The red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae), is considered one of the most threatening pests of coconut, banana, and other monocotyledonous plants on the American continent and in the Caribbean region (Etienne & Flechtmann 2006; Carrillo et al. 2011a; Navia et al. 2015). Infested leaves usually become yellowish, with the attacked area drying as the population grows (Flechtmann & Etienne 2004; Peña et al. 2006). Plants are more seriously affected when infestations are associated with water stress and malnutrition (Navia et al. 2015).

Raoiella indica was first reported from the Western Hemisphere in the mid 2000s (Flechtmann & Etienne 2004), spreading since then to extensive areas in the tropical and subtropical regions of the American continent and the Caribbean (Welbourn 2006; Rodrigues et al. 2007; Vásquez et al. 2008; Carrillo et al. 2011b; Kane et al. 2012). Since its first report in Brazil in 2009, in the state of Roraima (Navia et al. 2011), new records were published from the states of Amazonas (Rodrigues & Antony 2011), São Paulo (Oliveira et al. 2016), Paraná (Hata et al. 2017), Alagoas, Bahia, Ceará, Distrito Federal, Goiás, Maranhão, Minas Gerais, Paraíba, Pernambuco, Piauí, Rio Grande do Norte and Sergipe (Melo et al. 2018). The risk of establishment of this mite in different parts of Brazil has been evaluated by Amaro & Morais (2013), although knowledge about the distribution of this mite in the southern half of the extensive Brazilian territory is still limited (Oliveira et al. 2016; Hata et al. 2017).

Coconut, Cocos nucifera L. (Arecaceae), is the principal host of R. indica (Carrillo et al. 2011a; Navia et al. 2015; Otero-Colina et al. 2016; Gómez-Moya et al. 2017; Polanco-Arjona et al. 2017). Although mid-southern Brazil is not very important in the production of coconut, this plant is commonly found in southern Brazil and other parts of the country as backyard plantations, or as ornamentals in this and other Brazilian regions (IBGE 2017). Conversely, banana (Musa spp.; Musaceae), also a host of R. indica (Carrillo et al. 2011a), is an important crop in mid-southern Brazil, especially in the states of Espírito Santo, Minas Gerais, Rio de Janeiro, and Sao Paulo. In fact, severe damage to banana varieties ‘Prata' (AAB group) and ‘Cavendish’ (AAA group) was observed in 2016 in Missão Velha, Ceará State, northeastern Brazil (Rita de Cassia Rodrigues, personal communication). High levels of R. indica also were reported on banana cultivation in the Caribbean (Cocco & Hoy 2009; Kane et al. 2012; Rodrigues & Irish 2012).

Table 1.

Sampling sites where Raoiella indica was present or absent¹ on each plant species in surveys conducted in mid-southern Brazil between Nov 2015 and Oct 2018.

The objective of this study was to evaluate the distribution of R. indica and associated predatory mites in mid-southern Brazil on coconut, banana, and a few other plant species on which this mite has been found, discussing the possible southern limit to its distribution in the country.

Materials and Methods

The study was conducted between 2015 and 2018, soon after the first detection of the mite in Brazil south of the Amazonas River (Oliveira et al. 2016). Symptomatic coconut plants (especially), as well as ornamental date and banana plants found along highways, urban parks, and nurseries were examined in the Federal District, and in the states of Espírito Santo (ES), Goiás (GO), Mato Grosso (MT), Mato Grosso do Sul (MS), Minas Gerais (MG), Paraná (PR), Rio de Janeiro (RJ), Rio Grande do Sul (RS), Santa Catarina (SC), and São Paulo (SP). When mites resembling R. indica were detected with the use of hand lenses, leaflets or leaf pieces were transferred to vials partially filled with 70% ethanol and transported to the laboratory, where the mites were collected and mounted in Hoyer's medium. They were subsequently identified to species by comparing their morphology with the information provided in the original descriptions and redescriptions in the literature. Representative specimens of the species collected were deposited in the mite reference collection of Departamento de Entomologia e Acarologia, Escola Superior de Agricultura “Luiz de Queiróz,” Universidade de São Paulo (ESALQ/USP), Piracicaba, São Paulo, Brazil.

Fig. 1.

New findings of Raoiella indica in mid-southern Brazil between 2015 and 2018, and previous records throughout the country. (A) Brazilian map showing sites where the presence of the mite has been evaluated in this and previous surveys; (B) Enlarged view of the position of sites in Paraná (PR), Rio Grande do Sul (RS), and Santa Catarina (SC) states.

Results

Raoiella indica was found in the Federal District and 49 municipalities of the 9 states visited in the study (Table 1), of which the southernmost was Iporã, Paraná State (24.007222°S, 53.698333°W). It was not found in 26 other municipalities south of Iporã (Table 1, Fig. 1), namely: Paraná State: Campo Largo, Candoi, Cascavel, Corbélia, Coronel Vivida, Cruzeiro do Oeste, Curitiba, Guaraniaçú, Guarapuava, Imbaú, Irati, Ivaiporã, Laranjeiras do Sul, Mandaguari, Morretes, Palmeira, Palotina, Paranagá, Ponta Grossa, Pontal do Paraná, Terra Roxa, and Toledo; Rio Grande do Sul State: Boa Vista das Missões, Carazinho, and Frederico Westphalen; Santa Catarina State: Campo Erê.

