Vidović, Biljana ¹ ; Cvrković, Tatjana ² and Orapa, Warea ³

¹✉ University of Belgrade, Faculty of Agriculture, Department of Entomology and Agricultural Zoology, Nemanjina 6, 11080 Belgrade-Zemun, Serbia.
²Institute for Plant Protection and Environment, Banatska 33, 11080 Belgrade, Serbia.
³National Agriculture Research Institute, Sir Alkan Tololo Research Centre, PO Box 4415, Lae, Morobe Province, Papua New Guinea.

2023 - Volume: 63 Issue: 3 pages: 933-944

ZooBank LSID: F92CDDEF-9C2A-489E-8166-895DE352D43C

Original research

Keywords

Abstract

Introduction

Eriophyidae Nalepa (Acariformes: Prostigmata), as one of the smallest arthropods (body length around 200 µm) are obligate phytophagous species (Lindquist and Oldfield 1996). About 80% of described species are monophagous, registered on only one host plant (Skoracka et al. 2010). Some of them are significant pests in agriculture (Lindquist et al. 1996) at the same time, a certain number of species are considered potential agents for classical biological control of weeds (Smith et al. 2010; Marini et al. 2021). The attributes of eriophyid mites that qualify them as classical biological control agents of weeds are their high host specificity, dispersal by wind, high rates of reproduction, short generation times and their significant impact on plants (Lindquist et al. 1996; Cullen and Briese 1998).

Batai wood, Falcataria moluccana (Miq.) Barneby & Grimes (Fabaceae) is a large, fast-growing deciduous tree, native to parts of Indonesia and Papua New Guinea (PNG) (Wagner et al. 1999). It was introduced into Hawaii in 1917 for reforestation and as an ornamental plant, but it became invasive as well as on other Pacific and Indian Ocean islands (Hughes et al. 2011).

In the pursuit of a potential biological control agent for batai wood, eriophyid leaf gall mites have been identified and selected for further examination due to their potentially significant destructive capabilities. To date, a total of 47 eriophyid mite species have been described on host plants belonging to genera within the mimosoid clade (subfamily Caesalpinioidea DC.). The species described are from the genera Abacarus Keifer, Aceria Keifer, Aculops Keifer, Aculus Keifer, Heterotergum Keifer, Paratetra ChannaBasawanna, Pentamerus Roivainen, Phyllocoptes Nalepa, Porcupinotus Mohanasundaram, Tegonotus Nalepa, Tetra Keifer and only one species has been described from the genus of the subfamily Nothopodinae; tribe Nothopidini – Cosella deleoni (Keifer) on the host plant Pinthecollobium guadalupense (Pers.) Chapm. (Amrine & Stasna 1994; Chandrapatya et al, 2017).

The current literature has no records of eriophyid mites on Falcataria moluccana (syn. Albizia moluccana Miq.).

In this paper, one new genus and one new species of the subfamily Nothopodinae, tribe Colopodacini, are described. The mites were associated with Falcataria moluccana, causing erineum on both surfaces of the leaf, and were collected in Papua New Guinea. A key to the genera of the tribe Colopodacini described to date is provided.

Material and methods

Collection and morphological measurements

Plant samples of Falcataria moluccana were collected at Fanamafai Village, along Fangaloa Crossing, Kavieng District of New Ireland Province in Papua New Guinea. (02°52′19.21″S; 151°09′20.37″E).

The collected leaf pinnae of the plant were kept in sealed sample bottles containing 95-96% ethanol. The plant material thus collected was sent to Serbia and in the laboratory the mites were removed from the leaf samples by direct examination under a stereomicroscope and/or by extraction methods (de Lillo 2001; Monfreda et al. 2007), they were then mounted in Keifer's F medium (Amrine and Manson 1996). Structures relevant for taxonomic identification were examined using an Olympus BX53 research microscope with phase contrast and measured using the software package cellSens Entry 2 (CS-EN-V2) on the same microscope. Specimens were illustrated using a camera lucida on a Leica DMLS research microscope with phase contrast.

