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Functional and numerical responses of the predatory mite Amblyseius aerialis (Acari: Phytoseiidae) to Aceria guerreronis (Acari: Eriophyidae)

Ferreira, Camila Tavares 1 ; Noronha, Aloyséia Cristina da Silva 2 ; Souza Neto, Eduardo Pereira 3 ; De Oliveira, Raimundo Parente 4 ; Lins, Paulo Manoel Pontes 5 and Batista, Telma Fátima Vieira 6

1✉ Laboratório de Proteção de Plantas (LPP), Universidade Federal Rural da Amazônia (UFRA), Belém, PA, Brazil.
2Empresa Brasileira de Pesquisa Agropecuária (Embrapa Amazônia Oriental), Belém, PA, Brazil.
3Laboratório de Acarologia, Universidade Federal do Ceará (UFC), Fortaleza, CE, Brazil.
4Empresa Brasileira de Pesquisa Agropecuária (Embrapa Amazônia Oriental), Belém, PA, Brazil.
5Sococo S. A. Agroindústria da Amazônia, Moju, PA, Brazil.
6Laboratório de Proteção de Plantas (LPP), Universidade Federal Rural da Amazônia (UFRA), Belém, PA, Brazil.

2022 - Volume: 62 Issue: 1 pages: 27-35

https://doi.org/10.24349/w600-25ar

Original research

Keywords

coconut mite biological control Cocos nucifera predation oviposition

Abstract

The coconut mite, Aceria guerreronis Keifer, is one of the main pests of the coconut tree (Cocos nucifera L.) worldwide. Its control is mainly based on the use of acaricides. However, due to the habitat of this pest mite, which is protected by fruit bracts that act as a physical barrier, chemical control is often inefficient. Thus, natural enemies have been studied as an alternative to acaricides. We evaluated the functional and numerical responses of Amblyseius aerialis (Muma) to increasing densities of A. guerreronis (40, 80, 160, 240 and 360) and additionally the oviposition rates of the phytoseiid A. aerialis over 11 days on different food sources: coconut pollen, A. guerreronis and a mix of pollen and A. guerreronis. Our results showed that Amblyseius aerialis showed a type III functional response, where prey consumption increasing as the density of A. guerreronis increased, with a maximum consumption of up to 175 prey per predator. All the prey densities allowed female oviposition. The number of eggs laid by A. aerialis increased with increasing prey density and stabilized between 240 and 360 A. guerreronis individuals, with an average oviposition of 1.7 eggs/female. Furthermore, our results showed that all the food sources (coconut pollen, A. guerreronis and a mix of pollen and A. guerreronis) supported oviposition. The mean oviposition was approximately 1.5 eggs/female on all the food sources. Our study suggests that A. aerialis can be effective in the biological control of A. guerreronis. However, further studies are needed to investigate whether A. aerialis can explore the habitat of A. guerreronis and if that prey can support the development of immature stages and the reproduction of A. aerialis.


Introduction

The coconut mite (Aceria guerreronis Keifer) is a major pest of coconut (Cocos nucifera L.) fruits. It occurs in several countries worldwide (Haq et al. 2002; Lawson-Balagbo et al. 2008a; Fernando and Aratchige 2010; Negloh et al. 2011). In Brazil, it is found in all coconut plantations but with a lower incidence than in Africa and Asia (Lawson-Balagbo et al. 2008a). It develops in the perianth of the fruits below the bracts, initially causing a yellowish-white spot in a triangular shape close to the margin of the perianth. As the fruits grow, the damaged tissue becomes necrotic (Haq et al. 2002; Galvão et al. 2008; Navia et al. 2013). This damage leads to a reduction in the yield of solid and liquid albumens and even premature fruit fall (Wickramananda et al. 2007). A higher A. guerreronis incidence on fruits can decrease the mean number of fruits harvested per bunch by approximately 60% and decrease the liquid albumen volume by 28% (Rezende et al. 2016).

