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. 2026 Sep 1;17(9):915. doi: 10.3390/insects17090915

On the Identity of Pear Psyllids in Iran: A Plea Against the Continued Misuse of Cacopsylla pyricola (Hemiptera: Psylloidea)

Mohammadreza Lashkari 1,*, Liliya Štarhová Serbina 2,3
Editor: Wanzhi Cai
PMCID: PMC13607166  PMID: 42783282

Simple Summary

Pear psyllids are important pests of pear orchards, and some species are difficult to identify because they are very similar in appearance. Incorrect identification can affect pest management and quarantine decisions. In this study, we used DNA barcoding to identify pear psyllid species occurring in Iran. We also provide the first DNA barcode sequences for Cacopsylla permixta. Our results showed that the GenBank records of C. pyricola from Iran, which were examined in this study, were based on misidentified specimens belonging to other species. Our findings highlight the importance of accurate species records and careful use of GenBank databases. The occurrence of C. pyricola in Iran should be verified through targeted sampling and examination of reliably identified voucher specimens. Further studies are also needed to determine whether pear psyllid species can act as vectors of phytoplasma in Iran.

Keywords: Psyllidae, Pyrus, jumping plant lice, pests, identification key, GenBank species misidentifications, molecular barcodes

Abstract

Pear psyllids are among the most serious pests of cultivated pear. In the past, repeated misidentifications and the uncritical application of species names led to considerable confusion in biodiversity records and pest monitoring of pear psyllids. Although several revisions clarified many of these issues, misidentifications have persisted, particularly in records attributed to Cacopsylla pyricola (Foerster) in Iran, which may result in serious problems in quarantine and pest management. Currently, 34 species of Cacopsylla are known to be associated with Pyrus spp., five of which are confirmed to occur in Iran, while the occurrence of C. pyricola in the country remains likely but unconfirmed. In this study, we demonstrate that the examined Cacopsylla species differ significantly in their COI barcodes, which can be reliably used for species identification. The COI sequences for C. permixta are published here for the first time. Our results suggest that the GenBank and literature records of C. pyricola from Iran likely represent misidentifications of other species that occur throughout the pear-producing regions of Iran. These misidentifications likely resulted from the application of species names without adequate morphological or molecular confirmation. Our findings highlight the need for careful validation of species records and demonstrate that GenBank sequences should be used cautiously unless they are linked to reliably identified voucher specimens.

1. Introduction

Pyrus (Rosaceae), a genus of trees and shrubs with 73 valid species in the Palaearctic and Oriental regions [1], represents an economically significant crop in the temperate and subtropical regions of the world. Pear species, mostly Pyrus communis subsp. communis in Europe and North America, and P. bretschneideri, P. pyrifolia and P. ussuriensis in China rank among the five most widely produced fruits in the world [2]. In 2022, the estimated global pear production was over 26 million metric tonnes, with approximately 73% originating from China [3]. Pear is an important fruit crop in Iran, where orchards covered approximately 3273 hectares and produced about 95.4 thousand tonnes in 2024, ranking the country 21st among approximately 80–90 pear-producing nations worldwide [3]. Commercial cultivation occurs in the provinces of Khorasan, Tehran, Esfahan, West and East Azerbaijan, Zanjan, Qazvin, Kurdistan, Lorestan and Semnan [4].

Pear psyllids (Psyllidae: Psyllinae: Cacopsylla) are among the most serious pests of pear. They weaken plants through excessive removal of phloem sap and impede the development of flowers by feeding on flower buds; they also indirectly harm plants by secreting honeydew, which promotes the growth of sooty mould and reduces photosynthesis [5,6]. Moreover, several species act as vectors of ‘Candidatus Phytoplasma pyri’, the causal agent of Pear Decline [7,8]. Pear Decline has also been detected in Iran [9,10], although no psyllid species has yet been confirmed as a vector of the phytoplasma in the country, unlike in Europe and the USA [7,8,11].

