INTRODUCTION

Spontaneous vegetation is present within and outside crop fields and provides food, shelter, breeding, and overwintering sites for phytophagous insect species. Particularly for phytophagous thrips (Thysanoptera), the concept of host plant is very important since they can be associated with plant species that provide shelter and food for adults (incidental hosts) and those that are used for oviposition and larval rearing (true-breeding or reproductive hosts). The frequency of association between the insect and the true host is usually high (Mound & Marullo, 1996). Knowledge of the density of thrips in true host flowers in uncultivated margins could predict thrip density within vineyards and thus help to control their population growth (Canovas et al., 2023).

Among the insects cited in grapevine crops in Argentina are thrips (Viglianco, 2020; Viglianco et al, 2021; Dagatti et al., 2024). The presence of spontaneous vegetation or other species planted during the flowering period of the crop can be an important source of migration into vineyards (Hidalgo Fernández & Hidalgo Togares, 2011).

Viglianco et al. (2021) found that the most common thrips species in the vineyards of Colonia Caroya (Department Colón, province of Córdoba) is Frankliniella gemina Bagnall. The adults and larvae of this species cause scars or russet on the upper portion or the entire surface of grape berries affecting quality parameters such as average weight and seed weight (Viglianco, 2020). This is a Neotropical endemic species broadly distributed from Mexico to Argentina (Cavalleri & Mound, 2012), considered as a polyphagous pest due to the wide variety of host plants attacked (Zamar, 2011). Frankliniela gemina reproduces in spontaneous plant species in spring and subsequently colonises grapevines at the time of flowering (Botton et al., 2007).

In Argentina, Córdoba is the eighth largest wine-producing province, with over 50 % of vineyards near Colonia Caroya (Colón Department) (INV (Instituto Nacional de Vitivinicultura), 2023).

Plant species growing spontaneously in Argentine vineyards have been studied (Méndez, 2014; Rovai et al., 2017) but which of them are potential hosts of F. gemina is not yet known, despite its importance for planning thrips management strategies. The objectives of this study were to compile bibliographic information on the host plants of F. gemina in Argentina and to identify the species that serve as true and accidental hosts of F. gemina in the area around vineyards in Colonia Caroya, Córdoba, Argentina.

MATERIALS AND METHODS

Literature Review

In order to know the recorded plant hosts of F. gemina in Argentina, we searched for scientific articles published in the period 1980-2024, using the main bibliographic databases available on the Internet: Scopus, SciELO, ScienceResearch, ResearchGate, and Google Scholar. The keywords "Frankliniella gemina", their two synonymized species F. rodeos and F. allochroos (Cavalleri & Mound, 2012), in combination with "alternative hosts" and "weeds" were used as descriptors in both Spanish and English. The information was entered into a digital table in order to consider the following aspects: taxonomic family, the growth form of the host plant (herb, shrub, or tree), and its status in the study region as a cultivated or non-cultivated species.

Collection of plant hosts for F. gemina in vineyards of Colonia Caroya (Córdoba, Argentina)

In the initial phase (from August to December 2012), we conducted biweekly sampling of companion plant species in three commercial vineyards in Colonia Caroya, situated 50 km north of the city of Córdoba at 31°02'00" S and 64°05'00" W, at an altitude of 509 m a.s.l. The varieties were Malbec, Merlot, Chardonnay, Pinot Noir and Isabella. All fields were conventionally managed, i.e. using synthetic fungicides and herbicides.