Chemical control has been applied to the coconut mite worldwide. Successive pesticide sprayings are necessary to achieve satisfactory control as this pest develops in a habitat protected by fruit bracts that act as a physical barrier. However, this practice can cause undesired effects such as elimination of natural enemies, environmental contamination and presence of residues in fruits (Lawson-Balagbo et al. 2007; Fernando and Aratchige 2010; Van Leeuwen et al. 2010; Lima et al. 2012). The protection provided by bracts in fruits attacked by A. guerreronis was confirmed by Silva et al. (2017), who showed that bracts prevented exposure to the pesticide and that the pest was only vulnerable while dispersing. Therefore, alternative forms of control are necessary to manage this important pest.

The biological control of the coconut mite has been extensively researched. Predatory mites belonging to the family Phytoseiidae are considered the main natural enemies of the coconut mite, including Neoseiulus baraki (Athias-Henriot), Neoseiulus paspalivorus (De Leon), Amblyseius largoensis (Muma), Neoseiulus recifensis Gondim Jr. and Moraes and Euseius alatus De Leon (Lawson-Balagbo et al. 2008a, b; Reis et al. 2008; Galvão et al. 2011; Negloh et al. 2011; Lima et al. 2012; Melo et al. 2015).

The predatory mite Amblyseius aerialis (Muma) was predominant in surveys in coconut plantations in the municipality of Moju, in the state of Pará, Brazil. It was found in almost the same proportion both on leaflets and fruits, mainly on the external surfaces and in lesser quantities under the bracts after the A. guerreronis attack (unpublished results). According to McMurtry et al. (2013), this predator is considered a type III generalist, as it feeds on a wide variety of prey and pollen of different plant species as complementary food sources, being found on more than 20 species of host plants throughout Brazil (Castillo and Noronha 2008; Demite et al. 2014; Amaral et al. 2018; Ferreira et al. 2018). This species is commonly found in the Amazon region in different crops, such as fruit trees (Mineiro et al. 2009; Ferreira et al. 2018), physic nut (Jatropha curcas L.) (Cruz et al. 2012), rubber tree (Hevea brasiliensis L.) (Nuvoloni et al. 2014), coconut (C. nucifera) (Cruz et al. 2015), nance (Byrsonima crassifolia (L.) Kunth) (Noronha et al. 2020) and oil palm (Elaeis guineensis Jacq.) (Cruz et al. 2019). However, there are no reports on the interaction between this species and the coconut mite in spite of its high abundance in this region.

The study of the functional and numerical responses of a predator represents an important step in determination of its ability to regulate pests (Filgueiras et al. 2020) providing relevant information about the predation rate and prey density (Solomon 1949), and its ability to convert food into eggs (Hassell 1978). Thus, our study evaluated the functional and numerical responses of this predator to different densities of A. guerreronis. Additionally, to determine the relative nutritional value of coconut pollen compared to A. guerreronis we assessed A. aerialis fecundity when offered coconut pollen, A. guerreronis and a mix of coconut pollen and A. guerreronis.

Material and methods

Rearing of the predatory mite

All bioassays were conducted in the Laboratory of Entomology of the Empresa Brasileira de Pesquisa Agropecuária (Embrapa Amazônia Oriental), Belém, state of Pará, Brazil.

Colonies of the predatory mite, A. aerialis, were established from individuals collected from leaflets and fruits in commercial coconut plantations owned by Sococo S. A. Agroindústria da Amazônia, in the municipality of Moju, state of Pará (02°06'38.73'' S, 48°40' 45.71'' W). The mites were kept in rearing units made of plastic trays (16 × 22 × 7 cm) containing a piece of polyethylene foam (2 cm thickness) that was kept permanently moist by the daily addition of distilled water. Additionally, a 10 × 15 cm resin plate (Paviflex®) was laid on top of the foam piece, the edges of which were covered with cotton strips moistened with distilled water to prevent the mites from escaping. In the middle of the plate, pieces of cotton fibre were placed under a microscope coverslip (2 × 2 cm) to serve as a shelter, providing a place for the oviposition and development of the mites. The predators were fed daily with fresh coconut pollen, and 400 individuals of A. guerreronis in different stages were provided on perianth fragments (~1 cm3). The predators were transferred weekly to new rearing units kept in an incubator (25 ± 1 °C, 70 ± 10% RH, 12: 12 h L: D).

