Occurrence of Raoiella indica Hirst (Acari, Tenuipalpidae) in the Southeast region of the state of Pará, Brazil.

The red palm mite Raoiella indica Hirst attacks coconut, banana and açai trees. In 2007, the mite was recorded for the first time in South America. In the State of Pará, R. indica was recorded in the municipalities of the northwest, a region that is closer to the State of Amazonas, called 'Low Amazons'. Between October and November 2019, it was observed, by chance, that coconut and banana plants infested by R. indica, in residential backyards in municipalities from Marabá and Parauapebas, Southest of Pará, Brazilian Amazon. Three species from the Araceae family, two from Arecaceae, one Heliconiaceae and one Zingiberaceae, in addition to the banana Musaceae and açaí plantations, were examined. All stages of development of R. indica were found on coconut, banana trees and imperial palms, and few individuals were found on areca palm and red ginger leaves. This is the first record of the occurrence of the pest mite in the Southeast Pará sub-region.

Introduction

The red palm mite Raoiella indica Hirst, 1924 (Acari, Prostigmata, Tenuipalpidae), described in 1924 from specimens was collected from coconut trees (Cocus nucifera L., Arecaceae) na Índia (Hirst 1924). The mite attacks coconut and banana (Musa sp., Musaceae) leaves (Rodrigues et al. 2007; Morais et al. 2011; Gondin jr. et al. 2012; Kane et al. 2012). The mite was recently observed to cause severe injuries to açai palms (Euterpe oleracea Mart., Arecaceae) in Porto Seguro, in the state of Bahia (Nuvoloni et al. 2021). Other monocotyledonous plants of the families Heliconiaceae, Strelitziaceae, Zingiberaceae and Pandanaceae were considered reproductive hosts of R. indica (Carrillo et al. 2012). The mite causes yellowing and necrosis of leaves and even death of young plants (Etienne and Flechtmann 2006; Rodrigues et al. 2007).

Raoiella indica was first recorded in the Americas from specimens on the Caribbean island of Martinique (Flechtmann and Etienne 2004). Since then, economic losses have been recorded, mainly for coconut producers, in Caribbean countries (Rodrigues et al. 2007; Morais et al. 2011; Kane et al. 2012). In 2007, the mite was recorded for the first time in South America, in Venezuela (Vásquez et al. 2008) and later registered for the first time in Brazil in 2009, in the State of Roraima (Navia et al. 2011). In 2011, the mite was already in Manaus, in the state of Amazonas, still in the Brazilian Amazon region (Rodrigues and Antony 2011). In the following years, it was reported in several states of Brazil (Gómez-Moya et al. 2017; Hata et al. 2017; Oliveira et al. 2016; Barroso et al. 2019; Nora et al. 2019; Amaro et al. 2021; Castro et al. 2021). The mite was also been reported in Colombia (Carrillo et al. 2011) and more recently in Ecuador and Paraguay (Alcívar et al. 2020; Ramírez et al. 2020).

In the State of Pará, North Region of Brazil, R. indica was recorded in the municipalities of the northwest, a sub-region that is closer to the State of Amazonas, called ‘Low Amazons’. The first record was in the municipality of Juruti, in 2016, by technicians from the ‘Agencia de Defesa Agropecuária do Pará’—ADEPARA (Adepara 2016). Subsequently, surveys carried out in 12 of the 15 municipalities of the low amazons revealed the presence of R. indica in 11 of these, Alenquer, Almeirim, Belterra, Curuá, Faro, Mojuí dos Campos, Monte Alegre, Óbidos, Prainha, Santarém and Terra Santa (Moraes et al. 2017; Noronha et al. 2018).

Pará is the second largest state from Brazil (1,248 mi Km2), more than twice the territory of France and five times that of São Paulo, the most important Brazilian scientific and economic center. The state is the leader in the national production of açaí, and the 3rd and 4th largest producer of bananas and coconuts, respectively (Ibge 2022). Not all regions of the state are interconnected. The relative isolation of the sub-regions would make it possible to plan effective phytosanitary barriers, by ADEPARA, seeking to hinder the dispersion of R. indica to the municipalities that produce açai, banana and coconut. In this context, we aimed to confirm the presence of the red palm mite in the sub-region of Southeast Pará, hitherto free of the mite.

Material and methods

Between October and November 2019, shortly before the COVID-19 pandemic was triggered by the authorities of the World Health Organization (WHO), it was observed, by chance, that coconut and banana plants infested by Raoiella indica, in residential backyards in municipalities from Marabá (5°12′26.75" S and 49°02′46.14" O) and Parauapebas (6°04′39.50" S and 49°51′43.57" O).

Some specimens of mite were collected, taken to the entomology laboratory of the Universidade Federal Rural da Amazônia (UFRA), University Campus of Parauapebas, and mounted on slides in Hoyer's medium, to confirm the identification with the aid of a phase contrast microscope and dichotomous key for species of the genus Raoiella Hirst (Beard et al. 2018).

Additionally, other plants were examined, whose families are known to have host species of R. indica, which were located in residential backyards close to infested coconut and banana trees. Three species from the Araceae Family, three from Arecaceae, one Heliconiaceae and two Zingiberaceae, in addition to the banana Musaceae, were examined. Ten banana and coconut plants and between two and three plants of the other species were examined in each municipality.