The morphology and nomenclature follow Lindquist (1996), the genus classification is based on Amrine et al. (2003) and the nomenclature of the internal female genitalia follows Chetverikov (2014). Measurements and illustrations were made according to Amrine and Manson (1996) and de Lillo et al. (2010). All measurements are given in micrometers (μm) and, unless otherwise stated, signify the length of the structure.

Plant names are in accordance with The Plant List (2013) on-line database. The holotype and the paratype slides are deposited in the collections of the Acarology Laboratory, Department of Entomology and Agricultural Zoology, Faculty of Agriculture, University of Belgrade, Serbia.

Scanning electronic microscopy

Scanning electron micrographs (SEM) were taken according to Alberti and Nuzzaci (1996) by the technique of reconstructing eriophyids from dry plant material. The mite specimens are first transferred to Keifer's medium I in a cavity slide and heated to about 140^oC on an electric plate to bring the mites to their more or less original shape. The specimens are then transferred briefly, about 1 munite, into a KCl-glycerol solution. Excess solution is sucked off with philtre paper and the mites are then placed on the SEM holder. For specimen preparation before being placed on the SEM stage, mites were sputter-coated with gold for 100 s under 30 mA ion current. The mites were then studied in the vacuum chamber of a JEOL Scanning Electron Microscope (JEOL-JSM6390, Peabody, MA, USA) at the Laboratory of Electron Microscopy, Faculty of Agriculture, University of Belgrade, Serbia

DNA extraction, PCR amplification and sequencing

For molecular analysis, mites were removed by direct examination under a stereomicroscope from leaves of F. moluccana collected in Papua New Guinea, preserved in 96% ethanol, and stored at 4 °C until DNA extraction, which was performed in Serbia.

Total DNA was extracted from individual specimens in three replicates using the QIAGEN DNeasy® Blood & Tissue Kit, following the manufacturer's instructions, with modifications based on Dabert et al. (2008); the mites were not crushed. Amplification of the mitochondrial cytochrome c oxidase subunit I gene (COI) barcode region was performed using primers LCO1490 and HCOd (Folmer et al., 1994; Chetverikov et al., 2015). Polymerase chain reactions (PCR) were conducted using High Yield Reaction Buffer A with Mg (1x), 2.5 mM MgCl2, 0.6 mM of each dNTP, 0.5 μM of each primer and 1 U of KAPA Taq DNA polymerase (Kapa Biosystems, MA, USA) in a 25-μL final volume. PCR cycles were carried out in a Mastercycler ep Gradient S (Eppendorf, Germany), applying reaction conditions as described in Cvrković et al. (2016). PCR amplicons were visualized in a 1% agarose gel and purified using the QIAquick PCR purification Kit (QIAGEN, Germany) according to the manufacturer's instructions. Sequencing was performed in both directions with the same primer pairs as in the initial PCR procedure by Macrogen Europe (Amsterdam, Netherlands).

Results

Family Eriophyidae Nalepa 1898

Subfamily Nothopodinae Keifer 1956

Tribe Colopodacini Mohanasundaram 1984

Genus Solenidiversum gen. nov. Vidović

ZOOBANK: 1D18B589-59F1-4E76-988C-167423810536

(Figs. 1 & 2)

Type species — Solenidiversum falcatariae sp. nov.

Diagnosis — The subfamily Nothopodinae Keifer 1956 are distinguished from the other subfamilies of Eriophyidae by: the tibia of the legs is reduced or completely fused with the tarsus, tibia I without setae and tarsus without spatulate projections.

Within the subfamily Nothopodinae, it is possible to distinguish two tribes, Nothopodini Keifer 1956 and Colopodacini Mohanasundaram 1984. The characteristics of tribe Colopodacini are the presence of coxal setae 1b, coxae of leg I usually weakly divided and tibia of leg I completely fused with the tarsus, except in the genus Thaicesa Koçak & Kemal, which has very small tibiae. The characteristics of Nothopodini are the absence of coxal setae 1b, coxae and tibiae of leg I variable.