Functional and numerical responses

The functional and numerical response experiment was conducted in an experimental unit composed of a Petri dish (2 cm high, Ø 5 cm) containing a disc of filter paper and a piece of coconut leaflet with the abaxial side facing up. All the edges of the coconut leaflet were surrounded with hydrophilic cotton moistened with distilled water to prevent the mites from escaping. In each experimental unit, one of five densities of A. guerreronis (40, 80, 160, 240 and 360 mites/experimental unit) were offered to one female of A. aerialis (four days old), replicated 20 times for each prey density. During two days the number of prey consumed and the number of eggs deposited by A. aerialis females were counted every 24h, with daily replacement of prey to the initial amount offered. Data from the first day were excluded to avoid the influence of previous feeding experience (Sabelis 1990, Carrillo and Peña 2012). Prey consumption was assessed by subtracting the number of A. guerreronis that remained in the arena from the number initially provided. The experiment was in random blocks and conducted in an incubator (25 ± 1 °C, 70 ± 10% RH, 12: 12 h L: D).

Oviposition

The oviposition of the predator fed on three food sources, A. guerreronis, coconut pollen and a mixture of coconut pollen and A. guerreronis was investigated under the same environmental conditions used for the functional and numerical response. A mated female of A. aerialis (4 days old) was placed in each unit, and food sources (~240 A. guerreronis individuals, pollen (0.5 g) and mixture of ~240 A. guerreronis individuals + pollen (0.5 g)) was offered daily to each female. All the units were kept in an incubator (25 ± 1 °C, 70 ± 10% RH, 12:12 h L:D). The number of predator eggs laid in each replicate was recorded, and the eggs were removed daily for 11 days. Oviposition data from the first day were excluded to avoid the influence of previous feeding experience (Sabelis 1990, Carrillo and Peña 2012). The experiment was completely randomized, and for each food source, 20 females (replicates) were tested.

Data analysis

Functional and numerical responses

To determine the type of functional response (Type I, II or III), logistic regression curves were adjusted between the proportion of prey consumed and prey density, according to Juliano (1993). The type of functional response was determined by the significance and sign of the linear coefficient of the equations obtained for the proportions of prey eaten. Non-significant and linear coefficients indicate a type I response, negative and significant coefficients indicate a type II response, and positive and significant coefficients indicate a type III response (Holling 1959, 1961).

The parameters of attack rate (a') and handling time (Th) were estimated by the equation Ne = N0\{1 – exp[a'(ThNe – T)]\} (Rogers 1972) (for experiments without prey replacement) using nonlinear least-squares regressions. Here, Ne refers to the number of prey eaten; N0 , the initial prey density; a', the attack rate (the proportion of prey captured by a predator per unit of search time); and Th, the prey handling time (the time needed for a predator to capture, kill and digest the prey). All the statistical procedures were performed in SAS (SAS Institute 2018).

The numerical response was estimated through the polynomial regression of the number of eggs per A. aerialis female as a function of the prey density. The model was selected based on simplicity, parsimony and high values of F and R2 using Table Curve 2D 5.01 software (Systat Software 2014).

Oviposition

The oviposition rate data were analysed using repeated measures ANOVA and Tukey's test (HSD) to determine differences among the food sources. SAS software (2018) was used for the analyses.

Results

Functional and numerical responses

The number of prey consumed increased as availability increased (Figure 1a). The proportion of prey consumed initially increased under lower prey densities (40 and 80 mites) and decreased afterwards (Figure 1b), suggesting a type III functional response.

