The psyllid fauna (Hemiptera: Psylloidea) of vegetable fields in Brazil

ABSTRACT

Some psyllids transmit 'Candidatus Liberibacter solanacearum' (Lso), the causal agent of devastating plant diseases of cultivated Solanaceae and Apiaceae. The recent detection of Bactericera cockerelli and Lso in Ecuador seriously threatens these crops in South America. There, neither the role of native psyllids in the Lso epidemiology nor the psyllid fauna of vegetables are known. With the aim to identify potential vectors and risk scenarios for the spread of Lso in South America, a survey of the psyllid fauna of Solanaceae and Apiaceae crops and associated weeds was conducted in Brazil. Samples were taken at 29 localities in four states. A total of 2857 specimens were sampled, representing at least 37 species of 23 genera and seven families. The most frequent species on carrot, chilli pepper and potato were Russelliana solanicola, R. capsici and Isogonoceraia divergipennis, respectively. Immatures of R. capsici were found on chilli pepper and of R. solanicola on carrot and potato, confirming these plants as hosts. The two psyllid species have been suspected previously to transmit plant pathogens of unknown identity. Russelliana solanicola is one of the few polyphagous species. Here the species is reported for the first time from carrot. Recent collections in Rio Grande do Sul suggest that Solanum laxum represents the original host of R. capsici, which subsequently shifted to chilli pepper. Both, adaptation to agricultural crops and the possibility of ability to transmit pathogens, make the two Russelliana species dangerous potential vectors of Lso and other plant pathogens in South America.

Keywords:
Psyllid vectors; Host plants; Carrot; Chilli pepper; Potato; South America; New host records; New state records

Introduction

Jumping plant-lice or psyllids (Hemiptera: Psylloidea) are small phloem-sucking insects. Most of the approximately 4000 described species are highly host specific with only a few exceptions (Burckhardt et al., 2014; Ouvrard et al., 2015). While immatures can complete their development usually only on one or a few closely related plant species (=host plants), adults, which are always winged and therefore more mobile, can be encountered often also on non-hosts, called overwintering, shelter, food, or casual plants depending on the situation (Burckhardt et al., 2014). Some psyllids are economically important pests in agriculture, forestry and horticulture. The damage to plants can be direct or indirect. The most devastating damage is inflicted by those species that transmit plant pathogens (Burckhardt, 1994; Hodkinson, 2009; Queiroz et al., 2012)

Over the last decades, some psyllid species have emerged as major pests of vegetables, mainly as vectors of ‘Candidatus Liberibacter solanacearum’ (Lso), the putative etiological agent of potato zebra chip and other disorders in Solanaceae and Apiaceae. The tomato-potato psyllid, Bactericera cockerelli (Šulc), one of the few polyphagous psyllid species (Burckhardt and Lauterer, 1997; Serbina et al., 2015), is notorious as a vector of Lso infecting potatoes and other Solanaceae in North and Central America as well as in New Zealand (Liefting et al., 2009; Munyaneza, 2012). Recently, B. cockerelli and later Lso also were detected in South America (Castillo Carrillo et al., 2019; Caicedo et al., 2020). Bactericera trigonica Hodkinson and Dyspersa apicalis (Foerster) (=Trioza apicalis) transmit other haplotypes of Lso to carrots and other members of Apiaceae in Europe and the Mediterranean including the Canary Islands (Munyaneza et al., 2010; Alfaro-Fernández et al., 2012; Tahzima et al., 2014; Teresani et al., 2014; Mawassi et al., 2018). Furthermore, Bactericera nigricornis currently found in Europe and Asia has shown to be capable of transmiting Lso to potato and carrots (Moreno et al., 2021).

Bactericera cockerelli and Lso, which were recently discovered in Ecuador, represent a serious threat to the potato industry in South America (Castillo Carrillo et al., 2019; Caicedo et al., 2020). Recently the vector was also reported from Colombia and Peru but not Lso (ICA, 2021; SENASA, 2021). In the west Palaearctic, Lso infects other crops such as carrot and celery transmitted by native psyllids. This may happen also in South America. From South America, two Russelliana species, viz. R. capsici Burckhardt and R. solanicola Tuthill, are suspected to vector plant pathogens. Russelliana capsici (Figs 1A, B) was reported from Argentina (Buenos Aires, Entre Ríos) and Brazil (Minas Gerais, Pananá, Santa Catarina, São Paulo) associated with witches’ brooms on chilli pepper. It is suspected that the witches’ brooms are caused by a Candidatus Liberibacter or Phytoplasma species (Burckhardt et al., 2012). Russelliana solanicola (Figs 1C, D) was reported as pest on potato and as vector of an unidentified pathogen causing ‘Potato Yellows’ (Tuthill, 1959; Chávez et al., 2003; Salazar, 2006). It is known from Argentina, Bolivia, Brazil, Chile, Peru and Uruguay (Serbina and Burckhardt, 2017) and represents another one of the few polyphagous psyllid species, associated with several families of eudicots (clade Caryophyllales + asterids) (Serbina et al., 2015).

Figure 1
Habitus of Russelliana species; A) R. capsici Burckhardt, adult; B) R. capsici immature; C) R. solanicola Tuthill, adult; D) R. solanicola, immature. (Photos A, C, D: T.M.A. Kuhn; B: D.L. Queiroz).

As these plant pathogens are often controlled via their vectors, a better knowledge of the psyllid fauna of vegetable crops in South America is imperative and a matter of urgency. From Brazil, only 165 species of Psylloidea have been reported, of an estimated 1000 species that potentially occur there (Burckhardt and Queiroz, 2012, 2020, 2023). Similarly, there is a general lack of information on the psyllid fauna of vegetable crops in Brazil, making predictions about potential psyllid vectors of Lso difficult or even impossible. For closing this gap, a survey was conducted, sampling psyllids in vegetable fields in 16 important production areas in the Center-South region of Brazil with the aim to identify potential vector species of Lso and other phloem restricted plant pathogens.

Material and methods

From 2014 to 2016, vegetable fields at 87 localities were studied, and psyllids were found at 29 localities in 16 municipalities and four states of the Center-South region of Brazil (Table 1, Supplementary Material). The samples were taken using direct (visual inspection of plant, sweep net or beating tray) and indirect methods (yellow tray water trap).

Table 1
Collecting sites and dates of psyllid fauna collection (Hemiptera: Psylloidea) from vegetable fields in Brazil. GO = Goiás; PR = Paraná; MG = Minas Gerais; SP = São Paulo. Asterisks indicate localities with yellow tray water traps. Crop species: - Apiaceae: carrot (Daucus carota L.), celery (Apium graveolens L.), parsley [Petroselinum crispum (Mill.) Fuss]; - Solanaceae: African eggplant (Solanum aethiopicum Jacq.), chilli pepper (Capsicum chinense Jacq.), eggplant (Solanum melongena L.), potato (Solanum tuberosum L.), tobacco (Nicotiana tabacum L.).