In each vineyard, we selected three sampling plots, each measuring 1 m², between the rows of vines and three plots at least five meters away from the outermost row of vines. During each site visit and sampling date, the plant species present in the sampling area were collected and identified. In a second step, considering that F. gemina is an anthophilous species (Monteiro, 2002), simple flowers or inflorescences, depending on the plant species (from now on referred to as floral units “FU”), were collected in the three vineyards and their surroundings from the end of winter to the beginning of summer in 2013 and 2015. Plant species with an average frequency of occurrence equal to or greater than 20 % (data obtained in 2012) were sampled for floral resource analysis. Furthermore, the FU of Prunus persicae (L.) Stokes (peach) (Rosaceae), Medicago sativa L. (alfalfa) (Fabaceae) and Melia azedarach L. (chinaberry) (Meliaceae) were collected, as these are commonly occurring plant species in the area, typically found a few meters from the vineyards. Each sample consisted of 10-20 FU of each species, randomly selected from 1-4 plants. The total number of FUs collected depended on the availability of the plant species.

Sample processing and plant host determination

Samples were transported to the laboratory in polyethene bags for the specific identification of plants using keys (Marzocca, 1993; Carreras et al., 2005). Insects were removed from the FU and placed in AGA solution (60 % ethyl alcohol, glycerin and acetic acid in a ratio of 10:1:1) for preservation. On each date and sample, we recorded the presence of individuals (adult or larvae) of F. gemina on each plant species. We identified F. gemina specimens (larvae and adults) from temporary microscopic preparations using taxonomic keys (De Borbón, 2007, 2013; Mound, 2010; Cavalleri & Mound, 2012). In host plants where gravid females of F. gemina were found, the number of eggs in the ovarioles was counted. Adult specimens were deposited at the Entomological Collection of Córdoba (ENTOCOR).

RESULTS

We reported 122 host plant species for F. gemina by 17 publications from nine out of 23 provinces in Argentina (Table I). Plant species belong to 41 families, with Asteraceae and Fabaceae being the most frequently reported hosts. In the study region, we observed F. gemina on 26 plant species, primarily belonging to the same two plant families, representing 71 % of the evaluated plant species.

Sixty-five per cent of the plant species associated with F. gemina in Argentina were herbs, with a nearly equal proportion of cultivated and non-cultivated species. The number of shrubs reported as hosts was twice that of trees. In the study region, the prevalence of non-cultivated herbaceous plants was even more pronounced, accounting for 85 % of the total.

In Argentina, only 22 % of all species associated with F. gemina are true hosts, as both larval and adult stages were found on them (Table I). Flower samples of 32 plant species with an average frequency of occurrence equal to or greater than 20 % (data 2012) showed that a total of 6 plant species harbored both stages within the regional dataset: Conium maculatum L. (Apiaceae), Medicago sativa (Fabaceae), Melilotus albus Medik. (Fabaceae), Raphanus sativus L. (Brassicaceae), Nothoscordum gracile (Aiton) Stearn (Amaryllidaceae), and Melia azedarach L. (Meliaceae) (Table II)

Regarding the temporal distribution of F. gemina, adult and larval specimens were identified throughout the sampling period (August-December of both years) in a range of species of the surrounding vegetation. Some host plants were consistently associated with F. gemina, whenever they were present. These included M. alba (N= 10), N. gracile (N= 10), R. sativus (N= 10), C. maculatum (N= 6), M. azedarach (N= 6) and M. sativa (N= 6) (Table II). In October, a period before or coinciding with the beginning of grape flowering, 17 flowering plant species surrounding the vineyard were evaluated. We observed a maximum number of six true hosts in the vineyards. The highest number of flowering plant hosts of F. gemina was recorded in November (68 % of the total), coinciding with the grape flowering. In all samples (N= 6) of M. azedarach flowers, seven gravid females containing two to seven eggs were observed, while in the other hosts, females carried one to three eggs.

Some plant species, including C. maculatum, N. gracile, R. sativus and M. sativa, may be considered potential reservoirs of F. gemina, as they offered flowers over a greater temporal window and host both stages of the insect from the beginning of their flowering stage (Table III).