Figure 1. Functional response of Amblyseius aerialis fed with different densities of Aceria guerreronis, expression in number of prey consumed (a) and the proportion of prey eaten (b). In panel (a), the curve was fitted by Roger's equation III to the functional response, while in panel (b) the line represents the predicted values of Holling's type III disc equation.

A type III functional response was confirmed by the significance and sign of the linear coefficient of Hollings's equation, which showed a significant and positive linear coefficient (Table 1). The attack rate (a') and the handling time (Th) of A. aerialis fed with A. guerreronis were 0.0011 h-1 and 0.11 h, respectively (Table 2).

Table 1. Holling's equation and type of functional response of Amblyseius aerialis fed on different densities of Aceria guerreronis.

Table 2. Parameters (±SE) of functional responses of Amblyseius aerialis fed on increase densities of Aceria guerreronis.

All prey densities offered allowed oviposition by A. aerialis females. The number of eggs laid increased with increasing prey density and stabilized at high densities (240 and 360), with an average oviposition rate of 1.7 ± 0.09 eggs/female (Figure 2). Therefore, these findings supported the following bioassays using only coconut mite as prey.

Figure 2. Mean number of eggs laid by Amblyeius aerialis females provided with different densities of Aceria guerreronis.

Oviposition

The mean number of eggs laid by Amblyseius aerialis females was not affected by food sources (F2,53 = 1.97, P = 0.15). The females fed on Aceria guerreronis, coconut pollen and a mixture of coconut pollen and A. guerreronis laid an average of 1.4, 1.4 and 1.6 eggs/female/day (respectively) during the 11-day oviposition period (data from the first day were excluded) (Figure 3).

Figure 3. Average oviposition rates (eggs/female ± SE) by Ambyseius aerialis females given different food resources per 10 days.

Discussion

The functional response of A. aerialis showed a sigmoid curve, indicating a type III response, i.e. an increase in prey consumption with prey density. In contrast, the proportion of prey eaten decreased with increasing density. However, according to Holling (1965), type III predators show a reduced response at low prey densities, unlike type II predators. Since the prey in this experiment was an eriophyoid and was smaller than other mites (approximately 200 µm in length), the consumption by the predators increased, as they need to ingest a greater quantity of A. guerreronis to meet their nutritional requirements; this phenomenon characterizes the potential regulation of the prey population. However, it is difficult for predators to reach A. guerreronis under bracts due to the tight adherence of the bracts to the surface of the fruit; this prevents larger mites, such as most Phytoseiids, from penetrating this space at the same time as eriophyoids (Silva et al. 2016). The predation of A. guerreronis by other generalist predators, such as A. largoensis and E. alatus, may occur on the exposed surface of fruits, on spikelets when mites leave older fruits for younger ones, when mites move from one plant to another by aerial dispersion, and rarely, under the bracts of a fruit (Melo et al. 2015).

The phytoseiid N. baraki showed a type III functional response when fed with different densities of A. guerreronis (Lima et al. 2012; Teodoro et al. 2020). Lima et al. (2012) reported a maximum mean consumption of ~100 mites at a density of 240 A. guerreronis, and Teodoro et al. (2020) reported a mean consumption of ~150 mites at the same density. In our study, we observed a mean consumption by A. aerialis of ~140 A. guerreronis at a density of 240 mites. Despite being different species of predators, our results showed a predation rate similar to those found by other authors and suggest that A. aerialis may be effective in controlling A. guerreronis.

The handling time and attack rate shown by A. aerialis feeding on A. guerreronis (0.0011 and 0.11, respectively) were close to the values reported by Teodoro et al. (2020) for N. baraki (0.004 and 0.13) feeding on the same prey species. The time required by A. aerialis to identify, attack, subdue, and consume a unit of prey (handling time) was lower. This indicates that this predator needed less time to consume a single prey, which increased its prey consumption over a 24 h period. The attack rate determines the ability of a predator to capture its prey within a specific area (Holling 1959), and our findings demonstrate that A. aerialis was effective in capturing more prey per area than N. baraki.