Currently, 34 species of Cacopsylla are known to live on Pyrus spp. in the Palaearctic region, five of which are confirmed to occur in Iran, while the presence of C. pyricola still requires verification. Several species are polyvoltine, e.g., the members of the Cacopsylla pyri-group, and produce morphologically distinct summer and winter generations [12]. In contrast, members of the C. pyrisuga-group are univoltine and migrate to conifers to overwinter. Seasonal dimorphism within species and morphological similarity among species have historically led to taxonomic confusion, which was largely resolved by Burckhardt and Hodkinson (1986) [12] for Western Palaearctic taxa and by Yang et al. (2004) [13], Luo et al. (2012) [14] and Cho et al. (2017) [15] for Eastern Palaearctic taxa. Despite these revisions, confusion persists in published biodiversity and pest-monitoring data. Misidentifications in genetic databases, particularly GenBank, remain a major source of error.

The presence of five pear psyllid species in Iran has been well documented [12]: Cacopsylla bidens (Šulc, 1907), C. notata (Flor, 1861), C. permixta Burckhardt and Hodkinson, 1986, C. pyri (Linnaeus, 1758) and C. pyrisuga (Foerster, 1848). Another species, C. pyricola (Foerster, 1848), has been repeatedly reported from Iran, between 1961 and 2025, often based on questionable records or apparent misidentifications. The pear psyllids of Iran belong to two species groups: the Cacopsylla pyri-group (polyvoltine, overwintering as adults on the host plant or in leaf litter around the host) and the C. pyrisuga-group (univoltine, overwintering as adults on conifers). The Cacopsylla pyri-group is also characterised by a distinct morphological dimorphism between winter and summer generations. The summer form of C. pyri is distinguished from the winter form by the absence of brown clouding in the forewing, the presence of denser and more widespread forewing spinules, and its smaller size [12,16]. In C. bidens and C. permixta, the dimorphism affects mostly the body colour and size, with the winter form darker and larger than the summer form, which is lighter, variegated and smaller, while in C. notata, the seasonal dimorphism is very slight, affecting mostly the size [12].

The present study addresses these issues by analysing GenBank records, published literature and newly generated sequences, and by providing an illustrated morphological identification key to the Iranian pear psyllids, with the aim of helping pear growers and researchers accurately identify these species and avoid future misidentifications.

2. Materials and Methods

2.1. Literature Review

A structured literature search was conducted to compile previously published records of C. pyricola from Iran. Searches were performed across major Iranian and international scientific databases. The retrieved records were classified into two periods, before and after the taxonomic revision of the West Palaearctic pear psyllids by Burckhardt and Hodkinson (1986) [12], which provided a revised taxonomic framework for Pyrus-feeding Cacopsylla species. All relevant information was subsequently compiled in a standardised Excel database and categorised into four source types: (i) primary references, (ii) secondary references, (iii) GenBank records, and (iv) relevant online sources. For each record, available bibliographic, geographic, host plant, species identification, depository, and molecular information, including GenBank accession numbers, was extracted.

2.2. Material Examined

Material examined in this study came from two main sources: field collections and entomological collections. Field work was conducted by ML between 2022 and 2024 in pear orchards in Iran. Specimens were collected from plants using a sweep net and an aspirator. Collected specimens were stored in 96% ethanol at −20 °C for DNA extraction. For the molecular study, two specimens of Cacopsylla permixta (1 male, 1 female), identified by Daniel Burckhardt, were examined. Both specimens were collected from Pyrus sp. in Iran (Kerman Province, Mahan), on 5 September 2023 by M. Lashkari and are deposited in NHMB.

Additional material examined was preserved in the following collections: KGUT—Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran; NHMB—Naturhistorisches Museum, Basel, Switzerland; and MHNG—Muséum d’histoire naturelle, Geneva, Switzerland.

The morphological terminology follows Bastin et al. (2023) [17].

2.3. DNA Extraction, PCR and Sequencing

DNA from Cacopsylla permixta was extracted non-destructively from whole specimens using a DNeasy Blood & Tissue Kit (QIAGEN, Hilden, Germany). A fragment of the cytochrome oxidase c subunit I (COI) gene was amplified for DNA barcoding of C. permixta using the primer set described by Folmer et al. (1994) [18] and Bastin et al. (2023b) [19], LCOP-F (5′-AGAACWAAYCATAAAAYWATTGG-3′) and HCO2198 (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′), producing an expected amplicon of 658 bp. The primers were modified to include 5′ tag sequences described by Srivathsan et al. (2024) [20].