State	Municipality	Locality	Geographical coordinates	Altitude	Collecting dates	Crop species
GO	Campo Alegre de Goiás	Projeto Paineiras, Yokio	‑17.300443 ‑47.883381	946 m	29.ix.2015	potato
GO	Cristalina	Fazenda Santa Bárbara, Pivô 28	‑16.219014 ‑47.467233	981 m	30.ix.2015	carrot
GO	Cristalina	Fazenda Santa Bárbara, Pivô 29	‑16.222222 ‑47.469167	970 m	30.ix.2015	carrot
MG	Cristina	Produtor José Paulo Rocha	‑22.300000 ‑45.270000	1280 m	03.vi.2015	potato
MG	Maria da Fé	Produtor Roberto Teodoro da Silva	‑22.303889 ‑45.380000	1200 m	03.vi.2015	carrot
MG	Maria da Fé	*Sítio Alvorada	‑22.290808 ‑45.333884	1351 m	29.ix-03.xii.2015, 20.xi.2015	carrot, potato
MG	Maria da Fé	Sítio Nossa Senhora Aparecida	‑22.294219 ‑45.357400	1326 m	31.viii.2015	carrot
MG	Perdizes	Fazenda Rosário	‑19.396869 ‑47.339022	1088 m	26.xi.2015	carrot
MG	Perdizes	Grupo Bergamasco	‑19.394444 ‑47.332222	1070 m	26.xi.2015	carrot
MG	Perdizes	Grupo Rocheto	‑19.317625 ‑47.395625	1065 m	20.xi.2014	potato
MG	Perdizes	*Grupo Rocheto, Pivô 19	-19.368556 -47.383306	1041 m	13.viii-30.x.2015	potato
MG	Perdizes	*Grupo Rocheto, Pivô 30	-19.347750 -47.401139	1013 m	13.viii-30.x.2015	potato
MG	Rio Paranaíba	Produtor Elcio Tamekuni	‑19.301988 ‑46.261992	1139 m	05.viii.2015	carrot
MG	Rio Paranaíba	Produtor Leandro Fukuda	‑19.292392 ‑46.154611	1164 m	13.v.2015	carrot
MG	Santa Juliana	Horta urbana	‑19.309378 ‑47.529381	938 m	04.iii.2016	chilli pepper
MG	Tapiraí	Grupo Nascente	‑19.871111 ‑46.269722	1255 m	19.xi.2014	potato
PR	Castro	Área Madureira	‑24.824722 ‑49.895833	1000 m	20.iii.2015	potato
PR	Irati	Sítio Novo	‑25.480250 ‑50.647611	928 m	03.xii.2015	tobacco
SP	Campinas	*Fazenda Santa Elisa, IAC	‑22.858333 ‑47.080556	694 m	19.i-08.v.2015	potato
SP	Casa Branca	Campo Alegre, Pivô dos Macacos	‑21.762292 ‑47.154736	696 m	23.ix.2015	carrot
SP	Casa Branca	Grupo Rocheto, Área Bolinha	‑21.756389 ‑47.161944	695 m	23.ix.2015	potato
SP	Ibiúna	Marcio Hideriha, Talhão do Barracão	‑23.662778 ‑47.348333	880 m	12.v.2016	carrot
SP	Ibiúna	Sítio Dona Edna	‑23.721428 ‑47.192861	873 m	12.v.2016	parsley
SP	Ibiúna	Sítio Katahira	‑23.646667 ‑47.171667	860 m	12.v.2016	celery
SP	Piracicaba	*ESALQ, Entomologia	‑22.713389 ‑47.625822	538 m	12.ix-29.x.2014, 23.viii-21.ix.2016	chilli pepper, African eggplant, eggplant, potato
SP	Piracicaba	ESALQ, PACES	‑22.704997 ‑47.634306	540 m	21.ix.2016	potato
SP	São José do Rio Pardo	Sítio dos Médicos	‑21.680000 ‑46.960833	760 m	24.ix.2015	carrot
SP	São José do Rio Pardo	Sítio São Teodoro	‑21.683839 ‑46.950458	709 m	24.ix.2015	carrot
SP	Sorocaba	Produtor Claudenir	‑23.525964 ‑47.546103	579 m	16.iv.2015	eggplant

For the visual inspection, 5‒10 plants per species were examined for approximately one minute in each sampled area, counting the number of adult psyllids and checking for the presence or absence of immatures. With the sweep net and beating tray, 10 samples were taken consisting of 10 sweeps and four beats, respectively. In most localities, sampling using direct methods was performed on a single date, except for Piracicaba where samples were taken at nine dates (Supplementary Material). The psyllids were collected with an entomological aspirator and placed in vials with 70% ethanol for preservation. Eleven crop species and five weed species were examined (Table 2). The plant species varied according to their availability at different localities and sampling dates. Weeds, when present in pure clusters in or adjacent to the field, were sampled with a sweep net.

Table 2
Crops and weed species sampled during the collection of psyllid fauna (Hemiptera: Psylloidea) from vegetable fields in Brazil.

Family	Latin name	Common name
Crops
Apiaceae	Apium graveolens L.	celery
Apiaceae	Daucus carota L.	carrot
Apiaceae	Petroselinum crispum (Mill.) Fuss	parsley
Brassicaceae	Brassica oleracea var. capitata L.	cabbage
Solanaceae	Capsicum annum L.	bell pepper
Solanaceae	Capsicum chinense Jacq.	chilli or bonnet pepper, Chinese capsicum and many others
Solanaceae	Nicotiana tabacum L.	tobacco
Solanaceae	Solanum aethiopicum Jacq.	African or Ethiopian eggplant
Solanaceae	Solanum lycopersicum L.	tomato
Solanaceae	Solanum melongena L.	eggplant
Solanaceae	Solanum tuberosum L.	potato
Weeds
Amaranthaceae	Amaranthus sp.	pigweed
Asteraceae	Bidens pilosa L.	hairy beggarticks and many others
Asteraceae	Melampodium perfoliatum (Cav.) Kunth	perfoliate blackfoot
Asteraceae	Parthenium hysterophorus L.	ragweed parthenium and many others
Solanaceae	Solanum americanum Mill.	American black nightshade

Each two yellow tray water traps were installed at approximately 60 cm above ground at three municipalities and four at one municipality (Table 1, asterisk). They were filled with 500 ml water and 3 ml of liquid detergent. The insects were collected every seven days during the sampling period, which varied between the locality (Supplementary Material): Campinas, SP (15 weeks), Maria da Fé, MG (9 weeks), Perdizes, MG (13 weeks) and Piracicaba, SP (8 weeks). The insects were sifted, manually sorted and preserved in 70% ethanol.