From the observation of the presence of the mite in the municipalities in 2019, about ten incursions were made in areas of açaí cultivation, in both municipalities, to locate the mite in commercial plantations of the crop. More recently, in July 2022, a mite colony, with all stages of development, was found on a plant of the species Roystonea oleracea (Jacq.) (Arecaceae) and adult individuals of the mite on four plants of the species Alpinia purpurata (Vieill.) K. Schum. (Zingiberaceae), from a residential backyard in the city of Parauapebas (Fig. 1).

Fig. 1

The mite Raoiella indica on an imperial palm leaflet. A Mite colony with all stages of development (egg, nymphs, male and female adults); B detail of a female; C female and D male R. indica under a microscope

Results

Raoiella indica had been reported only in the Low Amazons municipalities (Fig. 2). In the municipalities prospected in the Northeast of Pará, until 2018, the mite was not detected (Fig. 2). In the following year (2019), however, the mite was found in Southeast Pará, in municipalities distant about 1,000 km from the places where it occurs in the State (Fig. 2).

Fig. 2

Map of the State of Pará, highlighting the municipalities where the red palm mite was found (in red) in the Low Amazons (Moraes et al. 2017; Noronha et al. 2018); municipalities where the mite was prospected and not found (in green), most in the 'Northeast of Pará' (Noronha et al. 2018); municipalities of Marabá and Parauapebas (in yellow) in the Southest of Pará

Abundance of R. indica, with the presence of all stages of development, was only observed in coconut, banana and imperial palm. At the time, these mites were not observed in açaí plants (nor in more recent surveys). A few individuals, all adults, were observed on areca palm (Dypsis lutescens (H.Wendl.) Beentje & J.Dransf.) leaves, in Marabá, and on red ginger leaves, in Parauapebas (Table 1).

Table 1

Hosts investigated in the municipalities of Marabá and Parauapebas, between October and November 2019 to July 2022, in the region of Carajás, in the southeast of the State of Pará

Common name	Family	Scientific name	Locality*	Year	Presence of R. indica**
Damp Cane	Araceae	Dieffenbachia seguine (Jacq.) Schott	P	2019	–
Flamingo Flower		Anthurium andraeanum Linden ex André	M	2019	–
Pacova		Philodendron martianum Engl	M	2019	–
Coconut tree	Arecaceae	Cocos nucifera L	M and P	2019	+  +  +
Areca palm		Dypsis lutescens (H.Wendl.) Beentje & J.Dransf	M	2019	+
Açai plantations		Euterpe oleracea Mart	M and P	2019/ 2022	–
Imperial palm		Roystonea oleracea (Jacq.)	P	2022	+  +
Heliconia	Heliconiaceae	Heliconia sp.	M	2019	–
Banana tree	Musaceae	Musa x paradisiaca L	M and P	2019	+  +  +
Torch ginger	Zingiberaceae	Etlingera elatior (Jack.) R.M. Smith	P	2019	–
Red ginger		Alpinia purpurata (Vieill.) K. Schum	P	2022	+

*M = Marabá; P = Parauapebas. ** +  +  +  = Great abundance of Raoiella indica found; +  +  = Intermediate abundance of R. indica found; +  = few individuals of R. indica found;-= Raoiella indica not found

Discussion

In the state of Pará, there are three Köppen climate types: Af- equatorial tropical, Am—monsoon tropical and Aw—savanna tropical (Alvares et al. 2013). The Aw climate occurs only in the Southeast of Pará sub-region, comprising a defined dry period in addition to high Amazonian temperatures (Alvares et al. 2013). Phytophagous mites are generally favored by periods of low rainfall and relative humidity (Cruz et al. 2013). Raoiella indica completed its development only in between 20 and 30 °C of air temperature and the reproductive parameters were higher at 27 °C, this being its optimal temperature (Fidelis et al. 2019). The climate in Marabá and Parauapebas is Aw (Köppen and Geiger, 1928), with average temperatures above 26 °C and annual precipitation around 1,800 mm (Inmet 2022). Thus, an estimate based on computer models showed probabilities of 0.4 and 0.6 (scale from 0 to 1) of R. indica occurring in the municipalities of Marabá and Parauapebas (Amaro et al. 2021). This work corroborates this estimate.

The municipalities of Southeast Pará are much closer to the states of Maranhão and Tocantins than to the Low Amazons (Fig. 1); in addition, there are more interstate trade routes from Southeast Pará than between the sub-regions of the state. This allows us to conjecture that it is likely that the population of R. indica found in this study came from these other states, from populations already identified in Northeast Brazil. There is still no record of the mite in Maranhão and Tocantins (Amaro et al. 2021).

This work is the first record of the mite in areca palm. This mite, in their dispersal, they could land in any plant species, but it does not mean this plant is a reproductive host for the mite. It is necessary to analyze whether the mite is capable of developing and reproducing on the plant (Carrillo et al. 2012).

Since the mite was found in Southeast Pará, and considering the theoretically favorable climatic conditions for R. indica in this region, it is now essential to conduct more in-depth studies, in the region and nearby states, about the dynamics of these mite populations and the occurrence or not of effective natural enemies for later sustainable pest management strategies.