Abstract
Some jumping plant-lice species are economically important due to their capacity as vectors of phytopathogenic bacteria, for example phytoplasmas. Previous studies have identified 80 jumping plant-louse species from Hungary; however, little is known about their occurrence during winter. To extend our knowledge of overwintering sites of jumping plant-lice in Hungary, we sampled them from conifers in various regions of the country. One of our main objectives was to find Cacopsylla pruni (Scopoli, 1763), the vector of ‘Candidatus Phytoplasma prunorum' during winter.
The period of this study extended from 2014 to 2020 in the winter months. Insects were collected at 18 sampling sites from Borsod-Abaúj-Zemplén county to Somogy county, located at Alsótekeres, Balatonvilágos, Boldogkőváralja, Budakeszi, Fenyőfő, Gyöngyöspata, Kecskemét, Martonvásár, Mátra Mountain, Nagykovácsi, Nagyszakácsi, Páty, Piliscsaba, Somogytúr, Soroksár, Sóskút and Verpelét.
A total of 1,600 jumping plant-louse specimens belonging to 20 species and three families (Psyllidae, Aphalaridae and Triozidae) were collected and identified during the study. In the case of plum psyllid (C. pruni) four shelter sites were identified as new records for Hungary.
The most common species were Trioza remota, Cacopsylla melanoneura, Trioza urticae, Bactericera albiventris, C. pruni and Cacopsylla crataegi.
Introduction
Jumping plant-lice (Hemiptera, Psylloidea) are small plant sap sucking insects, feeding mainly on woody plants and leaves of herbaceous plants and shrubs. Adults of many jumping plant-louse species migrate from host plants to conifers as shelter plants for overwintering (Čermák and Lauterer, 2008; Hodkinson, 2009; Gallinger and Gross, 2018). After egg hatching larvae go through five instars to adults. Jumping plant-lice typically feed on a single host plant species (monophagous) or on a few related ones (oligophagous) (Ossiannilsson, 1992). Amongst these insects many species are multivoltine (mostly in tropical to warm temperate regions), while others exhibit univoltine or bivoltine life cycles (Brambila and Hodges, 2008).
Jumping plant-lice include about 4,000 described species so far (Burckhardt and Queiroz, 2020). Some species cause serious economic losses to crop plants (Hodkinson, 2009), either by phloem feeding and honeydew production or indirectly by transmission of phytopathogenic agents like phytoplasmas. For example, the 16SrX or apple proliferation group phytoplasmas are transmitted exclusively by jumping plant-lice from the genus Cacopsylla (Jarausch et al., 2019). These pathogens cause serious damage on several fruit trees in Europe and North America (Tedeschi et al., 2002; Frisinghelli et al., 2000; Carraro et al., 1998; Grbic, 1974; Mergenthaler et al., 2017).
To date, 80 species of Psylloidea have been reported from Hungary (Kontschán et al., 2020).
In most cases jumping plant-louse species were collected from their host plants (e. g. Ripka, 2010; Kontschán et al., 2021; Ripka et al., 2018; Ripka and Csóka, 2016; Ripka, 2012). Although Kontschán and Ripka (2019) collected jumping plant-lice also from their winter shelter plants, little is known about the overwintering sites of most jumping plant-louse species in Hungary. Therefore, the objective of this study was to survey coniferous trees during winter for evidence of jumping plant-lice. A better understanding of the Hungarian jumping plant-lice populations provides greater knowledge about their biology, distribution and abundance.
Material and methods
Jumping plant-lice were collected from conifers in winter months from 2014 to 2020 from 18 different localities in Hungary including the oldest pine stand in Hungary (Fenyőfő) (Fig. 1 and Table 1).