Solenidiversum gen. nov. belongs to Colopodacini with coxal setae I (1b) present, tibiae of legs I and II completely fused with tarsus; empodium entire; solenidion on tarsus I on inner side of tarsus; solenidion on tarsus II in dorsal position; all leg setae present; scapular tubercles on rear shield margin; setae sc projecting backward; prodorsal shield with small subtriangular frontal lobe; body vermiform; opisthosoma evenly round and with annuli subequal dorsoventrally, entirely microtuberculated; all ventral opisthosomal setae present; accessory setae (h1) absent.

Remarks — It should be noted that fifteen genera have been described from the tribe Colopodacini. From nine of those genera, the tibia of leg I is completely fused with the tarsus (Colopodacus Keifer, Apontella Boczek & Nuzzaci, Paracolopodacus Kuang & Huang, Adenocolus Meyer & Ueckermann, Pseudocolopodacus Kuang, Dicolopodacus Huang, Kuangella Wei, Taicolopodacus Huang & Wang, and Juxtacolopodacus Flechtmann & De Queiroz) and in the other six (Thaicesa Koçak & Kemal 2008, Calliparus Li, Setibia Duarte & Navia, Aricolopodos Duarte & Navia, Calareolata Han & Zhang and Reginesus Reis & Navia) the tibia is reduced and very short, but not completely fused with the tarsus (Keifer 1960; Boczek and Nuzzaci 1988; Kuang and Huang 1994; Boczek and Chandrapatya 1996; Meyer and Ueckermann 1997; Kuang 1997; Huang 2001; Wei and Quin 2002; Koçak and Kemal 2008; Huang and Wang 2009; Flechtmann and De Queiroz 2010; Li et al. 2010; Reis et al. 2012; Duarte et al. 2017; Han and Zhang 2019).

Therefore, it is necessary to emphasize that the fusion of the tibia with the tarsus is not a distinguishing characteristics of the tribe Colopodacini, as specified in the Revised Keys to the World Genera of the Eriophyoidea (Amrine et al. 2003). Тhe character that distinguishes the Colopodacini tribe from the Nothopodini tribe within the subfamily Nothopodinae is the presence (in Colopodacini) versus the absence of 1b coxal setae (Nothopodini).

Differential diagnosis — The new genus is placed in Colopodacini, Nothopodinae, Eriophyidae, Eriophyoidea. There are sixteenth genera in Colopodacini. This new genus has the solenidion on the inner side of tarsus I, differentiating it from all other genera of the tribe.

The feature of displaced solenidia of leg I has so far been recorded in the genus Juxtacolopodacus (tribe Colopodacini), where the solenidion is displaced laterally, and in the genus Floracarus (Nothopodini) with a solenidion on the inner side of the tarsus (Flechtmann et al.2010, Meyer & Ueckermann 1997).

This new genus, like Thaicesa, Adenocolus, Caliparus and Setibia, has scapular tubercles and setae on rear prodorsal shield margin. It differs from Thaicesa and Adenocolus in the presence of bv setae on both legs (absent on both legs in Thaicesa, absent on leg II in Adenocolus). It differs from Caliparus by the fused tibia and tarsus (distinct tibia and tarsus in Caliparus). This new genus is most similar to Setibia, because only these two genera within the tribe Colopodacini have a worm-like body shape, unlike the other fourteen genera of this tribe. It differs from this genus, however, in the complete fusion of the tibia with the tarsus on both legs (in Setibia the tibia is reduced, but distinct) and in the absence of a prominent frontal lobe as in Setibia.