The predatory mite Proctolaelaps bickleyi (Bram) (Acari: Melicharidae) had a higher attack rate (0.1907) and a shorter handling time (0.0292) when provided with different densities of A. guerreronis (Lima et al. 2012). These values are better than those observed in our study, but the attack rate and handling time can change according to the predatory species and kind of prey.

The numerical response showed that even at lower prey densities (i.e., 40 and 80), A. aerialis could oviposit and that the number of eggs laid/day increased at high densities, indicating that the increment of individuals in the population will be greater as prey density increases. It is expected that to control pest mites, a good predatory mite should have, among other characteristics, the capacity to convert their prey into egg biomass and increase their population given abundant prey (Sabelis 1990). Galvão et al. (2007) reported a daily oviposition of 1.2 eggs per female for A. largoensis fed on A. guerreronis. Amblyseius largoensis is a natural enemy frequently found on coconuts and may also play a key role in the natural control of this pest. Lima et al. (2012) observed similar results for N. baraki fed on A. guerreronis. The mean number of eggs laid per day by N. baraki females at the highest density (140) was ~1.2. In our study, at a comparabler density (160 A. guerreronis), we observed a mean of 1.5 eggs laid per day. Thus, these results reinforce that A. aerialis can be effective in controlling A. guerreronis.

The possible benefit in the predator's fitness was verified by the daily oviposition of the predator A. aerialis (in the oviposition test when fed with A. guerreronis and coconut pollen). According to the classification by McMurtry et al. (2013), mites belonging to the genus Amblyseius genus have type III feeding habits, which are characterized by successful reproduction when feeding on a wide variety of prey, including mites of the Eriophyidae family. However, some species also successfully reproduce when feeding on pollen. The results obtained in this experiment are important, as they show that there was no difference in the predator's oviposition rate when fed coconut mites, coconut pollen or both. This generalist feeding habit may support the conservation of this predator in the field when prey is scarce feeding on coconut pollen.

This study represents the first effort to investigate the predatory and reproductive behaviours of A. aerialis on A. guerreronis through oviposition and predation activity. Our results suggest that this predator has the potential to control A. guerreronis. Moreover, the reproduction of A. aerialis is supported by either A. guerreronis or coconut pollen, suggesting that A. aerialis could be sustained under field conditions on coconut pollen as alternative food. Additional studies are necessary to evaluate life table parameters and to investigate under which circumstances A. aerialis can enter the microhabitat of A. guerreronis.

Acknowledgements

We thank the Sococo S. A. Agroindústria da Amazônia company for financial support and the Amazon Research and Support Foundation (Fundação Amazônia de Amparo a Estudos e Pesquisas - FAPESPA) for a scholarship granted to the first author.