Overwintering sites of jumping plant-lice in Hungary. Blue and orange spots indicate known and newly discovered localities, respectively
Citation: Acta Phytopathologica et Entomologica Hungarica 57, 2; 10.1556/038.2022.00156
Overwintering sites of jumping plant-lice in Hungary. Blue and orange spots indicate known and newly discovered localities, respectively
Citation: Acta Phytopathologica et Entomologica Hungarica 57, 2; 10.1556/038.2022.00156
Overwintering sites of jumping plant-lice in Hungary. Blue and orange spots indicate known and newly discovered localities, respectively
Citation: Acta Phytopathologica et Entomologica Hungarica 57, 2; 10.1556/038.2022.00156
Collecting localities, methods of collections and date of collections
| Locality | County | GPS coordinates | Altitude | Method | Date of collection |
| Alsótekeres | Somogy | N46.956295 E18.187529 | 167 m | net | 27/02/2017 |
| Balatonvilágos | Somogy | N46.97982 E18.165774 | 144 m | net | 27/02/2017 |
| Boldogkőváralja | Borsod-Abaúj-Zemplén | 48°21′26″N 21°14′19″E | 230 m | net | 10/03/2017 |
| Budakeszi | Pest | N47.525943 E18.873417 | 290 m | GLSM* | 5/02/2020 |
| Fenyőfő | Győr-Moson-Sopron | N47.354385 E17.762146 | 275 m | net | 19/01/2017 |
| Gyöngyöspata | Heves | N47.839356 E19.727127 | 250 m | GLSM* net | 25/02/2020 |
| Kecskemét | Bács-Kiskun | N46.938928 E19.569771 | 130 m | net | 5/02/2018 |
| Martonvásár | Fejér | 47°19′14″N 18°46′53″E | 120 m | net | January 2014 and February 2015 |
| Mátra Mountain | Heves and Nógrád | N47.82830 E.19.96375, N47.89482 E.19.86206, N47.90099 E19.94519, N47.89583 E19.95316 | 365 m 770 m 650 m 580 m | GLSM* net | 4/03/2019, 20/02/2020 and 25/02/2020 |
| Nagykovácsi | Pest | N47.545278 E18.934167 | 310 m | net | 20/12/2015 |
| Nagykovácsi- Júlia-major | N47.54786 E18.93470 | 316 m | net | 20/12/2015 | |
| Nagyszakácsi | Somogy | N46.4897 E17.31956 | 136 m | net | 13/03/2020 |
| Páty | Pest | N47.507691 E18.850542 | 265 m | net | January 2016 |
| Piliscsaba | Pest | N47.617277 E18.891953 | 290 m | net | 29/02/2020 |
| Somogytúr | Somogy | N46.724453 E17.797446 | 180 m | net | beginning of March, 2015 |
| Soroksár | Pest | N47.40053 E19.15433 | 109 m | net | 19/01/2018 |
| Sóskút | Pest | N47.439378 E18.849831 | 140 m | net | winter months in 2015, 2016, 2018 and 2019 |
| Verpelét | Heves | N47.801022 E.20.196172 | 190 m | net | January 2018 |
*GLSM: garden leaf suction machine
One of our aims was to determine overwintering sites of Cacopsylla pruni (Scopoli, 1763) as no data are currently available for Hungary. Insect captures were carried out in various pure and mixed coniferous forests. Because there are very few coniferous forests in our country, insects were also collected from forestry nurseries, botanical gardens and individual conifer trees. A diverse range of habitats was sampled with different altitudes and vegetation types.
Insect samples were collected from the following conifer species: Norway spruce (Picea abies), Scots pine (Pinus sylvestris), Serbian spruce (Picea omorika), Nordmann fir (Abies nordmanniana), giant redwood (Sequoiadendron giganteum), Atlas cedar (Cedrus atlantica), common yew (Taxus baccata), Douglas fir (Pseudotsuga menziesii), European black pine (Pinus nigra), blue spruce (Picea pungens), savin juniper (Juniperus sabina), and Leyland cypress (Cupressocyparis leylandii).
Insects were collected with an insect net attached to a five-meter telescopic handle or with a garden leaf suction machine equipped with a flexible suction pipe attached to a spliced bamboo rod that can be adjusted to the height of trees (up to 10 m in height). Collected material was preserved in 70% ethanol. Species identification was carried out under an Olympus SZ40 stereo-microscope according to Ossiannilsson (1992), and Hodkinson and White (1979), and their classification/nomenclature was performed according to Burckhardt et al. (2021).
