indonesia, Sumatra, Bengkulu Province, Seluma City, Air Periukan, on Loranthus sp. (Loranthaceae), living on cacao tree (Theobroma cacao L.), 30 m a.s.l., 04°01'37″S, 102°24'50″E, 08.vii.2022, coll. A. Zarkani (AZ1112-1114), 6 ♀♀.
The holotype and paratypes specimens were recorded from Nepal, all in a single slide and deposited at Entomological Institute, Hokkaido University, Sapporo, Japan (HUSJ) and Natural History Museum, United Kingdom, London (BMNH), respectively. It was originally recorded from Trachelospermum sp. (Apocynaceae) (
INDONESIA, Sumatra, Bengkulu Province, Bengkulu City, Muara Bangkahulu, on Loranthus sp. (Loranthaceae), living on cucumber tree (Averrhoa bilimbi L.), 30 m a.s.l., 03°45'36″S, 102°16'01″E, 12.vi.2022, coll. A. Zarkani (ΑΖ1080-1081), 3 ♀♀.
The holotype of P. bendovi was collected on peanut, Arachis hypogaea L. (Fabaceae) in Tripura and Orissa, India (
Indonesia, Sumatra, Bengkulu Province, Bengkulu City, Slebar, on Loranthus sp. (Loranthaceae), living on avocado tree (Persea americana Mill.), 20 m a.s.l., 03°49'25″S, 102°19'08″E, 08.vii.2022, coll. A. Zarkani (AZ1118-1120), 6 ♀♀.
The species is polyphagous on ornamental plants and fruit trees; it has been recorded from 36 plant families and 73 genera (
Indonesia, Sumatra, Bengkulu Province, Seluma City, Air Periukan, on Loranthus sp. (Loranthaceae). living on cacao trees (Theobroma cacao L.), 30 m a.s.l., 04°01'37″S, 102°24'50″E, 08.vii.2022, coll. A. Zarkani (AZ1112-1114), 6 ♀♀.
The species is polyphagous on ornamental plants and fruit trees; it has been recorded from 54 plant families and 114 genera (
The authors wish to thank Dr Takumasa Kondo (Corporación Colombiana de Investigación Agropecuaria – Agrosavia, Colombia), for his kind help and critique of the manuscript.
No conflict of interest was declared.
No ethical statement was reported.
The project was financially supported by Direktorat Riset, Teknologi, dan Pengabdian kepada Masyarakat (DRTPM), Directorate General of Higher Education, Republic of Indonesia with grants No. 211/E5/PG.02.00.PT/2022; 1947/UN30.15/PP/2022. The writing of the manuscript was assisted by World Class Professor, Dikti Program 2022.
Conceptualization: AZ. Data curation: AZ, AF. Supervision: MBK, DA. Validation: MBK. Agustin Zarkani: Sample collection, Slide Preparations, Scientific drawing, morphological identification. Ariffatchur Fauzi: Sample collection, Slide Preparations. Dwinardi Apriyanto: insect rearing, data supervision. Mehmet Bora Kaydan: morphological identification, data analysis.
Agustin Zarkani https://orcid.org/0000-0001-9837-5019
Ariffatchur Fauzi https://orcid.org/0000-0001-9900-0614
Dwinardi Apriyanto https://orcid.org/0000-0002-5286-9010
Mehmet Bora Kaydan https://orcid.org/0000-0002-0677-255X
All of the data that support the findings of this study are available in the main text or Supplementary Information.