The psyllids were identified to genus and, if possible, to species. Voucher specimens are deposited in the Naturhistorisches Museum Basel, Switzerland (NHMB). The following additional material of Russelliana capsici collected by DB and DLQ was examined (NHMB):

Brazil: GO: 3 ♂, 1 ♀, 1 immature, 9 km NE Mossâmedes, Fazenda Ribeirão Bonito, ‑16.1150 ‑50.1972, 640 m, 20.ii.2018, chilli pepper, #274(6). - MS: 18 ♂, 29 ♀, 2 immatures, 1 skin, Rio Verde do Mato Grosso, BR163, ‑18.9281/9519 ‑54.8357/9339, 350-440 m, 13.xi.2012, chilli pepper, #68(6). - PR: 2 ♂, 7 immatures, 1 skin, Curitiba, Boa Vista, ‑25.3941 ‑49.2474, 930 m, 7.x.2018, chilli pepper, #312(1); 23 ♂, 17 ♀, 24 immatures, 2 skins, same but Jardim Botânico, ‑25.4437 ‑49.2391, 930 m, 19.vii.2012, chilli pepper, #44(2); 6 ♂, 5 ♀, 4 immatures, same but 15.ii.2013, chilli pepper, #94(9); 3 ♂, 4 ♀, same but Parque Bacacheri, ‑25.3900 ‑49.2303, 920 m, 6.iv.2013, chilli pepper, #98(3); 1 ♀, same but Parque Barigui, ‑25.4268 ‑49.3099, 900 m, 19.vii.2012, #43(-); 1 ♂, 4 ♀, same but Parque Passaúna, ‑25.4756 ‑49.3777, 930 m, 27-30.xi.2012, chilli pepper, #78(2); 5 ♂, 8 ♀, 11 immatures, 1 skin, same but Parque Passaúna, ‑25.5736 ‑48.9893, 940 m, 5.ii.2013, chilli pepper, #89(8); 9 ♂, 19 ♀, 1 immature, same but Parque Tanguá, ‑25.3810 ‑49.2848, 930 m, 6.ii.2013, chilli pepper, #90(16); 2 ♂, 1 ♀, same but Parque Tingui, ‑25.3887/3953 ‑49.3061/3062, 910-920 m, 31.i.2016, chilli pepper, #189(9). - RJ: 1 immature, Rio de Janeiro, Jardim Botânico, ‑22.9695 ‑43.2242, 10 m, 12.iv.2019, chilli pepper, #326(2); RS: 3 ♀, Barra do Quaraí, Parque Estadual do Espinilho, ‑30.1914 ‑57.5285, 50 m, 15.ix.2018, Solanum laxum Spreng., #294(7); 3 ♀, same but ‑30.1958 ‑57.5284, 60 m, 15.ix.2018, Solanum laxum, #295(2); 66 ♂, 43 ♀, 16 immatures, same but Saladeira/along Rio Quaraí, ‑30.2078 ‑57.5586, 50 m, 15.ix.2018, Solanum laxum, #297(1); 1 ♂, 2 ♀, Passo Fundo, Embrapa, campus, ‑28.2288 ‑52.4065, 640 m, 20.ix.2018, Solanum laxum, #306(7); RS, 5 ♂, 3 ♀, Santana do Livramento, Cerro Verde, ‑30.7784 ‑55.5808, 280 m, 11.ix.2018, Solanum laxum, #288(9); 1 ♀, same but near BR293, ‑30.7807 ‑55.6384, 310 m, 12.ix.2018, Solanum laxum, #290(7); RS, 1 ♂, 1 ♀, São Francisco de Assis, RS377 km 303, ‑29.4827 ‑55.0613, 290 m, 18.ix.2018, Solanum laxum, #304(7). - SP: 1 ♂, 4 ♀, Nova Odessa, Jardim Botânico Plantarum, ‑22.7788 ‑47.3142, 560 m, 3.iv.2019, chilli pepper, #314(1).

The nomenclature of psyllids follows Ouvrard (2022) and that of the plants the World Flora Online (WFO, 2022). The classification of psyllids is that of Burckhardt and Queiroz (2023).

Results

During the survey, 2857 specimens (2818 adults and 39 immatures) were collected, representing at least 37 species of 23 genera and six families (Table 3). Of these, specimens representing 23 species could be identified to species, and the remainder only to genus or species group. These latter 14+ species represent undescribed species (e.g. Mitrapsylla) or species complexes (e.g. Euceropsylla), and describing and revising these is beyond the scope of the present study. The Brazilian psyllid fauna is poorly known and perhaps only 10% of the existing species are described (Burckhardt and Queiroz, 2012, 2020, 2023). Overall, the most frequent species were R. solanicola, Isogonoceraia divergipennis White and Hodkinson and R. capsici with 73%, 10% and 3%, respectively, of the total number of adult specimens collected (Tables 4 and 5). None of the currently known vectors of Lso, e.g. Bactericera species, were present in our collections, but two species were found that are suspected to vector plant pathogens, i.e. R. capsici and R. solanicola (Burckhardt et al., 2012; Serbina et al., 2015).

Table 3
Psyllids collected during the project with their known host plants and general distribution. Asterisks indicate the assumed host family for psyllid taxa that were not identified to species.