Results
Described in Table 2, a total of 1,600 jumping plant-louse specimens belonging to 20 species and three families (Psyllidae, Aphalaridae and Triozidae) were collected and identified during the study.
Jumping plant-lice species collected at overwintering sites in Hungary during winter months from 2014 to 2020
| Collection sites | Plant species | Jumping plant-lice species collected (number of specimens in brackets) | Date of collection |
| Alsótekeres | Serbian spruce | A. avicularis (1), A. polygoni (5) | 27/02/2017 |
| Nordmann fir | B. albiventris (2), C. melanoneura (1), T. remota (2) | ||
| savin juniper | T. remota (4), T. urticae (1) | ||
| blue spruce | B. albiventris (1), C. melanoneura (1), T. urticae (1), T. remota (7) | ||
| Balatonvilágos | Norway spruce | A. avicularis (1), B. albiventris (3), C. melanoneura (2), T. remota (22), T. urticae (6) | 27/02/2017 |
| Leyland cypress | T. urticae (4), T. remota (5) | ||
| Scots pine | A. polygoni (1), B. albiventris (1), C. melanoneura (1), T. remota (9) | ||
| Boldogkőváralja | Scots pine | A. avicularis (1), A. polygoni (3), T. remota (4) | 10/03/2017 |
| Budakeszi arborétum | Norway spruce | B. albiventris (3), C. pyricola (1), T. remota (16), T. urticae (1) | 05/02/2020 |
| Douglas-fir | A. avicularis (1), A. calthae (1), A. polygoni (1), B. albiventris (2), C. melanoneura (5), C. pruni (2), T. remota (28), T. urticae (1) | ||
| giant redwood | C. melanoneura (1) | ||
| Serbian spruce | C. melanoneura (3), T. remota (7), B. albiventris (1) | ||
| Atlas cedar | T. remota (1) | ||
| Leyland cypress | T. urticae (1) | ||
| Scots pine | A. avicularis (1), B. albiventris (2), C. melanoneura (7), T. remota (18) | ||
| Fenyőfő | Scots pine | B. albiventris (1), C. melanoneura (5), T. urticae (82) | 19/01/2017 |
| Gyöngyöspata | Norway spruce | B. albiventris (4), C. melanoneura (1), C. pruni (2), T. remota (12), T. rhamni (1), T. urticae (4) | 25/02/2020 |
| Kecskemét | Scots pine | B. albiventris (12), T. remota (31), T. urticae (2) | 05/02/2018 |
| Martonvásár | Norway spruce | T. remota (1) | 02/2015 |
| Scots pine | T. remota (1) | 01/2014 | |
| Mátra Mountain | Norway spruce | A. calthae (6), B. albiventris (8), B. curvatinervis (1), B, femoralis (1), C. crataegi (4), C. melanoneura (18), C. peregrina (4), C. pruni (12), C. pyrisuga (4), C. rhamnicola (2), T. apicalis (2), T. remota (104), T. rotundata (1), T. rhamni (2), T. urticae (10) | 04/03/2019 |
| A. avicularis (2), A. calthae (1), B. albiventris (12), C. crataegi (5), C. melanoneura (108), C. pruni (8), C. pyrisuga (1), T. remota (199), T. urticae (22) | 20/02/2020 | ||
| European black pine | C. crataegi (2), C. melanoneura (24), C. pyricola (2), C. rhamnicola (2), T. remota (40) | 04/03/2019 | |
| Scots pine | B. albiventris (2), C. melanoneura (4), T. remota (141), T. urticae (5), | 04/03/2019 | |
| A. avicularis (1), A. polygoni (1), B. albiventris (34), C. crataegi (2), C. melanoneura (6), T. neglecta (1), T. remota (34), T. urticae (2) | 25/02/2020 | ||