PCR conditions were as follows: 95 °C for 3 min; 40 cycles of 95 °C for 1 min, 48 °C for 30 s and 72 °C for 1 min; followed by 72 °C for 5 min. The resulting amplicons were sequenced using an Oxford Nanopore Technologies (ONT) MinION R10.4.1 flow cell on a GridION, using the SQK-LSK114 Ligation Kit v14 (Oxford Nanopore Technologies, Oxford, UK). Sequences were processed using ONTbarcoder 2.0, following the procedures developed by Srivathsan et al. (2021; 2024) [20,21].

In total, COI sequences from ten Cacopsylla species were included in the phylogenetic analysis. A total of 110 sequences were downloaded from GenBank. All sequences were aligned using ClustalW implemented in MEGA v11 [22]. Following multiple sequence alignment, a common overlapping region of 374 bp was identified across all sequences. Although this region was shorter than the standard length of the target DNA barcode, shorter sequences were retained rather than excluded to maximise the number of usable reference sequences and the representation of available taxa in the reference dataset. The 374 bp overlapping region was subsequently used for all analyses. The tree was constructed using the Neighbour-joining (NJ) algorithm with 1000 bootstrap replicates and the Kimura 2-Parameter (K2P) model.

Photos of dry-mounted specimens were taken by Dr. Daniel Burckhardt with a Leica Digital Camera DFC320 mounted on a Leica MZ12 dissecting microscope (Leica Microsystems (Switzerland) Ltd., Heerbrugg, Switzerland). CorelDRAW Graphics Suite v21 (Corel Corporation, Ottawa, ON, Canada) was used to redraw the morphological structures illustrated in Burckhardt and Hodkinson (1986) [12] for improved clarity and publication-quality presentation.

3. Results

3.1. Records of Cacopsylla pyricola in Iran

The literature review revealed numerous records of Cacopsylla pyricola from Iran, dating from 1961 to 2025. These records originated from a wide range of localities and were identified in primary and secondary references, GenBank records, and relevant web sources. A detailed summary of the records, their geographic origins, and the available taxonomic information is presented in Table 1.

Table 1.

Literature and online references reporting Cacopsylla pyricola or Psylla pyricola from Iran, with the possible identities of specimens suspected to have been misidentified. “Pre 1986” and “post 1986” indicate references published before and after Burckhardt & Hodkinson (1986) [12], respectively.