DISCUSSION

Literature records from Argentina indicate that F. gemina is associated with 122 species in 41 plant families (Table I). Our study adds 11 new records of both, true and incidental hosts, representing 9 % of the total host species recorded in the country. Our data support the conclusion that this species is extremely polyphagous, as Frankiniella occidentalis (Pergande), another relevant pest species in the genus (Pizzol et al., 2017). Asteraceae and Fabaceae were the dominant host families in both datasets studied here. Both families have been previously identified as the most commonly used hosts by several Thysanoptera species (Zamar, 2011; Carrizo & Amela García, 2017; Pizzol et al., 2017).

In considering the family Asteraceae, which includes the largest number of host species, it is evident that their capitulum inflorescences offer the benefits of a sequential and continuous availability of pollen and nectar, given the centripetal development of their floral units (Varatharajan et al., 2016). The higher representation of Brassicaceae observed in Colonia Caroya (sharing with Fabaceae the second place, with 14 % of the total) is rather similar to that observed in the horticultural belt of La Plata, where the families with the highest richness were Asteraceae (48 %), Fabaceae (19 %), and Brassicaceae (14 %) (Carrizo & Amela García, 2017). It could be attributed to the type of habitat in which we obtained the records. The study in La Plata and ours, from Colonia Caroya, were carried out in productive environments, while data in the rest of the publications were obtained in other habitats, such as urban and natural. Furthermore, F. gemina appears to attack a proportional number of species from each taxonomic family, as the most attacked families are also the most species-rich in the regional flora (Zuloaga et al., 2019).

In the study region, as well as in the horticultural fields of La Plata (Buenos Aires), F. gemina was associated with a lower number of host plants (26 and 21, respectively) (Carrizo & Amela García, 2017), compared to Jujuy, where more than 80 host plants were listed (Zamar, 2011). Two reasons may explain these differences: a higher sampling intensity in Jujuy (Zamar & Arce de Hamity, 1999; Muruaga de L’Argentier et al., 2005; Zamar, 2011; Tapia et al., 2014; Rodriguez, 2016), and climatic differences that probably favour F. gemina in the lower latitudes of northern Argentina. We identified only six plant species in which F. gemina larvae can feed (Melilotus alba, Medicago sativa, Conium maculatum, Raphanus sativus, Melia azedarach and Nothoscordum gracile). The first four species have been previously reported as primary hosts (De Borbón et al, 1999; Zamar & Arce de Hamity, 1999; Carrizo, 2002; De Borbón, 2005, 2007, 2013; Rodríguez, 2016; Carrizo & Amela García, 2017), while M. azedarach and N. gracile are new records. It is known that despite the adults of a certain species of Thysanoptera can be found on a large number of plants, their larvae will exploit relatively few plants (Kirk, 1985; Carrizo, 2002). This is consistent with the findings for F. gemina both regionally and in the study area, where only 23 % of the total plants associated with this thrips species can be considered as primary hosts. The important role of these primary host plants is confirmed by the fact that we found F. gemina in 100 % of the samples collected from these plants. This constancy of association is required to determine a plant species as a true host in Thysanoptera (Mound & Marullo, 1996). We found adult thrips on 17 other plant species, but these can be considered secondary or incidental hosts. Specimens of F. gemina were observed in only one flower sample of three of these species [Leonorus sibiricus L. (Lamiaceae), Passiflora caerulea L. (Passifloraceae) and Bromus catharticus Vahl (Poaceae)], suggesting they are likely to be fortuitous hosts.

We found a significant regression between the mean frequency of plant species occurrence and the frequency of plant F. gemina association. It suggests that this species behaves as an opportunistic generalist, with no clear host preferences. In general, the presence of polyphagous thrips species is closely related to the availability of plants used as food sources (Pizzol et al., 2017). The ability of F. gemina to feed on different species present in the area would explain its presence throughout the five months analysed (August-December). It agrees with the observed in other horticultural crops, where thrips occur throughout the year in spontaneous vegetation (Carrizo & Amela García, 2017).