| Nagykovácsi | Norway spruce | T. remota (7) | 20/12/2015 |
| Nagykovácsi-Júlia-major | Norway spruce | A. polygoni (10), B. albiventris (1), C. crataegi (1), C. melanoneura (4), T. urticae (8), T. remota (87) | 20/12/2015 |
| common yew | T. urticae (1) | ||
| Nagyszakácsi | Norway spruce | C. melanoneura (1), C. pruni (1) | 13/03/2020 |
| Páty | Scots pine | B. albiventris (8), C. crataegi (1), T. remota (17), T urticae (1) | 01/2016 |
| Piliscsaba | Norway spruce | B. albiventris (1), A. calthae (1) | 29/02/2020 |
| Somogytúr | Norway spruce | T. urticae (1) | 03/2015 |
| savin juniper | C. melanoneura (1) | ||
| Scots pine | A. polygoni (1), C. melanoneura (2), T. urticae (1), T. remota (44) | ||
| Soroksár | European black pine | A. polygoni (1), B. albiventris (1), C. melanoneura (2), T. urticae (3), T. remota (8) | 19/01/2018 |
| savin juniper | T. remota (1) | ||
| Norway spruce | A. polygoni (1), T. remota (1) | ||
| Sóskút | Scots pine | T. urticae (2) | winter months 2016 |
| A. polygoni (1), B. albiventris (1), C. melanoneura (3), T. remota (23), T. urticae (2) | winter months 2018 | ||
| C. melanoneura (1), T. remota (9), T. urticae (2) | winter months 2019 | ||
| Norway spruce | B. albiventris (1), T. urticae (1), T. remota (4), | winter months 2015 | |
| Verpelét | Scots pine | A. polygoni (2), B. albiventris (5), C. melanoneura (14), C. crataegi (2), C. saliceti (3), T. remota (88), T. urticae (2) | 01/2018 |
The most common species were Trioza remota (972 specimens), Cacopsylla melanoneura (221), Trioza urticae (174), Bactericera albiventris (106), Cacopsylla pruni (25), and Cacopsylla crataegi (17).
Special attention was paid to the plum psyllid (C. pruni) that was found in Mátra Mountain, Gyöngyöspata, Nagyszakácsi and in the Budakeszi arboretum on Norway spruce and Douglas fir.
Thirteen of the collected jumping plant-louse species are known to feed on woody plants, while 7 species on herbaceous hosts. Some species feeding on woody host plants have a great importance as vectors of phytoplasmas: Cacopsylla pruni, Cacopsylla melanoneura (Foerster, 1848), Cacopsylla pyricola (Foerster, 1848), Cacopsylla pyrisuga (Foerster, 1848).
The following species were identified: Aphalara avicularis (Ossiannilson, 1981), Aphalara calthae (Linnaeus, 1761), Aphalara polygoni (Foerster, 1848), Bactericera albiventris (Foerster, 1848), Bactericera curvatinervis (Foerster, 1848), Bactericera femoralis (Foerster, 1848), Cacopsylla crataegi (Schrank, 1801), Cacopsylla melanoneura, Cacopsylla peregrina (Foerster, 1848), Cacopsylla pruni (Scopoli, 1763), Cacopsylla pyricola (Foerster, 1848), Cacopsylla pyrisuga, Cacopsylla rhamnicola (Scott, 1876), Cacopsylla saliceti (Foerster, 1848), Trioza apicalis (Foerster, 1848), Trioza neglecta (Loginova, 1978), Trioza remota (Foerster, 1848), Trioza rhamni (Schrank, 1801), Trioza rotundata (Flor, 1861) and Trioza urticae (Linnaeus, 1758).
The number of jumping plant-louse species collected from a certain shelter plant species are presented in Table 3.