Psyllid family	Psyllid subfamily	Psyllid species	Host family	Host species	Distribution
Aphalaridae	Phacopteroninae	Pseudophacopteron longicaudatum Malenovský, Burckhardt, Queiroz, Isaias & Oliveira, 2015	Apocynaceae	Aspidosperma spp.	Brazil
Aphalaridae	Rhinocolinae	Leurolophus oriformae Burckhardt & Basset, 2000	Anacardiaceae	Lithraea spp.	Argentina, Brazil
Aphalaridae	Spondyliaspidinae	Blastopsylla occidentalis Taylor, 1985	Myrtaceae	Eucalyptus spp.	Australia; adventive in Africa, America, Asia, Europe and Oceania
Aphalaridae	Spondyliaspidinae	Ctenarytaina spatulata Taylor, 1997	Myrtaceae	Eucalyptus spp.	Australia; adventive in America, Europe and Oceania
Aphalaridae	Spondyliaspidinae	Glycaspis brimblecombei Moore, 1964	Myrtaceae	Eucalyptus spp.	Australia; adventive in Africa, America, Asia, Europe and Oceania
Carsidaridae	Carsidarinae	Paracarsidara sp.	*Malvaceae	-	-
Liviidae	Liviinae	Diclidophlebia crassiflagellata (Burckhardt, 1996)	Malvaceae	Luehea paniculata Mart.	Brazil, Paraguay
Liviidae	Liviinae	Diclidophlebia sp.	-	-	-
Mastigimatidae		Mastigimas anjosi Burckhardt, Queiroz, Queiroz, Andrade, Zanol, Rezende & Kotrba, 2011	Meliaceae	Cedrela fissilis Vell., Toona ciliata M.Roem.	Brazil, Trinidad, Venezuela
Mastigimatidae		Mastigimas sp.	*Meliaceae	-	-
Psyllidae	Aphalaroidinae	Baccharopelma dracunculifoliae Burckhardt, Espírito-Santo, Fernandes & Malenovský, 2004	Asteraceae	Baccharis dracunculifolia DC.	Argentina, Brazil, Paraguay
Psyllidae	Aphalaroidinae	Russelliana capsici Burckhardt, 1987	Solanaceae	Capsicum annuum L., Solanum laxum Spreng.	Argentina, Brazil
Psyllidae	Aphalaroidinae	Russelliana solanicola Tuthill, 1959	polyphagous	polyphagous	Argentina, Bolivia, Chile, Peru; presumable adventive in Brazil and Uruguay
Psyllidae	Ciriacreminae	Caradocia longiantennata White & Hodkinson, 1980	Anacardiaceae	Tapirira guianensis Aubl.	Brazil
Psyllidae	Ciriacreminae	Caradocia sp.	*Anacardiaceae	-	-
Psyllidae	Ciriacreminae	Euceropsylla martorelli (Caldwell, 1944) group	*Fabaceae	-	-
Psyllidae	Ciriacreminae	Euceropsylla russoi Boselli, 1929 group	*Fabaceae	-	-
Psyllidae	Ciriacreminae	Heteropsylla caldwelli Burckhardt, 1987	Fabaceae	Albizia adinocephala (Donn.Sm.) Record, A. edwallii (Hoehne) Barneby & J.W. Grimes, Enterolobium contortisiliquum (Vell.) Morong, E. cyclocarpum (Jacq.) Griseb., Senegalia polyphylla (DC.) Britton	Argentina, Brazil, Colombia, Costa Rica, Nicaragua, Panama, Paraguay
Psyllidae	Ciriacreminae	Heteropsylla cubana Crawford, 1914	Fabaceae	Leucaena spp.	America; adventive in Africa, Asia, Australia and Oceania
Psyllidae	Ciriacreminae	Heteropsylla spinulosa Muddiman, Hodkinson & Hollis, 1992	Fabaceae	Mimosa diplotricha Sauvalle	Brazil; adventive in Australia and Oceania
Psyllidae	Ciriacreminae	Heteropsylla tenuata Muddiman, Hodkinson & Hollis, 1992	Fabaceae	Enterolobium contortisiliquum (Vell.) Morong	Brazil
Psyllidae	Ciriacreminae	Heteropsylla sp.	*Fabaceae	-	-
Psyllidae	Ciriacreminae	Isogonoceraia divergipennis White & Hodkinson, 1980	Fabaceae	Caesalpinia pluviosa DC.	Brazil
Psyllidae	Ciriacreminae	Isogonoceraia sp.	*Fabaceae	-	-
Psyllidae	Ciriacreminae	Jataiba uncigera Burckhardt & Queiroz, 2020	Fabaceae	Copaifera langsdorffii Desf.	Brazil
Psyllidae	Ciriacreminae	Mitrapsylla copaiferae Burckhardt & Queiroz, 2020	Fabaceae	Copaifera spp.	Brazil
Psyllidae	Ciriacreminae	Mitrapsylla gloriae Burckhardt & Queiroz, 2020	Fabaceae	Copaifera spp.	Brazil
Psyllidae	Ciriacreminae	Mitrapsyllaspp.	*Fabaceae	-	-
Psyllidae	Diaphorininae	Diaphorina citri Kuwayama, 1908	Rutaceae	Citrus spp., other Rutaceae	Asia; adventive in Africa, America and Oceania
Psyllidae	Macrocorsinae	Apsyllopsis mexicana (Crawford, 1914)	Fabaceae	Hymenaea spp.	Brazil, Mexico, Panama
Psyllidae	Platycoryphinae	Platycorypha sp.	*Fabaceae	-	-
Psyllidae	-	unidentified genus sp.	-	-	-
Triozidae		Calinda plaumanniOlivares & Burckhardt, 1997	Asteraceae	Baccharis dracunculifolia DC.	Brazil
Triozidae		Calinda sp.	*Asteraceae	-	-
Triozidae		Leuronota sp.	-	-	-
Triozidae		Trioza tabebuiae Santana & Burckhardt, 2001	Bignoniaceae	Handroanthus spp.	Brazil
Triozidae		Trioza sp.	-	-	-

Table 4
Psyllid species and number of individuals collected on vegetable crops (Carrot - Daucus carota L.; Parsley - Petroselinum crispum (Mill.) Fuss; Chilli pepper - Capsicum chinense Jacq.; Tobacco - Nicotiana tabacum L.; African eggplant - Solanum aethiopicum Jacq.; Eggplant - Solanum melongena L.; Potato - Solanum tuberosum L.) and weeds by direct sampling methods. See Supplementary Material for details.

Psyllid species	Crops							Weeds
	Carrot	Parsley	Chilli pepper	Tobacco	African eggplant	Eggplant	Potato	Amaranthus sp.	Bidens pilosa	Melampodium perfoliatum	Parthenium hysterophorus	Solanum americanum
Baccharopelma dracunculifoliae						1
Blastopsylla occidentalis			1
Calinda plaumanni	1						1
Calinda sp.							1
Euceropsylla sp. russoi group	1						1
Heterospylla cubana			1		1
Heteropsylla tenuata			1
Isogonoceraia divergipennis	25		2	1			77
Jataiba uncigera										1
Leuronota sp.							1
Mitrapsylla copaiferae	2
Mitrapsylla spp.	66	1				1	2	1
Paracarsidara sp.	1
Platycorypha sp.	3						1
Russelliana capsici			98
Russelliana solanicola	1965		4				8		2		70	1
genus sp.	1

Table 5
Psyllid species and number of individuals collected with yellow tray water traps in vegetable crop fields (Carrot - Daucus carota L.; African eggplant - Solanum aethiopicum Jacq.; Eggplant - Solanum melongena L.; Potato - Solanum tuberosum L.). See Supplementary Material for details.

Psyllid species	Carrot	African eggplant	Eggplant	Potato
Apsyllopsis mexicana				3
Blastopsylla occidentalis			2	5
Caradocia longiantennata				2
Caradocia sp.				1
Ctenarytaina spatulata				2
Diaphorina citri				1
Diclidophlebia crassiflagellata				1
Diclidophlebia sp.	1
Euceropsylla sp. martorelli group		8	2	1
Euceropsylla sp. russoi group		5		1
Glycaspis brimblecombei			1	1
Heteropsylla caldwelli	3			60
Heterospylla cubana		14	3	3
Heteropsylla spinulosa				5
Heteropsylla sp.	2
Isogonoceraia divergipennis	1	157	32	2
Isogonoceraia sp.			1
Leurolophus oriformae				1
Mastigimas anjosi			4	3
Mastigimas sp.				1
Mitrapsylla copaiferae				1
Mitrapsylla gloriae				1
Mitrapsylla spp.	1	3	3	33
Paracarsidara sp.				56
Platycorypha sp.			1	30
Pseudophacopteron longicaudatum				2
Russelliana solanicola		1	1	4
Trioza tabebuiae		1		6
Trioza sp.				1

With direct methods, 2344 total adult specimens were found: 2269 on crop plants and 75 on weeds (Table 4). On carrot, of the 2065 total specimens, 1965 were R. solanicola, 68 were Mitrapsylla spp., 25 were I. divergipennis and the seven remaining specimens belonged to five other species. On chilli pepper, of the 107 total specimens, 98 were R. capsici, four were R. solanicola, two were I. divergipennis, and the remaining three specimens belonged to three other species. Of the 92 specimens collected from potato 77 were I. divergipennis, eight were R. solanicola and the remaining seven belonged to six other species. Among the weeds, only Parthenium hysterophorus L. yielded a high number of psyllids: 70 specimens of R. solanicola. No psyllids were collected on bell pepper (Capsicum annuum L.), cabbage (Brassica oleracea var. capitata L.), celery (Apium graveolens L.) and tomato (Solanum lycopersicum L.). A few single psyllids were found on tobacco (Nicotiana tabacum L.), parsley [Petroselinum crispum (Mill). Fuss], African or Ethiopian eggplant (Solanum aethiopicum Jacq.), and eggplant (Solanum melongena L.) among the crop plants, and Amaranthus spp. L., Bidens pilosa L., Melampodium perfoliatum (Cav.) Kunth and Solanum americanum Mill. among the weeds (Table 4).