Etymology — The genus name Solenidiversum is a combination of Soleni (from the Latin solenidion – optically inactive chemosensory seta) and diversum (from the Latin diversus, meaning opposite). It refers to the opposite positions of the solenidion on the tarsus of leg I (ventral positions) in relation to the positions of the solenidion on the tarsus of leg II (dorsal positions). Gender: neutral

Solenidiversum falcatariae sp. nov. Vidović

ZOOBANK: CC826E3B-ABBB-4C5F-B47F-363DF1699A7B

(Figs. 1 & 2)

Description

FEMALE (n=10). Body vermiform 187 (166–194), 41 (38–45) wide, whitish in color. Gnathosoma 15 (12–16) projecting slightly downwards, chelicerae 9 (8–9), dorsal pedipal genual setae d 3. Prodorsal shield 22 (17–22) including the small subtriangular frontal lobe, 21 (20–22) wide. Triangular with a rounded frontal lobe over the gnathosoma; median and admedian lines complete; I pair of submedian lines present on anterior half, incomplete; II and III pair of submedian lines incomplete, extending from anterior margin and ending ahead of prodorsal shield tubercles; in the lower half of the shield there are numerous dashes between all lines of prodorsal shield; on both lateral margins, of the rear of shield, there are areas with more numerous and densely dashes. Tubercles sc on rear shield margin 12 (11–12) apart, scapular setae sc 24 (22–26). Leg I 24 (19–24); femur 10 (8-10), ventral basifemural setae bv 6 (4–6); genu 4 (3–4), antaxial genual setae l″ 15 (12–16); tibiotarsus 7 (5–8), paraxial fastigial tarsal setae ft′ 9 (8– 11), antaxial fastigial tarsal setae ft″ 17 (14–18); tarsal solenidion ω 4 (3–4); tarsal empodium 5 (4–6), 6-rayed. Leg II 20 (16–20); femur 9 (7–9), ventral basifemural setae bv 5 (5–7); genu 3 (3–4), antaxial genual setae l″ 6 (5–7); tibiotarsus 6 (5–6), paraxial fastigial tarsal setae ft′′ 4, antaxial fastigial tarsal setae ft″ 16 (14–17); tarsal solenidion ω 7 (6–8); tarsal empodium 4 (4–5), 6–7-rayed. Coxigenital region with 5–6 semiannuli betwen coxae and genitalia. Coxisternal plates granulated; sternal line 6; proximal setae on coxisternum I (1b) 4 (4–5), tubercles 1b 4 apart; anterolateral setae on coxistenum II (1a) 20 (18–23), tubercles 1a 6 (5–6) apart, proximal setae on coxisternum II (2a) 29 (25–32), tubercles 2a 12 (11–13) apart. External genitalia 10 (8–10), 12 (12–14) wide, granulated proximally and with two transverse curved lines distally, setae 3a 5 (5–6), 9 (8–11) apart. Internal genitalia with anterior, transversal apodeme trapezoidal, longitudinal bridge relatively long, spermathecal tubes directed latero-posterad, spermathecae egg-shaped, globose. Opisthosoma with subequal annuli: 55 (53–66) dorsal and 58 (56–68) ventral annuli. Dorsal and ventral opisthosoma with oval, elongated microtubercles close to the rear margins of annuli. Setae c2 14 (13–16), 27 (27–33) apart, on annulus 8 (8–9); setae d 34 (30–38), 24 (21–26) apart, on annulus 20 (18–22); setae e 41 (36–41), 19 (16–20) apart, on annulus 36 (36–42); setae f 16 (14–17), 10 (10–12) apart, on annulus 53 (52–63); seta h2 76 (74–83), 7 (7–8) apart; setae h1 absent.