Between August and October, thrips visited 20-69 % of the flowering plant species near the vineyards. In October, a period preceding or coinciding with the flowering of the vines, the presence of F. gemina on nine plant species (six of which were true hosts) indicated that the surrounding vegetation represented a reservoir of populations that would later infest the crop. It was consistent with observations of Thrips tabaci (Linderman), Thrips obscuratus (Crawford) and F. gemina in vineyards in Italy, New Zealand and Brazil (Rigamonti, 2000; Schmidt et al., 2006; Botton et al., 2007).

Almost 90 % of flowering plants were visited by F. gemina in November and just over 70 % in December. It suggests that individuals may move to these spring-summer flowering plant species when the number of vine flowers decreases. This is consistent with Carrizo & Amela García (2017), who mentioned a strong increase in F. gemina on flowering plants in November and December.

Two primary hosts of F. gemina are recorded here for the first time and deserve special attention. The first is Nothoscordum gracile, an American herbaceous species with a wide distribution, naturalized in temperate regions of other continents (Hurrell, 2009) and frequently found in central Argentina (Flora Argentina, 2018). The only record of this plant species as a primary host of thrips was for Frankliniella platensis De Santis in Mendoza (De Borbón, 2018). Secondly, a new association with Melia azedarach, a tree species native to Asia (Hanan Alipi & Mondragón Pichardo, 2009), was recorded. Most importantly, it was demonstrated that this plant species is a true host for F. gemina. This finding is significant due to the wide distribution of M. azederach in Argentina, especially in agricultural fields where it is invasive (Ghersa et al., 2002). In its flowers, F. gemina females had a higher number of eggs than in other plant species, suggesting that this primary host provides good quality for thrips development. In this regard it is important to note that the nutritional value of a host plant for a Thysanoptera species is demonstrated by insect fecundity (Terry, 1997). Anthophilous species obtain the proteins necessary for reproduction mainly from pollen and improve some physiological functions (Lu et al., 2013). The medium size of M. azedarach pollen grains and their high nutritional quality (Marí Herguido, 2017) would allow F. gemina to fully exploit them, indicating that this plant species is an important reproductive host. Up to the present, associations between M. azedarach and thrips have not been reported in Argentina. However, in other countries, Thrips hawaiiensis Morgan (Singh & Varatharajan, 2014), Thrips coloratus Schmutz, Scirtothrips dorsalis Hodd (Zheng et al., 2005) and Lefroyothrips pictus (Hood) (Mound & Ng, 2021) were reported on its flowers. It is important to emphasise the significance of considering woody plant species as potential hosts for thrips. These species are frequently disregarded in plant-thrips interaction studies and are not commonly targeted for sampling, despite their ecological relevance.

The richness of spontaneously flowering vegetation directly correlates with the number of insects attacking the crop (Schmidt et al., 2006; Botton et al., 2007; Silva et al, 2018). Frankliniella gemina can transmit topoviruses to plants (De Borbon et al., 2006), although its role as vector of viral diseases to vineyards has not been demonstrated. However, the information about their true hosts is particularly relevant since transmission of thrip-transmitted viruses is usually only possible when the virus is acquired during the larval stages (Rotenberg et al., 2015). Therefore, understanding the identity of true hosts for F. gemina in Colonia Caroya is relevant for designing strategies within an Integrated Pest Management programme. Moreover, in order to reduce the population density of F. gemina in vineyards and therefore its damages, it is particularly recommended to avoid the presence of those true hosts that offer flowers in the months prior to the flowering of the vines, time of greatest vulnerability of the vines to be damaged by the thrips. Our results indicate that in vineyards of Colonia Caroya these species are N. gracile, C. maculatum and R. sativus. In relation to the woody M. azederach, although its floration coincides with that of the vineyards, the high fecundity that the insect reaches in its flowers should be reason enough to consider its occurrence in vineyards.

Acknowledgments

We acknowledge vine growers who permitted this study. This work was supported by Secretaría de Ciencia y Técnica (SECYT), Universidad Nacional de Córdoba, Argentina.

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Notas de autor

aviglian@agro.unc.edu.ar

Información adicional

redalyc-journal-id: 3220