Reference Locality Possible Identity of Specimens Reported as C. pyricola
Pre 1986
Farahbakhsh 1961 [23] Tehran, Caspian Sea area C. bidens, C. permixta or C. pyri
Davatchi & Esmaili 1966 [24] Karaj C. bidens, C. permixta or C. pyri
Radjabi &Behechti 1975 [25] Iran (without details) C. bidens, C. permixta or C. pyri
Post 1986
Davoodi 1986 [26] Tehran C. bidens, C. permixta or C. pyri
Davoudi &Farzaneh 1991 [27] Tehran C. bidens, C. permixta or C. pyri
Burckhardt &Lauterer 1993 [28] Elborz, Tehran C. bidens, C. permixta or C. pyri
Heydari Alizadeh &Mossadegh 1997 [29] Karaj C. bidens, C. permixta or C. pyri
Jooyandeh et al., 2010 [30] Tehran C. bidens, C. permixta or C. pyri
Bayati et al., 2011 [31] Tehran C. bidens, C. permixta or C. pyri
Kolyaee 2011 [32] Tehran C. bidens, C. permixta or C. pyri
Ahmadi et al., 2012 [33] East Azerbaijan C. bidens, C. permixta or C. pyri
Emami &Taheri 2012 [34] Isfahan C. bidens, C. permixta or C. pyri
Emami et al., 2014a [35] Isfahan C. bidens, C. permixta or C. pyri
Emami et al., 2014b [36] Isfahan C. bidens, C. permixta or C. pyri
Zendedel 2015 [37] Razavi Khorasan, South Khorasan, Isfahan, East Azer-baijan, West Azerbaijan C. bidens, C. permixta or C. pyri
Ardestanirostami et al., 2016 [38] Karaj C. bidens, C. permixta or C. pyri
Zendedel et al., 2016 [39] Razavi Khorasan, South Khorasan, Isfahan, East Azerbaijan, West Azerbaijan C. bidens, C. permixta or C. pyri
Emami 2017 [40] Isfahan C. bidens, C. permixta or C. pyri
Emami et al., 2017 [41] Isfahan C. bidens, C. permixta or C. pyri
Ezzati et al., 2017 [42] Kurdistan C. bidens, C. permixta or C. pyri
Sherafat et al., 2018 [43] Fars, Razavi Khorasan C. bidens, C. permixta or C. pyri
Emami 2019 [44] Isfahan C. bidens, C. permixta or C. pyri
Hassanzadeh-Avval et al., 2020 [45] Razavi Khorasan C. bidens, C. permixta or C. pyri
Fathi 2023 [46] East Azerbaijan C. bidens, C. permixta or C. pyri
Latifian et al., 2023 [47] Karaj C. bidens, C. permixta or C. pyri
Emami 2025 [48] Isfahan C. bidens, C. permixta or C. pyri
GenBank (Accession No.)
KT258635– KT258636 Isfahan C. bidens
KT258637–KT258640 Razavi Khorasan, Ferdous C. bidens
KT258641–KT258644 Razavi Khorasan, Mashhad C. bidens
KT258645–KT258647 Razavi Khorasan, Kalat C. bidens
KT258648–KT258649 East Azerbaijan, Urmia C. pyri
KT258650–KT258651 East Azerbaijan, Urmia C. bidens
KT258652–KT258655 Razavi Khorasan, Shandiz C. bidens
KT258656–KT258658 East Azerbaijan, Marand C. bidens
KT258659–KT258661 Razavi Khorasan, Zoshk C. bidens
KP192848 Kerman C. permixta
KP843860 Kerman C. permixta
Secondary references
Gentry 1965 [49] Iran (without details) C. bidens, C. permixta or C. pyri
Behdad 1991 [50] Iran (without details) C. bidens, C. permixta or C. pyri
Ossiannilsson 1992 [51] Iran (without details) C. bidens, C. permixta or C. pyri
Modarres Awal 2002 [52] Iran (without details) C. bidens, C. permixta or C. pyri
Lotfalizadeh &Gharali 2008 [53] Iran (without details) C. bidens, C. permixta or C. pyri
Askari et al., 2009 [54] Iran (without details) C. bidens, C. permixta or C. pyri
Ghahari et al., 2010 [55] Iran (without details) C. bidens, C. permixta or C. pyri
Fallahzadeh &Japoshvili 2010 [56] Iran (without details) C. bidens, C. permixta or C. pyri
Khaghaninia et al., 2010 [57] Iran (without details) C. bidens, C. permixta or C. pyri
Moravvej et al., 2016 [58] Iran (without details) C. bidens, C. permixta or C. pyri
Biranvand et al., 2017 [51,59] Iran (without details) C. bidens, C. permixta or C. pyri
Hemmati et al., 2021 [60] Iran (without details) C. bidens, C. permixta or C. pyri
Sinha et al., 2022 [61] Iran (without details) C. bidens, C. permixta or C. pyri
Biranvand et al., 2024 [62] Iran (without details) C. bidens, C. permixta or C. pyri
websites
https://mihankesht.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://agripars.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://bartarnahal.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://lib.salamkeshavarzco.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://fartakabizendehrood.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://narenjspadana.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://kavoshkimia.com, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
https://taranomesabz.ir, accessed on 27 August 2026 Iran (without details) C. bidens, C. permixta or C. pyri
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3.2. Morphology of Iranian Pear Psyllids and Identification Keys

3.2.1. Pear Psyllid Species Recorded from Iran

Figure 1.

Figure 1

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Adults of Cacopsylla spp., lateral view. (a) Cacopsylla bidens (summer form); (b) C. bidens (winter form); (c) C. notata; (d) C. permixta; (e) C. pyri; (f) C. pyricola; (g) C. pyrisuga. Scale bars = 0.5 mm.

Figure 2.

Figure 2

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Forewings of Cacopsylla spp. (a) Cacopsylla bidens; (b) C. notata; (c) C. permixta; (d) C. pyri; (e) C. pyricola; (f) C. pyrisuga. Redrawn from Burckhardt and Hodkinson (1986) [12].

Figure 3.

Figure 3

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Inner surface of paramere of Cacopsylla spp., lateral view. (a) Cacopsylla bidens; (b) C. notata; (c) C. permixta; (d) C. pyri; (e) C. pyricola; (f) C. pyrisuga. Redrawn from Burckhardt and Hodkinson (1986) [12].

Figure 4.