MALE (n=2). Smaller than females and generally similar to them, 130–150, 35–40 wide. Gnathosoma 10–12 curved down, cheliceral stylets 6–7. Prodorsal shield 17–19, 19–21 wide. Prodorsal shield tubercles on the rear shield margin 12–13 apart, setae sc 12–14, projecting posteriorly. Shield design similar to female. Leg I 16–18; femur 7, setae bv 4; genu 3, setae l″ 9; tibiotarsus 5, setae ft′ 8, setae ft″ 13; solenidion ω 3; empodium em 4, and 6-rayed. Leg II 16; femur 7, setae bv 4; genu 3, genual setae l″ 5; tibiotarsus 4, setae ft′ 3–4, setae ft″ 13; solenidion ω 7; empodium em 4. Coxigenital region with 5–6 semiannuli between coxae and genitalia. Coxisternal plates granulated; sternal line 3; setae 1b 3–4, 1b tubercles 3–4 apart; setae 1a 11–12, 1a tubercles 6 apart; setae 2a 19–22, 2a tubercles 13–14 apart. External genitalia 13–14 wide, epiandrum typically ornamented with small granules, setae 3a 3–5, 3a tubercles 10–11 apart, setae eu absent. Opisthosoma with subequal annuli: 54–56 dorsal and 54–56 ventral annuli; setae c2 12–13, 37 apart, on annulus 6–7; setae d 21–22, 24– 25 apart, on annulus 15; setae e 24–26, 18 apart, on annulus 30–32; setae f 11–12, 10 apart, on annulus 49–52; setae h2 30–35, 6–7 apart, setae h1 absent.

NYMPH (n=3). Body vermiform, 123–132, 40–43 wide. Gnathosoma 9–12, chelicerae 7–8. Prodorsal shield 17–19, 23 wide, scapular tubercles 15–16 apart, setae sc 9–10. Leg I 12–13, femur 5–6, setae bv 3; genu 2–3, setae l″ 6–8; tibiotarsus 3–4, setae ft′ 3–4, setae ft″ 9–11; solenidion ω 2–3; empodium em 3–4, and 5-rayed. Leg II 11–12; femur 4–5, setae bv 2; genu 2, genual setae l″ 4–6, tibiotarsus 3, setae ft′ 2–3, setae ft″ 10–11; solenidion ω 4–5; empodium em 3–4. Coxigenital region with 5–6 complete annuli, setae 3a 2, tubercles 4–5 apart. Coxisternal plate granulated; setae 1b 2, 1b tubercles 5 apart; setae 1a 4–5, 1a tubercles 5–6 apart; setae 2a 8, 2a tubercles 13–14 apart. Opisthosoma with subequal annuli: 40–45 dorsal and 44–50 ventral annuli; setae c2 4-5, 32–33 apart, on annulus 8; setae d 11–13, 22 apart, on annulus 16–17; setae e 7, 12–14 apart, on annulus 27–29; setae f 10, 11–12 apart, on annulus 40–45; setae h2 18–19, 6–7 apart, setae h1 absent.

Type host plant

Falcataria moluccana (Miq.) Barneby & Grimes (Fabaceae)

Type locality

Papua New Guinea: Fanamafai Village, along Fangaloa Crossing, Kavieng District, New Ireland Province (02°52′19.21″S; 151°09′20.37″E; Alt. 267 m.a.s.l.).

Type material. Female holotype (slides 946/5) and paratypes 37 females, 3 males; 10 nymphs; 10 February 2021, collected by Warea Orapa.

Additional material. Papua New Guinea: Kafa Road, South of Pimaga Government Station, Lake Kutubu District, SHP. (06°31′42.67″S; 143°32′08.88″E; Alt. 933 m.a.s.l) 31 January 2021, 25 slides, collected by Warea Orapa. Relation to the host. The infestation caused by this mite results in the formation of white erineum on both surfaces of the leaflets, later the erineum darkens (Fig. 3).

Etymology

The species name is based on the host plant's generic name, Falcataria.

COI sequence

The whole barcode region (658 bp) of mtCOI was generated from three specimens of Solenidiversum falcatariae sp. nov. As all nucleotide sequences were 100% identical, only one of them was submitted to the GenBank database under accession number OQ401030. The translation of the nucleotide sequences resulted in 219 amino acid positions. Base pair frequencies show that the region is AT-rich (A: 0.242, C: 0.140, G: 0.147, T: 0.471).