All 18 species of predatory mites found in association with R. indica are found in the order Mesostigmata (Table 2). Fourteen of them were in family Phytoseiidae, 1 in Blattisociidae, and 3 in Melicharidae. By far, the phytoseiid Euseius citrifolius Denmark & Muma was the most numerous and widespread (45 specimens found in 5 states), followed by Iphiseiodes zuluagai Denmark & Muma, and Amblyseius largoensis (Muma), also phytoseiids and both found in similar numbers (17 and 14 specimens in 3 and 1 states, respectively).

Discussion

The results of this study expand the known distribution of R. indica in Brazil to include areas where its most important host plant, coconut, is not an important crop. Although the absence of R. indica in some sampling sites could have been due to the unsuitability of some of the plants examined, this does not seem to have been the case, because in most places the plants examined were known hosts of R. indica, except for Syagrus romanzoffiana (Cham.) Glassman (Aracaceae) (in Coronel Vivida, Curitiba, and Ivaiporã), where coconut was not found.

Although failure to find R. indica in some sampling areas could be by chance, its absence in areas of southern Brazil (Rio Grande do Sul, Santa Catarina, and part of Paraná States) could reflect the ecological unsuitability of those places. These results fit well with what was predicted by the model developed by Amaro & Morais (2013), based on 20 environmental variables. The authors concluded that the variables that most influenced their prediction were related to temperature. The altitude of the sites where R. indica was not found across the central region of Paraná State is at least about 500 masl, except Morretes, Palotina, Pontal do Paraná, and Terra Roxa (333, 374, 11, and 285 masl, respectively). Conversely, the altitude of the sites where it was found in the northern part of the state is at most 500 masl, except Londrina (543 masl). Hence, being higher and further south make central Paraná State colder than northern Paraná. An examination of the historical records (Continente 2018) showed that average minimum monthly temperatures in places where R. indica was found in northern Paraná are at least 9 °C, except Maringá (7.2 °C), whereas in places where it was not found, temperatures are at most 9 °C, except Morretes, Palotina, Pontal do Paraná, and Terra Roxa (12.3, 9.6, 13.7, and 9.8 °C, respectively). However, according to that the study of Amaro & Morais (2013), it is still possible that the mite could be found further south, along the coast of Rio Grande to Sul and Santa Catarina, areas not surveyed in this work. Also, according to that study, R. indica is expected to be able to extend south of the maximum latitude where it was detected during the current study (Iporã), in neighboring Paraguay and Argentina, along the low lands of the Paraguay River basin.

Table 2.

Mesostigmatid mites associated with Raoiella indica on host plants in mid-southern Brazil in surveys conducted between 2015 and 2018.

The highest frequency of R. indica on coconut in this study is certainly due to the concentrated effort to search for it on symptomatic coconut, given its known preference for this host plant. The spread of R. indica is facilitated by the fact that new coconut plantations are usually established with plantlets acquired commercially, which may harbor the mite at low population levels, allowing its unnoticeable transportation over long distances. Dispersal can be facilitated further by the transportation of other infested plants that are used principally as ornamentals. The permanent availability of the host plant, and the seemingly limited capacity of natural enemies to maintain the pest at low levels, may account also for its ability to disperse (Navia et al. 2013). Hence, occurrence of R. indica south of Iporã in Brazil seems possible, in protected or restricted microhabitats, especially on protected ornamentals or in banana-producing areas, usually microhabitats with mild climate.

Although the diversity of predatory mites associated with R. indica in this study could not be considered low, not much can be said about the type of relationship they have to that prey, because basically most of those species found in this work have been reported from coconut in Brazil and elsewhere, regardless of the presence of R. indica (Lawson-Balagbo et al. 2008; Oliveira et al. 2012). Amblyseius largoensis, the third most numerous phytoseiid predator in association with R. indica in the present study, often has been reported in association with R. indica in the Neotropics, usually in coastal areas (Etienne & Flechtmann 2006; Rodrigues et al. 2007; Roda et al. 2008; Carrillo et al. 2010; Hastie et al. 2010; Carrillo et al. 2011c; Gondim Jr. et al. 2012; Moraes et al. 2012; Flores-Gallano et al. 2017). This predator has received the most attention as a possible candidate for practical use as biological control agent of the pest (Carrillo et al. 2010; Carrillo et al. 2011c; Carrillo et al. 2012; Domingos et al. 2012; Carrillo et al. 2014; Morais et al. 2016; Mendes et al. 2018).

In conclusion, since its first report in Brazil, R. indica now has been found in 18 states in the country, in sites ranging from 2°N to 23°S latitude. Complementary studies, especially in western Brazil, might demonstrate that it is also present there.