Figure 4

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Female terminalia of Cacopsylla spp., lateral view. (a) Cacopsylla bidens; (b) C. notata; (c) C. permixta; (d) C. pyri; (e) C. pyricola; (f) C. pyrisuga. Redrawn from Burckhardt and Hodkinson (1986) [12].

Material examined. IRAN, Alborz: 5 ♂, 5 ♀, Gachsar (36.03° N, 51.31° E), 2045 m, 16.ix.2022, leg. M Lashkari; 5 ♂, 5 ♀, Kondor (35.84° N, 51.10° E), 1874 m, 16.ix.2022, leg. M Lashkari; Esfahan: 5 ♂, 5 ♀, Abyaneh (33.58° N, 51.65° E), 1938 m, 19.x.2023, leg. M Lashkari; Razavi Khorasan: 5 ♂, 5 ♀, Mashhad (36.61° N, 59.69° E), 1286 m, 30.viii.2023, leg. M Lashkari.

Distribution in Iran. East Azerbaijan [33], Elborz (Karaj) [28], Esfehan [63], Kerman [64,65], Kurdistan [42,63], Razavi Khorasan [39], Tehran [28], West Azerbaijan [28,63], Zanjan [63], without details [12,15,66,67,68].

Distribution in Iran. Kohgiluyeh and Boyer-Ahmad (Yasuj) [28], without details [15,69].

Material examined. IRAN, Kerman: Mahan (30.09° N, 57.21° E), 1908 m, 5.ix.2023, leg. M Lashkari; 5 ♂, 5 ♀, Bardsir (29.53° N, 56.66° E), 2595 m, 5.x.2022, leg. M Lashkari.

Distribution in Iran. Alborz [63], Golestan [28], North Khorasan [63], Tehran [63], Semnan [28].

Distribution in Iran. East Azerbaijan [33], Tehran [70], Zanjan [28], without details [15,68].

Distribution in Iran. Elborz [28], Mazandaran (as Psylla pyrisuga) [71], without details [15].

3.2.2. Misidentification

Previous records of C. pyricola (Foerster, 1848) from Iran are considered doubtful and are summarised in Table 1.

3.2.3. Key to Adults of Iranian Pear Psyllids; Modified from Burckhardt and Hodkinson (1986)

  1. Forewings longer than 2.8 mm; apex of clavus not brown (Figure 2f). Paramere longer than distal segment of aedeagus (Figure 3f)································································································································································································C. pyrisuga (Foerster)
    • -
      Forewings shorter than 2.7 mm; if longer (in some C. pyri adults) then clavus with apical brown patch (Figure 2a–e). Paramere as long as or shorter than distal segment of aedeagus (Figure 3a–e)································································································································2
  2. Paramere in profile sickle-shaped (Figure 3d). Dorsal margin of female proctiger in profile with strong constriction in the middle (Figure 4d) ····································································································································································································C. pyri (L.)
    • -
      Paramere in profile lamellar. Dorsal margin of female proctiger in profile cuneate························································································································································································································3
  3. Parameres with a long, forward-directed tooth and a shorter, inwardly directed tooth at apex; foremargin with a wide lobe (Figure 3a). Dorsal margin of female proctiger in profile with a small hump in the middle, apex blunt or subacute (Figure 4a) ···············································································································································································································C. bidens (Šulc)
    • -
      Paramere and aedeagus different. Dorsal margin of female proctiger in profile concave························································································································································································································4
  4. Paramere with a forward-directed apical tooth (Figure 3c). Female proctiger often clearly exceeding subgenital plate (Figure 4c) ········································································································································································C. permixta Burckhardt & Hodkinson
    • -
      Paramere with inwardly directed blunt apex. Female proctiger only slightly exceeding subgenital plate·····························································································································································································································5
  5. Forewings with white veins (Figure 1c). Body smaller (head width: 0.55–0.71 mm; forewing length: 1.38–2.09 mm; ratio of antennal length to head width: 1.12–1.57) ·······················································································································································C. notata (Flor)
    • -
      Forewings with yellow to brown or dark brown veins (Figure 1f). Body larger (head width: 0.60–0.73 mm; forewing length: 1.62–2.54 mm; ratio of antennal length to head width: 1.31–1.79) ··································································································C. pyricola (Foerster)*

* The presence of Cacopsylla pyricola in Iran remains unconfirmed. Although no reliably verified record currently confirms its occurrence in the country, the species is included in the identification key to facilitate its recognition.