The presence of immature psyllids is important to determine whether a particular plant constitutes a host (Burckhardt et al., 2014) or if the presence of the psyllid is just accidental. In our survey, all samples of Russelliana capsici, which always included some immatures (not shown in tables), were collected exclusively on chilli pepper, varieties 'biquinho', 'bode' and 'malagueta'. Similarly, the majority of specimens of R. solanicola were collected on carrot, on which we found also immatures (Supplementary Material). A single immature of R. solanicola was found on potato (Supplementary Material).

Yellow tray water traps were set up in fields of carrot, African eggplant, eggplant and potato (Table 5). The two psyllid species, which were represented by immatures in the direct collection methods, were not (Russelliana capsici) or only poorly (R. solanicola) represented in the traps. The most frequent species was Isogonoceraia divergipennis present in all traps but most numerous in fields of African eggplant. Two other psyllids, Heteropsylla caldwelli Burckhardt and Paracarsidara sp. had large numbers mostly in potato. The other species were represented in smaller numbers.

With both direct and indirect collecting methods, the largest numbers of individuals were found in late spring and early summer (September and October), particularly Russelliana solanicola on carrot in São José do Rio Pardo in 2015 (1872 individuals: 1861 adults and 11 immatures) and Isogonoceraia divergipennis on carrot and potato in Casa Branca in 2015 (99 adults, no immatures).

Discussion

At least 37 species were collected, of which only two develop on the studied vegetables: Russelliana capsici on chilli pepper and R. solanicola on carrot and potato. Chilli pepper, carrot and potato are, hence, confirmed host plants of the two species. Hosts of the other psyllids belong, as far as known, to the Fabaceae (over 15 species), Anacardiaceae, Asteraceae, Myrtaceae (each three species) and six other families with one or two species each (Table 1). Apart from the two Russelliana species, all psyllids were collected on non-host plants. An example to illustrate this is I. divergipennis, the second most abundant species in our study. The species is monophagous on Caesalpinia pluviosa (Burckhardt and Queiroz, 2012), a widely planted ornamental and shade tree (Lorenzi, 1992). It was found on carrot, chilli pepper, potato and tobacco, in addition to traps in all four crops. Since no immatures were found, its occurrence on potato (27% of the collections of this species) and other crops is accidental. Similar observations were made in European vegetable fields. In a study on Swiss carrot psyllids, 41 species (corresponding to over a quarter of the known Swiss psyllid fauna) were trapped, and only four of them develop on carrots (Burckhardt and Freuler, 2000). In Spain, representatives of seven psyllid genera (Arytainilla, Bactericera, Blastopsylla, Cacopsylla, Ctenarytaina, Spanioza and Trioza) have been found associated with carrot and potato (Antolínez et al., 2019), but only two Bactericera species actually develop on the crops: B. nigricornis (Foerster) on carrot and potato (Antolínez et al., 2019; Moreno et al., 2021); and B. trigonica Hodkinson on carrot and celery (Antolínez et al., 2017).

The species composition varied considerably from one locality to another, but no geographic patterns could be detected. The localities that were sampled with traps that were deployed for a longer period of time usually, but not always, had more diverse samples: Perdizes (11 weeks): 20 spp., Maria da Fé (6 weeks): 14 spp., Piracicaba (7 weeks): 12 spp. and Campinas (16 weeks): 4 spp. All of the 23 species that were identified to species have been reported previously from Brazil (Burckhardt and Queiroz, 2012, 2020). Sixteen of them represent native species that are widely distributed on hosts that often grow on the edges of fields. The other seven species are associated with crops; three species are native (the two Russelliana spp. and Mastigimas anjosi Burckhardt et al. on Cedrela and Toona), and four are adventive (Blastopsylla occidentalis Taylor, Ctenarytaina spatulata Taylor and Glycaspis brimblecombei Moore on eucalypts, as well as Diaphorina citri Kuwayama on Citrus and other rutaceous hosts).

We found the highest number of psyllids in late spring and early summer (September and October), which is consistent with other studies in Brazil. In citrus orchards in the State of São Paulo, the highest density of D. citri was observed in the same months (Yamamoto et al., 2001). A study on population fluctuations of the guava psyllid Triozoida limbata (Enderlein) showed that the species is present during the whole year, but with a peak in October (Dalberto et al., 2004). The large number of psyllids collected during spring indicates, in addition to population peaks, the increase in the movement of adult psyllids at this time of year, probably in search of suitable mates and hosts. In our study, this could explain the large numbers of adults of some species on the crops despite the fact that they do not develop on these plants (e.g. species of the genera Heteropsylla, Mitrapsylla, Paracarsidara or Platycorypha).

There were significant differences between direct and indirect sampling methods. The yellow trays yielded a larger species diversity, however, the most abundant species in the yellow trays were not the most common species observed directly on the plants. The most abundant species on carrot (R. solanicola) and potato (I. divergipennis) by direct collection methods were not the most collected in the yellow trays in these two crops. Since, yellow trays are not neutral traps and may attract insects different from the ones than land on a given crop (Hall et al., 2007), it is highly likely that several species collected in yellow trays in our work are migrant insects, which do not develop on the crop.