Key to the genera of Colopodacini

1. Prodorsal shield lacking scapular tubercles and setae
...... Pseudocolopodacus Kuang, 1997

— Scapular tubercles and setae present
...... 2

2. Empodia divided; shield with three anterior lobes
...... Dicolopodacus Huang, 2001

— Empodia entire
...... 3

3. Scapular tubercles and setae on rear prodorsal shield margin; antaxial genual setae (l") of leg II and ventral setae (e) present
...... 4

— Scapular tubercles and setae not on rear prodorsal shield margin; antaxial genual setae (l") of leg II and ventral setae (e) variable
...... 8

4. Tibia completely fused with tarsus
...... 5

— Tibia very small but distinct
...... 6

5. Basiventral femoral seta (bv) of leg I present; basiventral femoral seta (bv) of leg II absent; dorsal position of selenidion on both tarsus
...... Adenocolus Meyer & Ueckermann, 1997

— Basiventral femoral seta (bv) present on both legs; solenidion on tarsus I on inner side of tarsus, solenidion on tarsus II in dorsal position
...... Solenidiversum gen. nov.

6. Basiventral femoral seta (bv) absent on both legs
...... Thaicesa Koçak & Kemal, 2008

— Basiventral femoral seta (bv) present on both legs
...... 7

7. Dorsal opisthosoma flat with weak submedian ridges, dorsal annuli undulated
...... Calliparus Li, Wang & Wei, 2010

— Dorsal opisthosoma entirely microtuberculated
...... Setibia Duarte & Navia, 2017

8. Scapular tubercles and setae on the lateral side of the prodorsal shield
...... 9

— Scapular tubercles and setae ahead of rear prodorsal shield margin
...... 10

9. Opisthosoma with smooth tergites
...... Kuangella Wei, 2002

— Opisthosoma with middorsal ridge
...... Juxtacolopodacus Flechtmann & de Queiroz, 2010

10. Tibia completely fused with tarsus
...... 11

— Tibia very small but distinct
...... 14

11. Antaxial genual setae (l") of leg II and ventral setae (e) absent
...... 12

— Antaxial genual setae (l") of leg II and ventral setae (e) present
...... 13

12. Dorsal opisthosoma without ridges
...... Paracolopodacus Kuang & Huang, 1994

— Dorsal opisthosoma with median and subdorsal ridges
...... Taicolopodacus Huang & Wang, 2009

13. Basiventral femoral setae (bv) present on both legs; dorsal opisthosoma with median ridge
...... Colopodacus Keifer, 1960

— Basiventral femoral setae (bv) of leg I absent; dorsal opisthosoma with narrow median furrow
...... Apontella Boczek & Nuzzaci, 1988

14. Antaxial genual setae (l") of leg II present; dorsal opisthosoma without ridges
...... Calareolata Han & Zhang, 2019

— Antaxial genual setae (l") of leg II absent; dorsal opisthosoma with the ridge
...... 15

15. Basiventral femoral setae (bv) present on both leg
...... Aricolopodos Duarte & Navia 2017

— Basiventral femoral setae (bv) absent on both legs
...... Reginesus Rei & Navia 2012

Acknowledgements

The authors would like to thank Prof. R. Petanović, University of Belgrade, Serbia, for the critical review of the manuscript and for her assistance on the nomenclature of the names Solenidiversum. Special gratitude is due to Dragica Smiljanić (University of Belgrade, Belgrade-Zemun, Serbia) for her technical support and Dr. Quentin Paynter (Manaaki Whenua-Landcare Research New Zealand) for his support of the field work in Papua New Guinea.

Funding

This study was supported by: Ministry of Education, Science and Technological Development of the Republic of Serbia, contract No. 451-03-68/2022-14/200116, No. 451-03-68/2022-14/200010; New Zealand Ministry of Foreign Affairs and Trade (MFAT) through the Managing Invasive Species for Climate Change Adaptation in the Pacific (MISSCAP) programme and Manaaki Whenua – Landcare Research (PRJ2839, Subcontract No. 1920-23-039 G).

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

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