3.3. Identification of Iranian Pear Psyllids Based on Molecular Characters

In total, COI sequences from ten Cacopsylla species were compared. The COI fragments obtained from two voucher specimens of C. permixta were successfully amplified and sequenced, and the resulting sequences were deposited in GenBank for the first time under accession numbers PZ344517 and PZ344518 (Table 2). The COI sequences of the remaining nine species were downloaded from GenBank and included in the comparative analyses (Table 2).

Table 2.

Accession numbers of COI sequences of pear psyllids (Cacopsylla spp.) analysed in the present study. The table compares species names under which the sequences were originally deposited in GenBank with identifications proposed by Cho et al. (2020) [68] and with the corrected identifications established in the present study. Accession numbers generated here for the first time are in bold and correspond to the COI sequences of true Cacopsylla permixta.

Accession Number in GenBank Species Name in GenBank Country Reference ID in Cho et al., 2020 ID in This Study
MK039595 C. bidens Slovenia Cho et al., 2020 [68] - -
MK039638–MK039639 C. burckhardti South Korea Cho et al., 2020 [68] - -
MK039614–MK039617 C. burckhardti South Korea Cho et al., 2020 [68] - -
MK039622–MK039625 C. jukyungi South Korea Cho et al., 2020 [68] - -
MK039600–MK039603 C. jukyungi South Korea Cho et al., 2020 [68] - -
MK039629–MK039630 C. maculatili Japan Cho et al., 2020 [68] - -
MK039626–MK039628 C. maculatili South Korea Cho et al., 2020 [68] - -
MK039604–MK039607 C. maculatili South Korea Cho et al., 2020 [68] - -
MK039608–MK039609 C. maculatili Japan Cho et al., 2020 [68] - -
MG988669 C. notata Bulgaria Percy et al., 2018 [72] - -
PZ344517 C . permixta Iran Present study - C . permixta
PZ344518 C . permixta Iran Present study - C . permixta
MK039632–MK039634 C. pyri Czech Republic Cho et al., 2020 [68] - -
MK039596–MK039599 C. pyri Czech Republic Cho et al., 2020 [68] - -
MG988672 C. pyri Percy et al., 2018 [72] - -
KU517192 C. pyri UK Hodgetts et al., 2016 [73] - -
KT258648–KT258649 C. pyricola Iran Zendedel 2015 [37] C. pyri C. pyri
OP899395–OP899403 C. pyricola Czech Republic Serbina et al., 2023 [74] - -
MT021781 C. pyricola UK Sumner-Kalkun et al., 2020 [75] - -
MK039635 C. pyricola Poland Cho et al., 2020 [68] - -
MK039591–MK039594 C. pyricola Czech Republic Cho et al., 2020 [68] - -
MK039590 C. pyricola Poland Cho et al., 2020 [68] - -
KT258635–KT258661 C. pyricola Iran Zendedel (2015) [37] C. bidens C. bidens
KP843860 C. pyricola Iran Zohdi & Hossini, 2015 (unpublished) [76] Cacopsylla sp. C. permixta
KP192848 C. pyricola Iran Zohdi & Hossini, 2015 (unpublished) [76] Cacopsylla sp. C. permixta
JF327670–JF327709 C. pyricola South Korea Kang et al., 2012 [77] C. jukyungi -
AF493566 C. pyricola France Agustí et al., 2003 [78] - -
MK039612–MK039613 C. pyrisuga Czech Republic Cho et al., 2020 [68] - -
MK039636–MK039637 C. sandolbaea South Korea Cho et al., 2020 [68] - -
MK039610–MK039611 C. sandolbaea South Korea Cho et al., 2020 [68] - -
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The interspecific K2P distances of the analysed sequences ranged from 11.94 to 22.65% (Supplementary Table S1). The lowest interspecific distance (11.94%) was observed between C. pyricola (MK039590–MK039594, MK039635, MT021781 and AF493566) and C. bidens (MK039595). The highest divergence (22.65%) occurred between C. bidens (KT258657) and C. burckhardti (MK039639).