Russelliana capsici has been recorded from Argentina (Buenos Aires, Entre Ríos) and Brazil (MG, SC, SP) (Burckhardt et al., 2012). In the present study we collected the species in MG and SP and we examined additional material from Goiás, Mato Grosso do Sul, Rio de Janeiro and Rio Grande do Sul, thus expanding the known range of distribution. In RS we collected seven samples, including one with many immatures, on Solanum laxum (Solanaceae, tribe Solaneae), a new host record, which is within the subfamily Solanoideae only distantly related to Capsicum (tribe Capsiceae). Solanum laxum occurs naturally in southeastern Brazil from MG to RG, to the Río de la Plata in Argentina and Uruguay, and into Paraguay. The plant also is cultivated in temperate and subtropical regions around the world and is often naturalized (Knapp, 2013). On the other hand, chilli pepper is suspected to originate from tropical northern Amazonia (Pickersgill, 1971). Judging from the presumed native distribution of the two plants it seems more likely that S. laxum is the original host plant of R. capsici and chilli pepper constitutes a more recently acquired host. Shifts from native to introduced plants (but not necessarily the closest relatives) seem to turn the psyllids into invasive pests, as in Diaphorina citri (shift from Murraya koenigii (L.) Spreng. (=Bergera koenigii L.) to Citrus) or M. anjosi (shift from Cedrela to Toona) (Hollis, 1987; Burckhardt et al., 2011)

Russelliana solanicola is one of the few polyphagous psyllid species. It has been reported from plants in the Amaranthaceae, Asteraceae, Escalloniaceae and Solanaceae (Serbina et al., 2015; Serbina and Burckhardt, 2017). Here we report it for the first time from Apiaceae (carrot) which belongs to the same clade (asterid II) as Asteraceae and Escalloniaceae. Of all specimens of this species collected in our study, 96% were captured directly on carrot, at different locations in GO, MG and SP. Russelliana solanicola is widely distributed in subtropical and temperate South America and was reported as a pest of potato in Chile and Peru (Serbina et al., 2015). Interestingly, in our study R. solanicola was rare on this crop with only eight adults and one immature. The reason for this discrepancy is unknown, but it may be influenced by different environmental conditions or different host races. A similar case is known from another potato psyllid, Bactericera nigricornis. It is considered a severe pest of potato in Iran (Fathi, 2011) but was found only in very low numbers in Spain without any eggs or immatures (Antolínez et al., 2019). In our study, we collected a large number of R. solanicola on the weed Parthenium hysterophorus L. This weed is a confirmed host of R. solanicola (Serbina et al., 2015).

While the majority of the collected psyllid species does not seem to have any negative impact on the crops, the situation with the two Russelliana species is more serious, as both might be potential vectors of Lso or other plant pathogens. Russelliana capsici apparently shifted within Solanaceae from a native plant to a crop species and may do this again in future. Russelliana solanicola is known to colonize a broad range of crops and weeds. The wide host range shown by R. solanicola represents a serious threat to Solanaceae and Apiaceae crops if there is a Lso introduction in areas where the species is established. Accordingly, special attention should be given to countries such as Peru where R. solanicola and B. cockerelli may co-occur. The possibility exists that R. solanicola could acquire Lso, or that B. cockerelli could acquire the apparent pathogen transmitted by R. solanicola reported by Salazar (2006) and others. Psyllid testing is beyond the scope of this paper; however, we encourage routine monitoring of Lso and other relevant plant pathogens in this psyllid species to confirm its vectorial capacity and also as part of a surveillance strategy to avoid spill over of Lso and other vectored plant pathogens to other countries in the region.

Conclusions

This is the first comprehensive study of the psyllid fauna of vegetable fields in South America. Russeliana capsici was found to be associated with chilli pepper, and R. solanicola was found on carrot and potato. It is important to emphasize that this is the first report of R. solanicola from carrot. The two species develop on these crops, documented by the presence of immatures. The polyphagous R. solanicola also was found in large numbers on Parthenium hysterophorus, a weed that was known previously as a host (Serbina et al., 2015). During the survey, at least 37 additional psyllid species were found. Specimens of 23 of these species could be identified to species, with the remaining 14+ species being undescribed or belonging to genera that are taxonomically poorly known. Most of the species collected are native taxa often associated with Fabaceae, along with several adventive species associated with citrus and eucalypts. Even though some of the species were found in considerable numbers (I. divergipennis, Heteropsylla caldwelli or Paracarsidara sp.) none of these psyllids develop on any of the examined crop species.

Another very important conclusion from our study is that for monitoring psyllid populations in vegetable fields, direct methods, such as visual inspection or the use of a sweep net or beating tray, are much more efficient than yellow tray water traps. The traps collected only six specimens of R. solanicola compared to 98 adults of R capsici and 2050 adults of R. solanicola taken with direct methods.

To date, Lso has not been reported from South America outside of Ecuador (Castillo Carrillo et al., 2019; Caicedo et al., 2020), and it is unknown whether the two native R. capsici and R. solanicola would be capable of transmitting Lso. Salazar (2006) and others reported what they thought to be a virus transmitted by R. solanicola in potatoes in Peru. Moreover, Hansen et al (2022) and Kwak et al. (2021) reported a new Candidatus Liberibacter species associated with R. capsici that may be potentially pathogenic on Capsicum. The role played by weeds as reservoirs for the psyllids and associated plant pathogens is unknown. Future studies should address these aspects along with surveys to observe the spread of B. cockerelli and Lso, as well as plant pathogens associated with native Russelliana species, in South America.

Acknowledgments

The authors are grateful for the logistic support of the Associação Brasileira da Batata (ABBA), specially to Natalino Yassushi Shimoyama and of all the producers involved. We thank Susan Halbert (Florida Department of Agriculture and Consumer Services, Division of Plant Industry) and David Ouvrard (ANSES) for their careful review providing useful comments and suggestions to improve the manuscript. Collecting and export permits were provided by IBAMA/SISBIO (permit numbers: 11832-Licença permanente para coleta de material zoológico; 37053-Autorização para atividades com finalidade científica: áreas fora de parques em PR, SC e RS; 44493-Autorização para atividades com finalidade científica: Parque Nacional da Serra da Canastra, Parque Nacional da Serra da Bocaina, Parque Nacional do Itatiaia, Parque Nacional da Tijuca; and CNPq (Projeto ‘Biodiversidade de Psylloidea no Brasil’, processo de Expedição Científica nº 002152/2012).

• Funding

  This research was funded by the Associação Brasileira da Batata (ABBA), as well as by grants of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. 427539/2016-1 and 314181/2020-2).