References

  1. Amaral F.S.R., Lofego A.C., Cavalcante A.C.C. 2018. Oviposition rates of Amblyseius aerialis (Muma) and Amblyseius chiapensis DeLeon (Acari: Phytoseiidae) under seven foods different patterns for the same genus. Syst. Appl. Acarol., 23: 795-798. https://doi.org/10.11158/saa.23.5.1
  2. Carrillo D., Peña J.E. 2012. Prey-stage preferences and functional and numerical responses of Amblyseius largoensis (Acari: Phytoseiidae) to Raoiella indica (Acari: Tenuipalpidae). Exp. Appl. Acarol., 57: 361-372. https://doi.org/10.1007/s10493-011-9488-7
  3. Castillo A.B., Noronha A.C.S. 2008. Estudio de los aspectos fundamentales de la biología de Amblyseius aerialis (Muma) (Acari: Phytoseiidae) en condiciones de laboratorio. CitriFrut., 25: 45-52.
  4. Cruz W.P., Sarmento R.A., Teodoro A.V., Erasmo E.A.L., Pedro Neto M., Ignácio M., Ferreira Júnior D.F. 2012. Acarofauna em cultivo de pinhão-manso e plantas espontâneas associadas. Pesquisa Agropecuária Brasileira, 47: 319-327. https://doi.org/10.1590/S0100-204X2012000300002
  5. Cruz W.P., Krug C., Vasconcelos G.J.N., Moraes G.J. 2015. Diversity of mites associated with Raoiella indica (Acari: Prostigmata) on coconut palms in the central region of the Brazilian Amazonia, with emphasis on the predaceous Phytoseiidae (Acari: Mesostigmata). Syst. Appl. Acarol., 20: 875-886. https://doi.org/10.11158/saa.20.8.4
  6. Cruz W.P., Krug C., Vasconcelos G.J.N., Moraes G.J. 2019. Mite (Arachnida: Acari) diversity and abundance on oil palms in the central region of the Brazilian Amazonia. Syst. Appl. Acarol., 24: 1736-1750. https://doi.org/10.11158/saa.24.9.10
  7. Demite P.R., McMurtry J.A., Moraes G.J. 2014. Phytoseiidae Database: a website for taxonomic and distributional information on phytoseiid mites (Acari). Zootaxa, 5: 571-577. https://doi.org/10.11646/zootaxa.3795.5.6
  8. Fernando L.C.P., Aratchige N.S. 2010. Status of coconut mite Aceria guerreronis and biological control research in Sri Lanka. In: Sabelis MW, Bruin J, editors. Trends in acarology. Amsterdam: Springer. pp. 379-384. https://doi.org/10.1007/978-90-481-9837-5_68
  9. Ferreira C.T., Krug C., Garcia M.V.B., Moraes G.J. 2018. Leprosis mite and other mite species (Acari) associated to orange groves in Brazilian Central Amazon. Syst. Appl. Acarol., 23: 449-462. https://doi.org/10.11158/saa.23.3.4
  10. Filgueiras R.M.C., Mendes J.A., Silva F.W.B., Sousa Neto E.P., Melo J.W.S. 2020. Prey stage preference and functional and numerical responses of Neoseiulus barkeri Hughes (Acari: Phytoseiidae) to eggs of Raoiella indica Hirst (Acari: Tenuipalpidae). Syst. Appl. Acarol., 25: 1147-1157. https://doi.org/10.11158/saa.25.6.16
  11. Galvão A.S., Gondim Jr M.G.C., Moraes G.J., Oliveira J.V.D. 2007. Biology of Amblyseius largoensis (Muma) (Acari: Phytoseiidae), a potential predator of Aceria guerreronis Keifer (Acari: Eriophyidae) on coconut trees. Neotrop. Entomol., 36: 465-470. https://doi.org/10.1590/S1519-566X2007000300016
  12. Galvão A.S., Gondim Jr M.G.C., Michereff E.S.J. 2008. Escala diagramática de dano de Aceria guerreronis Keifer (Acari: Eriophyidae) em Coqueiro. Neotrop. Entomol., 6: 723-728. https://doi.org/10.1590/S1519-566X2008000600015
  13. Galvão A.S., Gondim Jr M.G.C., Moraes G.J., Melo J.W.S. 2011. Distribution of Aceria guerreronis and Neoseiulus baraki among and within coconut bunches in northeast Brazil. Exp. Appl. Acarol., 54: 373-384. https://doi.org/10.1007/s10493-011-9464-2