According to our results, all GenBank entries labelled as ‘Cacopsylla pyricola’ from Iran (accession numbers KT258635–KT258661, KP192848 and KP843860) were misidentified. Based on our analysis, all sequences submitted by Zendedel (2015) [37] (except KT258648 and KT258649) belong to C. bidens. These sequences are genetically close to C. bidens from Slovenia [68], differing from the Slovenian sequences by a genetic distance of 1.08%. The two remaining sequences from Zendedel (2015) [37], KT258648 and KT258649, were identified as C. pyri and differed from other specimens of this species from the Czech Republic and the UK by genetic distances ranging from 3.84 to 4.12%. A substantial intraspecific genetic divergence was also observed between the Japanese and South Korean lineages of C. maculatili, with a genetic distance of 5.61%. The remaining two sequences (KP192848 and KP843860) were also misidentified and, based on our analysis, represent C. permixta, showing no genetic divergence from the C. permixta specimens sequenced in the present study (Figure 5, Supplementary Table S1).

Figure 5.

Figure 5

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Neighbour-joining tree based on Kimura 2-parameter COI genetic distances between ten Cacopsylla spp., associated with pear trees. Bootstrap support values are shown at the branch points and are based on 1000 replicates.

4. Discussion

The accurate identification of species is key to successful biological research [79], as misidentifications can lead to substantial problems in quarantine, pest management and control measures. DNA barcoding has become a widely used and effective tool for species identification [80] and has been successfully applied to numerous psyllid groups [68,81,82,83,84,85,86,87]. This method is particularly valuable for distinguishing taxa that lack distinct morphological differences or that exhibit seasonal or sexual dimorphism [80]. However, a major challenge in DNA barcoding studies is the misidentification of the specimens used to generate reference sequences. Therefore, it is crucial that new entries submitted to public databases such as BOLD and GenBank are accurately identified.

In pear psyllids, misidentifications are especially frequent because several species of the Cacopsylla pyri-group are morphologically similar, occur on the same host plants, and show seasonal dimorphism [12]. In addition, some records appear to have been based mainly on the occurrence of specimens in pear orchards rather than on a detailed examination of morphological characters. The newly generated COI sequences from morphologically identified specimens of C. permixta are particularly important, because they provide a reliable reference for this species and demonstrate that KP192848 and KP843860, previously labelled as C. pyricola in GenBank, were misidentified and actually belong to C. permixta.

In the present study, the sequences KT258648 and KT258649, which clustered within C. pyri, showed K2P distances of 3.84–4.12% from the other available C. pyri sequences. Similarly, the Japanese and South Korean lineages of C. maculatili exhibited substantial genetic divergence in the COI gene, with a K2P distance of 5.61% between the two lineages. Although these values exceed the approximately 3% threshold proposed for intraspecific divergence in pear psyllids, such levels of divergence have also been documented in C. maculatili. Cho et al. (2020) reported a maximum intraspecific divergence of 5.9% in C. maculatili [68]. Percy (2003), in her study of legume-feeding psyllids from the Canary Islands, suggested that high levels of intraspecific mitochondrial divergence may be associated with geographic population structure and historical patterns of dispersal and colonization [88]. Therefore, the relatively high COI divergence observed in the present study should not, by itself, be interpreted as evidence of species-level differentiation. The strong bootstrap support for the placement of KT258648 and KT258649 within the C. pyri clade, the clustering of the Japanese and South Korean C. maculatili lineages within the C. maculatili clade, and their geographic distribution are more consistent with pronounced intraspecific genetic differentiation. Nevertheless, additional independent evidence, particularly from nuclear markers and morphological characters, would be necessary to determine whether these divergent lineages represent geographically structured populations or distinct taxa.

In our study, we also found strong congruence among the molecular, morphological and biological evidence supporting the delimitation of the ten pear psyllid species. The highest genetic distances involved C. burckhardti and C. pyrisuga relative to the remaining taxa, reflecting their distinct morphology and biology. In accordance with the molecular results, C. burckhardti and C. pyrisuga differ from the other analysed species in having longer forewings (>3.0 mm), the absence of an apical brown patch on the clavus, and parameres that are relatively long in relation to the length of the distal segment of the aedeagus. The two species also differ biologically from the other species examined here. Members of the Cacopsylla pyri-group (seven species: C. bidens, C. jukyungi, C. maculatili, C. notata, C. permixta, C. pyri and C. pyricola) and the C. nigella-group (C. sandolbaea) do not migrate to conifers, overwinter on their host plants, and produce two or more generations per year. In contrast, C. burckhardti and C. pyrisuga migrate to conifers to overwinter and are univoltine [6,15,16]. Furthermore, C. sandolbaea was placed in a separate group. Morphologically, this species is distinct from the other analysed Cacopsylla species, having an almost entirely dark brown to black body and forewing membrane, with very dense surface spinules covering the entire membrane up to the veins. These morphological differences are also reflected in its molecular divergence from the remaining taxa. By contrast, the most similar species, both morphologically and molecularly, were C. bidens and C. pyricola.