References

• Alfaro-Fernández, A., Siverio, F., Cebrián, M.C., Villaescusa, F.J., Font, M.I., 2012. “Candidatus Liberibacter solanacearum” associated with Bactericera trigonica affected carrots in the Canary Islands. Plant Dis. 96, 581. https://doi.org/10.1094/PDIS-10-11-0878-PDN
  » https://doi.org/10.1094/PDIS-10-11-0878-PDN
• Antolínez, C.A., Fereres, A., Moreno, A., 2017. Risk assessment of ‘Candidatus Liberibacter solanacearum’ transmission by the psyllids Bactericera trigonica and B. tremblayi from Apiaceae crops to potato. Sci. Rep. 7, 45534. https://doi.org/10.1038/srep45534
  » https://doi.org/10.1038/srep45534
• Antolínez, C.A., Moreno, A., Ontiveros, I., Pla, S., Plaza, M., Sanjuan, S., Palomo, J.L., Sjölund, M.J., Sumner-Kalkun, J.C., Arnsdorf, Y.M., Jeffries, C.J., Ouvrard, D., Fereres, A., 2019. Seasonal abundance of psyllid species on carrots and potato crops in Spain. Insects 10, 287. https://doi.org/10.3390/insects10090287
  » https://doi.org/10.3390/insects10090287
• Burckhardt, D., 1994. Psylloid pests of temperate and subtropical crop and ornamental plants (Hemiptera, Psylloidea): a review. Entomol. (Trends in Agril. Sci.). 2, 173-186.
• Burckhardt, D., Lauterer, P., 1997. A taxonomic reassessment of the triozid genus Bactericera (Hemiptera: psylloidea). J. Nat. Hist. 31, 99-153. https://doi.org/10.1080/00222939700770081
  » https://doi.org/10.1080/00222939700770081
• Burckhardt, D., Freuler, J., 2000. Jumping plant-lice (Hemiptera, Psylloidea) from sticky traps in carrot fields in Valais, Switzerland. Mitt. Schweiz. Entomol. Ges. 73, 191-209.
• Burckhardt, D., Queiroz, D.L., Queiroz, E.C., Andrade, D.P., Zanol, K., Rezende, M.Q., Kotrba, M., 2011. The jumping plant-louse Mastigimas anjosi spec. nov., a new pest of Toona ciliata (Meliaceae) in Brazil. Spixiana 34, 109-120.
• Burckhardt, D., Queiroz, D.L., 2012. Checklist and comments on the jumping plant-lice (Hemiptera: Psylloidea) from Brazil. Zootaxa 3571, 26-48. https://doi.org/10.11646/zootaxa.3571.1.2
  » https://doi.org/10.11646/zootaxa.3571.1.2
• Burckhardt, D., Queiroz, D.L., Rezende, M.Q., Queiroz, E.C., Bouvet, J.P., 2012. The capsicum psyllid, Russelliana capsici (Hemiptera, Psylloidea), a pest on Capsicum annuum (Solanaceae) in Argentina and Brazil. Mitt. Der Schweiz. Entomologischen Ges. 85, 71-78.
• Burckhardt, D., Ouvrard, D., Queiroz, D.L., Percy, D., 2014. Psyllid host-plants (Hemiptera: Psylloidea): resolving a semantic problem. Fla. Entomol. 97, 242-246. https://doi.org/10.1653/024.097.0132
  » https://doi.org/10.1653/024.097.0132
• Burckhardt, D., Queiroz, D.L., 2020. Neotropical jumping plant-lice (Hemiptera, Psylloidea) associated with plants of the tribe Detarieae (Leguminosae, Detarioideae). Zootaxa 4733, 1-73. https://doi.org/10.11646/zootaxa.4733.1.1
  » https://doi.org/10.11646/zootaxa.4733.1.1
• Burckhardt, D., Queiroz, D.L., 2023. Psylloidea in catálogo taxonômico da fauna do Brasil. PNUD. Available in: http://fauna.jbrj.gov.br/fauna/faunadobrasil/97523 (accessed 02 January 2023).
  » http://fauna.jbrj.gov.br/fauna/faunadobrasil/97523
• Caicedo, J.D., Simbaña, L.L., Calderón, D.A., Lalangui, K.P., Rivera-Vargas, L.I., 2020. First report of ‘Candidatus Liberibacter solanacearum’ in Ecuador and in South America. Australas. Plant Dis. Notes 15, 6. https://doi.org/10.1007/s13314-020-0375-0
  » https://doi.org/10.1007/s13314-020-0375-0
• Castillo Carrillo, C., Fu, Z., Burckhardt, D., 2019. First record of the tomato potato psyllid Bactericera cockerelli from South America. Bull. Insectol. 72, 85-91.
• Chávez, R., Salazar, L., Upadhya, M., Chujoy, E., Cabello, R., Garcia, A., Linares, J., 2003. The occurrence of genetic resistance and susceptibility to the new potato virus SB-29 among tetraploide potato populations (Solanum tuberosum L., 2n = 4x = 48 AAAA) in an arid agroecosystem. Idesia 21, 9-22.
• Dalberto, F.M.S., Menezes Junior, A.O., Simões, H.C., Benito, N.P., Pitwak, J., 2004. Flutuação populacional do psilídeo-da-goiabeira, Triozoida limbata (Hemiptera: Psyllidae) na região de Londrina, PR. Semina: Ciênc. Agrár. 25, 87-92.
• Fathi, S.A.A., 2011. Population density and life-history parameters of the psyllid Bactericera nigricornis (Forster) on four commercial cultivars of potato. Crop Prot. 30, 844-848. https://doi.org/10.1016/j.cropro.2011.03.003
  » https://doi.org/10.1016/j.cropro.2011.03.003
• Hall, D.G., Hentz, M.G., Ciomperlik, M.A., 2007. A comparison of traps and stem tap sampling for monitoring adult Asian Citrus Psyllid (Hemiptera:Psyllidae) in citrus. Fla. Entomol. 90, 327-334. https://doi.org/10.1653/0015-4040(2007)90[327:ACOTAS]2.0.CO;2
  » https://doi.org/10.1653/0015-4040(2007)90[327:ACOTAS]2.0.CO;2
• Hansen, A.K., Sanchez, A.N., Kwak, Y., 2022. Divergent host-microbe interaction and pathogenesis proteins detected in recently identified Liberibacter species. Microbiol. Spectr. 10, 1-11. https://doi.org/10.1128/spectrum.02091-22
  » https://doi.org/10.1128/spectrum.02091-22
• Hodkinson, I.D., 2009. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J. Nat. Hist. 43, 65-179. https://doi.org/10.1080/00222930802354167
  » https://doi.org/10.1080/00222930802354167
• Hollis, D., 1987. A new citrus-feeding psyllid from the Comoro Islands, with a review of the Diaphorina amoena species group (Homoptera). Syst. Entomol. 12, 47-61. https://doi.org/10.1111/j.1365-3113.1987.tb00547.x
  » https://doi.org/10.1111/j.1365-3113.1987.tb00547.x
• Instituto Colombiano Agropecuario - ICA, 2021. Reporte de Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) en el Departamento de Nariño. Available in: https://www.ica.gov.co/areas/agricola/servicios/epidemiologia-agricola/saf/notificacion-oficial/detalle-notificacion-oficial/reporte-de-bactericera-cockerelli-sulc-hemipter (accessed 15 September 2022).
  » https://www.ica.gov.co/areas/agricola/servicios/epidemiologia-agricola/saf/notificacion-oficial/detalle-notificacion-oficial/reporte-de-bactericera-cockerelli-sulc-hemipter
• Knapp, S., 2013. A revision of the Dulcamaroid Clade of Solanum L. (Solanaceae). PhytoKeys 22, 1-428. https://doi.org/10.3897/phytokeys.22.4041
  » https://doi.org/10.3897/phytokeys.22.4041