  14. Haq M.A., Sumangala K., Ramani N. 2002. Coconut mite invasion, injury and distribution. In: Fernando LCP, Moraes GJ, Wickramananda IR, editors. Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis). Sri Lanka: Coconut Research Institute: 41-49.
  15. Hassell M.P. 1978. The dynamics of arthropod predator-prey systems. Princeton (NJ): Princeton University Press. 248 pp.
  16. Holling C.S. 1959. Some characteristics of simple types of predation and parasitism. The Canadian Entomologist, 91: 385-398. https://doi.org/10.4039/Ent91385-7
  17. Holling C.S. 1961. Principles of insect predation. Annual Review of Entomology, 6: 163-182. https://doi.org/10.1146/annurev.en.06.010161.001115
  18. Holling C.S. 1965. The functional response of predators to prey density and its role in mimicry and population regulation. The Memoirs of the Entomological Society of Canada, 97: 5-60. https://doi.org/10.4039/entm9745fv
  19. Juliano S.A. 1993. Nonlinear Curve Fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J, editors. Design and Analysis of Ecological Experiments. New York: Chapman and Hall: 159-182.
  20. Lawson-Balagbo L.M., Gondim Jr M.G.C., Moraes G.J., Hanna R., Schausberger P. 2007. Refuge use by the coconut mite Aceria guerreronis: fine scale distribution and association with other mites under the perianth. Biol. Control, 43: 102-110. https://doi.org/10.1016/j.biocontrol.2007.05.010
  21. Lawson-Balagbo L.M., Gondim Jr M.G.C., Moraes G.J., Hanna R., Schausberger P. 2008a. Exploration of the acarine fauna on coconut palm in Brazil with emphasis on Aceria guerreronis (Acari: Eriophyidae) and its natural enemies. Bull. Entomol. Research, 98: 83-96. https://doi.org/10.1017/S0007485307005421
  22. Lawson-Balagbo L.M., Gondim Jr M.G.C., Moraes G.J., Hanna R., Schausberger P. 2008b. Compatibility of Neoseiulus paspalivorus and Proctolaelaps bickleyi, candidate biocontrol agents of the coconut mite Aceria guerreronis: spatial niche use and intraguild predation. Exp. Appl. Acarol., 45: 1-13. https://doi.org/10.1007/s10493-008-9156-8
  23. Lima D.B., Melo J.W.S., Gondim Jr M.G.C., Moraes G.J. 2012. Limitations of Neoseiulus baraki and Proctolaelaps bickleyi as control agents of Aceria guerreronis Keifer. Exp. Appl. Acarol., 56: 233-246. https://doi.org/10.1007/s10493-012-9515-3
  24. McMurtry J.A., Moraes G.J., Famah Sourassou N. 2013. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst. Appl. Acarol., 18: 297-320. https://doi.org/10.11158/saa.18.4.1
  25. Melo J.W.S., Lima D.B., Staudacher H., Silva F.R., Gondim Jr M.G.C., Sabelis M.W. 2015. Evidence of Amblyseius largoensis and Euseius alatus as biological control agent of Aceria guerreronis. Exp. Appl. Acarol., 67: 411-421. https://doi.org/10.1007/s10493-015-9963-7
  26. Mineiro J.L.C, Silva W.R., Silva R.A. 2009. Ácaros em fruteiras e outras plantas no Estado do Amapá. Biota Neotropica, 9: 103-106. https://doi.org/10.1590/S1676-06032009000200009
  27. Navia D., Godim Jr M.G.C., Aratchige N.S., Moraes G.J. 2013. A review of the status of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), a major tropical mite pest. Exp. Appl. Acarol., 59: 67-94. https://doi.org/10.1007/s10493-012-9634-x
  28. Negloh K., Hanna R., Schausberger P. 2011. The coconut mite, Aceria guerreronis, in Benim and Tanzania: occurrence, damage and associated acarine fauna. Exp. Appl. Acarol., 55: 361-374. https://doi.org/10.1007/s10493-011-9474-0
  29. Noronha A.C.S., Mineiro J.L.C., Ferla N.J., Castro T.M.M.G., Silva G.L., Lofego A.C., Azevedo A.O. 2020. Mites associated with Byrsonima crassifolia (L.) Kunth (Malpighiaceae) in the state of Pará, Brazil. Entomol. Communications, 2: ec02026. https://doi.org/10.37486/2675-1305.ec02026