In the faunistic literature, C. pyricola was reported from Iran by Ossiannilsson (1992) [51] and Burckhardt and Lauterer (1993) [28]. The latter record was considered doubtful and was based on only two females. The species was also reported by Zendedel (2015) [37] based on GenBank information, but without confirmation through morphological identification. The identifications reported by Ahmadi et al. (2012) [33] and Ezzati et al. (2017) [42] are also doubtful, as there is no evidence that they were morphologically confirmed (Table 1). At present, there is no confirmed evidence for the occurrence of C. pyricola in Iran. Its presence remains possible, but requires verification using reliably identified voucher specimens, preferably supported by COI sequences.

Taken together, our results show that COI barcoding is a generally useful tool for identifying and distinguishing pear psyllid species, particularly when combined with diagnostic morphological characters. However, the present study also demonstrates that GenBank entries should not be used uncritically for species identification, especially in taxonomically difficult groups. Public barcode databases are valuable only when sequences are linked to correctly identified voucher specimens. To improve our understanding of pear psyllids and to ensure effective management of these pests, their distributions, host plant relationships and biology need to be determined more precisely. Moreover, in Iran, a phytoplasma has been detected in infected pear trees [9], but no psyllid has yet been identified as its vector. Further research is therefore needed to determine whether C. bidens, C. permixta or C. pyri can act as vectors in Iran.

5. Conclusions

Based on the examination of COI sequences deposited in GenBank, we suggest that previous records of Cacopsylla pyricola from Iran are currently unconfirmed and likely represent misidentifications of other members of the C. pyri-group, particularly C. bidens, C. permixta or C. pyri, all of which occur widely in pear-producing areas of Iran.

These misidentifications likely result from three main factors: (1) a tendency to apply the names C. pyri or C. pyricola to any psyllid found in pear orchards without confirming its identity using morphological and/or molecular characters, (2) reliance on earlier studies that themselves contained misidentified material, and (3) errors in GenBank entries, including several sequences that were incorrectly attributed to C. pyricola.

We therefore strongly recommend that researchers consult expert taxonomists when accurate species-level identification is required, particularly for economically important pest species. For taxonomically problematic taxa, reliance on GenBank entries alone should be avoided.

Acknowledgments

We thank Daniel Burckhardt and Diana Percy for their valuable comments, suggestions and help, and the anonymous reviewers for their constructive comments on a previous version of the manuscript.

Abbreviations

The following abbreviations are used in this manuscript:

KGUT Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
NHMB Naturhistorisches Museum, Basel, Switzerland
MHNG Muséum d’histoire naturelle, Geneva, Switzerland.
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Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/insects17090915/s1. Supplementary Table S1. Interspecific and intraspecific K2P distances (COI gene fragment) of the analysed pear psyllids (see Table 2 for details on accession numbers).

insects-17-00915-s001.zip (99.6KB, zip)

Author Contributions

Conceptualization, M.L. and L.Š.S.; Methodology, M.L. and L.Š.S.; Software, M.L. and L.Š.S.; Validation, M.L.; Formal analysis, M.L. and L.Š.S.; Investigation, M.L. and L.Š.S.; Resources, M.L.; Data curation, M.L.; Writing—original draft, M.L.; Writing—review and editing, M.L. and L.Š.S.; Visualization, M.L.; Supervision, M.L.; Project administration, M.L.; Funding acquisition, M.L. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

The COI sequences of Cacopsylla permixta generated in this study are available in GenBank under accession numbers PZ344517 and PZ344518.

Conflicts of Interest

The authors declare no conflicts of interest.

Funding Statement

This research has been supported by the Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran, grant number 03.3359.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

insects-17-00915-s001.zip (99.6KB, zip)

Data Availability Statement

The COI sequences of Cacopsylla permixta generated in this study are available in GenBank under accession numbers PZ344517 and PZ344518.

Articles from Insects are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)

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