• Kwak, Y., Sun, P., Meduri, V.R., Percy, D.M., Mauck, K.E., Hansen, A.K., 2021. Uncovering symbionts across the psyllid tree of life and the discovery of a new Liberibacter species, “Candidatus” Liberibacter capsica. Front. Microbiol. 12, 1-17. https://doi.org/10.3389/fmicb.2021.739763
  » https://doi.org/10.3389/fmicb.2021.739763
• Liefting, L.W., Weir, B.S., Pennycook, S.R., Clover, G.R.G., 2009. ´Candidatus Liberibacter solanacearum’, associated with plants in the family Solanaceae. Int. J. Syst. Evol. Microbiol. 59, 2274-2276. https://doi.org/10.1099/ijs.0.007377-0
  » https://doi.org/10.1099/ijs.0.007377-0
• Lorenzi, H., 1992. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil., 2nd ed. Nova Odessa Plantarum, São Paulo.
• Mawassi, M., Dror, O., Bar-Joseph, M., Piasezky, A., Sjölund, J.M., Levitzky, N., Shoshana, N., Meslenin, L., Haviv, S., Porat, C., Katsir, L., Kontsedalov, S., Ghanim, M., Zelinger-Reichert, E., Arnsdorf, Y.M., Gera, A., Bahar, O., 2018. ´Candidatus Liberibacter solanacearum’ is tightly associated with carrot yellows symptoms in Israel and transmitted by the prevalent psyllid vector Bactericera trigonica. Phytopathology 108, 1056-1066. https://doi.org/10.1094/PHYTO-10-17-0348-R
  » https://doi.org/10.1094/PHYTO-10-17-0348-R
• Moreno, A., Miranda, M. P., Fereres, A., 2021. Psyllids as major vectors of plant pathogens. Entomol. Gen. 41, 419-438. https://doi.org/10.1127/entomologia/2021/1289
  » https://doi.org/10.1127/entomologia/2021/1289
• Munyaneza, J.E., Fisher, T.W., Sengoda, V.G., Garczynski, S.F., Nissinen, A., Lemmetty, A., 2010. Association of “Candidatus Liberibacter solanacearum” with the psyllid, Trioza apicalis (Hemiptera: Triozidae) in Europe. J. Econ. Entomol. 103, 1060-1070. https://doi.org/10.1603/ec10027
  » https://doi.org/10.1603/ec10027
• Munyaneza, J.E., 2012. Zebra chip disease of potato: biology, epidemiology, and management. Am. J. Potato Res. 89, 329-350. https://doi.org/10.1007/s12230-012-9262-3
  » https://doi.org/10.1007/s12230-012-9262-3
• Ouvrard, D., Chalise, P., Percy, D.M., 2015. Host-plant leaps versus host-plant shuffle: a global survey reveals contrasting patterns in an oligophagous insect group (Hemiptera, Psylloidea). Syst. Biodivers. 13, 434-454. https://doi.org/10.1080/14772000.2015.1046969
  » https://doi.org/10.1080/14772000.2015.1046969
• Ouvrard, D., 2022. Psyl'list - The world Psylloidea database. Available in: http://www.hemiptera-databases.org/psyllist/ (accessed 2 January 2022).
  » http://www.hemiptera-databases.org/psyllist/
• Pickersgill, B., 1971. Relationships between weedy and cultivated forms in some species of chili peppers (Genus Capsicum). Evolution 25, 683-691. https://doi.org/10.2307/2406949
  » https://doi.org/10.2307/2406949
• Queiroz, D.L., Burckhardt, D., Majer, J., 2012. Integrated pest management of eucalypt psyllids (Insecta, Hemiptera, Psylloidea). In: M.L. Larramendy, S. Soloneski (Eds.), Integrated Pest Management and Pest Control - Current and Future Tactics. IntechOpen, London, pp. 385-412. https://doi.org/10.5772/32631
  » https://doi.org/10.5772/32631
• Salazar, L. F., 2006. Emerging and re-emerging potato diseases in the Andes. Potato Res. 49, 43-47. https://doi.org/10.1007/s11540-006-9005-2
  » https://doi.org/10.1007/s11540-006-9005-2
• Serbina, L., Burckhardt, D., Birkhofer, K., Syfert, M.M., Halbert, S.E., 2015. The potato pest Russelliana solanicola Tuthill (Hemiptera: Psylloidea): taxonomy and host-plant patterns. Zootaxa 4021, 33-62. https://doi.org/10.11646/zootaxa.4021.1.2
  » https://doi.org/10.11646/zootaxa.4021.1.2
• Serbina, L., Burckhardt, D., 2017. Systematics, biogeography and host-plant relationships of the Neotropical jumping plant-louse genus Russelliana (Hemiptera: psylloidea). Zootaxa 4266, 1-114. https://doi.org/10.11646/zootaxa.4266.1.1
  » https://doi.org/10.11646/zootaxa.4266.1.1
• Servicio Nacional de Sanidad Agraria - SENASA, 2021. 'Zebra chip', Plaga de la Papa, no está Presente en el Perú. Available in: https://www.senasa.gob.pe/senasacontigo/senasa-zebra-chip-plaga-de-la-papa-no-esta-presente-en-el-peru/ (accessed 15 September 2022).
  » https://www.senasa.gob.pe/senasacontigo/senasa-zebra-chip-plaga-de-la-papa-no-esta-presente-en-el-peru/
• Tahzima, R., Maes, M., Achbani, E. H., Swisher, K.D., Munyaneza, J.E., De Jonghe, K., 2014. First report of ‘Candidatus Liberibacter solanacearum’ on carrot in Africa. Plant Dis. 98, 1426. https://doi.org/10.1094/PDIS-05-14-0509-PDN
  » https://doi.org/10.1094/PDIS-05-14-0509-PDN
• Teresani, G.R., Bertolini, E., Alfaro-Fernández, A., Martínez, C., Tanaka, F.A.O., Kitajima, E.W., Roselló, M., Sanjuán, S., Ferrándiz, J.C., López, M.M., Cambra, M., Font, M.I., 2014. Association of ‘Candidatus Liberibacter solanacearum’ with a vegetative disorder of celery in Spain and development of a Real-Time PCR method for its detection. Phytopathology 104, 804-811. https://doi.org/10.1094/PHYTO-07-13-0182-R
  » https://doi.org/10.1094/PHYTO-07-13-0182-R
• Tuthill, L.D., 1959. Los Psyllidae del Peru Central (Insecta, Homoptera). Rev. Peru. Entomol. Agric. 2, 1-27.
• World Flora Online - WFO. (2022). Available in: http://www.worldfloraonline.org (accessed 23 January 2022).
  » http://www.worldfloraonline.org
• Yamamoto, P.T., Paiva, P.E.B., Gravena, S., 2001. Flutuação populacional de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em pomares de citros na região Norte do Estado de São Paulo. Neotrop. Entomol. 30, 165-170. https://doi.org/10.1590/S1519-566X2001000100025
  » https://doi.org/10.1590/S1519-566X2001000100025

Supplementary Material

The following online material is available for this article:

Psyllids collected in vegetable fields in the Center-South region of Brazil with information on state, locality, geographical coordinates, altitude, sampling date, crop species and sampled plant (if different both are given), methods, psyllid species with sampled number of specimens (N).

Edited by

Associate Editor:

Adeney Bueno

Publication Dates

• Publication in this collection
  16 Jan 2023
• Date of issue
  2023

History

• Received
  01 June 2022
• Accepted
  21 Dec 2022