Share this article    

       

       

New parasitism record of Pyemotes tritici (LaGreze-Fossat & Montagne, 1851) (Acari: Pyemotidae) on boll weevils inside cotton squares

da Silva, Carlos A. D. 1 ; de Moraes, Gilberto J. 2 ; Castilho, Raphael C. 3 ; Ramalho, Francisco S. 4 and Lima, Tardelly A. 5

1✉ Embrapa Algodão, Rua Oswaldo Cruz, n° 1.143, Centenário, CEP 58428‑095, Campina Grande, PB, Brazil & Universidade Estadual da Paraíba, Programa de Pós-Graduação em Ciências Agrárias, Rua Baraunas, n° 351, Universitário, CEP 58429-570 Campina Grande, PB, Brazil.
2Escola Superior de Agricultura Luiz de Queiroz (ESALQ), Universidade de São Paulo (USP), Av. Pádua Dias, n° 11, Agronomia, CEP 13418-900, Piracicaba, SP, Brazil.
3Escola Superior de Agricultura Luiz de Queiroz (ESALQ), Universidade de São Paulo (USP), Av. Pádua Dias, n° 11, Agronomia, CEP 13418-900, Piracicaba, SP, Brazil.
4Embrapa Algodão, Rua Oswaldo Cruz, n° 1.143, Centenário, CEP 58428‑095, Campina Grande, PB, Brazil.
5Universidade Estadual da Paraíba, Programa de Pós-Graduação em Ciências Agrárias, Rua Baraunas, n° 351, Universitário, CEP 58429-570 Campina Grande, PB, Brazil.

2022 - Volume: 62 Issue: 2 pages: 426-430

https://doi.org/10.24349/lldq-iy5f

Short note

Keywords

Anthonomus grandis dust mite parasitism toxin

Abstract

We report the occurrence of Pyemotes tritici (LaGreze-Fossat & Montagne) (Acari: Pyemotidae) parasitizing the boll weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae), in shed squares of cotton grown in a greenhouse. Parasitized larvae, pupae and adults of the cotton boll weevil had abdominal sternites and/or tergites covered by whitish spherical physogastric females of P. tritici. This is the first record of the cotton boll weevil parasitized by this mite species.


Introduction

Mites of the family Pyemotidae are reported as ectoparasites of a large number of arthropods He et al., 2019; Sousa et al., 2020; Chen et al. 2021), mainly insects of the orders Lepidoptera (Cunha et al., 2006; Oliveira et al., 2007; He et al. 2012, 2014; Liu et al, 2020; Tian et al. 2020), Hemiptera (Han, 2016; Li et al. 2019; Yu et al. 2019), and Coleoptera (Cunha et al. 2006; Guo et al. 2009; Oliveira et al., 2010). Pyemotes spp., also known as ''straw itch mites'', are of particular interest in applied acarology, both for their behavior as insect parasites and for their medical importance (Tomczyk-Socha et al. 2017; He et al., 2019). Adult females of this mite attach themselves to the host to feed, undergoing physogastry, the expansion of the posterior portion of their body (opisthosoma) to facilitate offspring development (Cunha et al. 2006). According to Tomalski et al. (1988), approximately 200 to 350 sexually mature mites are produced per female. Males are the first to be born, as adults, immediately copulating with their adult sisters. The newborn females immediately seek new hosts, which once parasitized, become paralyzed by the release of toxins (Sousa et al., 2020). Neurotoxins from a single female are sufficient to paralyze an insect host up to 150,000 times the size of the mite (Mullen and Oconnor, 2019). Studies on the potential of Pyemotes zhonghuajia as a biological control agent for eggs, larvae and pupae of the fall armyworm Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) and the oriental armyworm Mythimna separata (Walker) (Lepidoptera: Noctuidae) demonstrated that a female is capable of killing more than 50% of first to third instar larvae of S. frugiperda and M. separata within 72 h under laboratory conditions (Liu et al., 2020; Tian et al., 2020).

Here, we report a case of a pyemotid species parasitizing the cotton boll weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae) in Brazil.

Material and methods

The initial study was conducted to evaluate the resistance of cotton lines against the boll weevil, A. grandis, using transgenic and non-transgenic isolines (BRS 372) of cotton plants maintained in 15 L pots in a greenhouse at 29 ± 1°C, 60 ± 10% relative humidity and a 12 h photophase at Embrapa Algodão (7°13′50″S and 35°52′52″W). The pots were filled with 75% soil and 25% Plantmax™ commercial substrate (60% pine bark, 15% vermiculite and 25% humus). Forty-five days after germination, 481 cotton squares with oviposition punctures caused by cotton boll weevils were shed. These were collected and taken to the laboratory, where each was placed in a screened cage (23 × 35 × 31 cm) to await the emergence of adult weevils. Observations were made daily, until emergence ceased. Squares for which emergence did not occur were then dissected to assess whether the cause of mortality was due to the toxic Bt protein incorporated into the transgenic cotton plants. The dissection of cotton squares was performed according to Ramalho et al. (1993).