  30. Nuvoloni F.M., Lofego A.C., Rezende J.M., Feres R.J.F. 2014. Phytoseiidae mites associated with Hevea spp. from the Amazon region: A hidden diversity under the canopy of native trees. Syst. Biodiv., 13: 182-206. https://doi.org/10.1080/14772000.2014.985344
  31. Reis A.C., Gondim Jr. M.G.C., Moraes G.J., Hanna R., Schausberger P., Barros R. 2008. Population dynamics of Aceria guerreronis Keifer (Acari: Eriophyidae) and associated predators on coconut fruits in northeastern Brazil. Neotrop. Entomol., 37: 457-462. https://doi.org/10.1590/S1519-566X2008000400015
  32. Rezende D., Melo J.W.S., Oliveira J.E.M., Gondim M.G.C. 2016. Estimated crop loss due to coconut mite and financial analysis of controlling the pest using the acaricide abamectin. Exp. Appl. Acarol., 69: 297-310. https://doi.org/10.1007/s10493-016-0039-0
  33. Rogers D. 1972. Random search and insect population models. Journal of Animal Ecology, 41: 369-383. https://doi.org/10.2307/3474
  34. Sabelis M.W. 1990. How to analyse prey preference when prey density varies? A new method to discriminate between effects of gut fullness and prey type composition. Oecologia, 82: 289-298. https://doi.org/10.1007/BF00317473
  35. SAS Institute. 2018. SAS/STAT User's guide, version 8.02, TS level 2 MO. Cary, North Carolina, SAS Institute Inc.
  36. Silva F.R., Moraes G.J., Lesna I., Sato Y., Vasquez C., Hanna R., Sabelis M.W., Janssen A. 2016. Size of predatory mites and refuge entrance determine success of biological control of the coconut mite. Biol. Control, 61: 681-689. https://doi.org/10.1007/s10526-016-9751-2
  37. Silva V.F, França G.V., Melo J.W.S., Guedes R.N.C., Gondim Jr. M.G.C. 2017. Targeting hidden pests: acaricides against the coconut mite Aceria guerreronis. Journal of Pest Science, 90: 207-215. https://doi.org/10.1007/s10340-016-0776-1
  38. Solomon M.E. 1949. The natural control of animal populations. The Journal of Animal Ecology, 18: 1-35. https://doi.org/10.2307/1578
  39. SYSTAT SOFTWARE. TABLE CURVE 2D (Trial Version 5.01). San Jose, 2014. Available from: https://systatsoftware.com/products/tablecurve-2d/tablecurve-2d-version-5-01-cumulative-patch/
  40. Teodoro A.V., Oliveira N.N.F.C., Galvão A.S., Sena Filho J.G., Pinto-Zevallos D.M. 2020. Interference of plant fixed oils on predation and reproduction of Neoseiulus baraki (Acari: Phytoseiidae) feeding on Aceria guerreronis (Acari: Eriophyidae). Biol. Control, 143: 104204. https://doi.org/10.1016/j.biocontrol.2020.104204
  41. Van Leeuwen T., Vontas J., Tsagkarakou A., Dermauw W., Tirry L. 2010. Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochem. Molec. Biol., 40: 563-572. https://doi.org/10.1016/j.ibmb.2010.05.008
  42. Wickramananda I.R., Peiris T.S.G., Fernando M.T., Fernando L.C.P., Edgington S. 2007. Impact of the coconut mite (Aceria guerreronis Keifer) on the coconut industry in Sri Lanka. Cord., 23: 1-16.


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Article editorial history
Date received:
2021-06-29
Date accepted:
2021-12-10
Date published:
2022-01-10

Edited by:
Kreiter, Serge

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This work is licensed under a Creative Commons Attribution 4.0 International License
2022 Ferreira, Camila Tavares; Noronha, Aloyséia Cristina da Silva; Souza Neto, Eduardo Pereira; De Oliveira, Raimundo Parente; Lins, Paulo Manoel Pontes and Batista, Telma Fátima Vieira
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