Jumping plant-louse species found on overwintering/shelter plant species during winter months from 2014 to 2020
| Overwintering/shelter plant species | Number of collected jumping plant-louse species per plant species |
| Serbian spruce | 5 (A. avicularis, A. polygoni, C. melanoneura, T. remota, B. albiventris) |
| Nordmann fir | 3 (A. albiventris, C. melanoneura, T. remota) |
| savin juniper | 3 (T. remota, T. urticae, C. melanoneura) |
| blue spruce | 4 (B. albiventris, C. melanoneura, T. urticae, T. remota) |
| Norway spruce | 18 (A. avicularis, B. albiventris, C. melanoneura, T. remota, T. urticae, C. pyricola, C. pruni, T. rhamni, A. polygoni, C. crataegi, A. calthae, B. curvatinervis, B. femoralis, C. peregrina, C. pyrisuga, C. rhamnicola, T. apicalis, T. rotundata,) |
| Leyland cypress | 2 (T. urticae, T. remota) |
| Scots pine | 9 (A. polygoni, B. albiventris, C. melanoneura, T. remota, A. avicularis, T. urticae, C. crataegi, T. neglecta, C. saliceti) |
| Douglas fir | 7 (A. avicularis, A. calthae, A. polygoni, B. albiventris, C. melanoneura, T. remota, T. urticae) |
| giant redwood | 1 (C. melanoneura) |
| Atlas cedar | 1 (T. remota) |
| common yew | 1 (T. urticae) |
| European black pine | 8 (C. crataegi, C. melanoneura, C. pyricola, C. rhamnicola, T. remota, A. polygoni, B. albiventris, T. urticae) |
Discussion
Jumping plant-lice collected on conifers in Hungary was dominated by Trioza and Cacopsylla species in agreement with literature data (Ripka et al., 2018 and references therein, Kontschán et al., 2020). Among the Cacopsylla species found, C. pyricola (Tedeschi and Alma, 2004), C. pyrisuga (Grbic, 1974), C. melanoneura (Tedeschi and Alma, 2004; Frisinghelli et al., 2000; Tedeschi et al., 2002) and C. pruni (Carraro et al., 1998; Mergenthaler et al., 2017) play a pivotal role in transmission of phytoplasmas associated with serious plant diseases.
In this study we recorded 20 out of the 80 jumping plant-louse species reported from Hungary. The new and the previously reported overwintering sites are shown in Fig. 1. One species, Trioza neglecta is known as a non-native species in Hungary (Lauterer and Janiček, 1990; Kontschán et al., 2020).
Although C. melanoneura was reported to overwinter at Kék in Hungary (Kontschán and Ripka, 2019), we found it at ten new localities.
Four overwintering sites of C. pruni, the vector of ‘Candidatus Phytoplasma prunorum' were identified: Mátra Mountain, Budakeszi arboretum, Gyöngyöspata and Nagyszakácsi.
We also found 14 new overwintering sites of T. urtice which was previously known only from Budapest, Martonvásár and Kék (Kontschán and Ripka, 2019).
Prior to this study there were no known overwintering sites in Hungary for the following 14 species: A. avicularis, A. calthae, A. polygoni, C. rhamnicola, C. saliceti, B. curvatinervis, B. albiventris, B. femoralis, T. neglecta, T. remota, T. rhamni, and T. rotundata. New overwintering sites (Mátra Mountain) and plant (Norway spruce) was found for C. peregrina, C. pyricola, C. pyrisuga and T. apicalis.
The overwintering sites of jumping plant-lice are relatively poorly studied in Hungary, and collection data provided in this work includes additional information about the overwintering sites of jumping plant-louse species in Hungary, which broadens our knowledge of the regional jumping plant-lice fauna.
Acknowledgements
Thanks for the participation of Emese Kiss Tibenszkyné, Szilvia Orosz (National Food Chain Safety Office, Food Chain Safety Laboratory Directorate, Plant Health Diagnostic National Reference Laboratory), Balázs Kiss and Gergely Tholt (Plant Protection Institute, Centre of Agricultural Research, Department of Zoology) for their participation in insect collections. Thanks to András Koltay (Forest Research Institute, University of Sopron) and Sándor Lukács (Budakeszi Arboretum) for their permit and technical support.
This project was supported in 2019 and 2020 by (NKFIH) K 128838.
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