Results and discussion

Emergence was not recorded from 154 (32%) cotton squares. In 42 of these (27%), the weevil was found to be parasitized by the mite Pyemotes tritici (LaGreze-Fossat & Montagne) (Acari: Pyemotidae); identification based on Cross et al. (1981). No differences were observed in the parasitism rates of boll weevils between transgenic and non-transgenic cotton plants. Among the parasitized insects, five (12%), 18 (43%) and 19 (45%) were in the larval, pupal (Figure 1A) and adult (Figure 1B) phases, respectively. The mites were found on the abdominal sternites and/or tergites of the host, visible as whitish spherical physogastric females (Figure 1 A, B).

Figure 1. The cotton boll weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae) parasitized by Pyemotes tritici (LaGreze-Fossat & Montagne) (Acari: Pyemotidae). A: Pupae and B: adult (B). Scale bar = 1mm.

In Brazil, P. ventricosus mites have been recorded on the pink bollworm Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) (Costa Lima, 1917). Pyemotid mites were also reported on the tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) (Cunha et al., 2006; Oliveira et al., 2007), the flour moth Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae), the corn weevil Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) (Cunha et al. 2006), as well as on Cathartus quadricollis (Guérin-Méneville) (Coleoptera: Silvanidae) and Callosobruchus maculatus (Fabricius) (Coleoptera: Curculionidae) (Oliveira et al., 2010). The first report of Pyemotes group ventricosus mites parasitizing cotton boll weevils was made by Herrera in northern Mexico (Cross and Chesnut, 1971), but the species was not identified. Therefore, this is the first report of the cotton boll weevil being parasitized by P. tritici. Because this mite species is free-living, being commonly found in dried, insect-infested plant products such as hay, straw, and grains (Sousa et al., 2020); we believe that they were introduced into the greenhouse through the substrate incorporated into the soil used for cotton cultivation. In Brazil, infestations by P. tritici of nests of stingless bees, Melipona subnitida, M. asilvae, Tetragonisca angustula and Frieseomelitta varia (Hymenoptera: Meliponina) and of laboratory reared Sitophilus zeamais (Coleoptera: Curculionidae), Alphitobius diaperinus (Coleoptera: Tenebrionidae), Lasioderma serricorne (Coleoptera: Anobiidae), Acanthoscelides obtectus (Coleoptera: Bruchidae), Rhyzopertha dominica (Coleoptera: Bostrichidae), Ephestia sp. (Lepidoptera: Pyralidae) and Tribolium castaneum (Coleoptera: Tenebrionidae) was previously reported (Kerr et al. 1996; Nogueira-Neto, 1997; Menezes et al. 2009; Sousa et al. 2020). P. tritici females have high reproductive potential, producing approximately 254 offspring per female (Bruce and Wrensch, 1990), potentially explaining their high incidence in populations of cotton boll weevils in the greenhouse.

Although P. tritici has characteristics relevant to biological control, such as a short life cycle, wide host range and rapid population growth (He et al., 2019), the direct use of mites of this group as a biological control agent for cotton boll weevils through their release into the environment is not recommended. Past attempts at field releases of P. ventricosus in cotton crops in Texas, USA were apparently disappointing (Pierce et al., 1912; Cross and Chesnut, 1971). In addition, and more importantly, this mite can have undesirable effects on humans, causing dermatitis (Cunha et al., 2006; Tomczyk-Socha et al., 2017). Due to these practical problems, past research turned toward the potential use of toxins synthesized by certain mite species of this genus. The TxP1 toxin, for example, produced by P. tritici, has been purified and characterized by Tomalski et al. (1988). The incorporation of this toxin improved success in the use of nuclear polyhedrosis virus against Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) and of Baculovirus species against Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) (Popham et al., 1997; Burden et al., 2000; Kroemer et al., 2015). Therefore, we believe that the best way to take advantage of the P. tritici mite in biological control programs for cotton boll weevils is through the incorporation of its toxins into bioinsecticides. Furthermore, these bioinsecticides have the potential to improve the effectiveness of current pest control programs and, in some cases, may exhibit synergism with existing integrated pest management (IPM) techniques (Wratten, 2009), without causing undesirable effects in humans. These P. tritici mite toxins can also be incorporated into the genome of entomopathogens and cultivated plants (Windley et al., 2012).

Acknowledgements

The authors acknowledge the Instituto Brasileiro do Algodão (IBA) for the financial support.



References

  1. Bruce, W.A., Wrensch, D.L. 1990. Reproductive Potential, Sex Ratio, and Mating Efficiency of the Straw Itch Mite (Acari: Pyemotidae). J. Econ. Entomol. 83: 384-391. https://doi.org/10.1093/jee/83.2.384
  2. Burden J.P., Hails R.S., Windass J.D., Suner M.M., Cory J.S. 2000. Infectivity, speed of kill & productivity of a baculovirus expressing the itch mite toxin txp-1 in second and fourth instar larvae of Trichoplusia ni. J. Invertebr. Pathol. 75: 226-236. https://doi.org/10.1006/jipa.1999.4921
  3. Chen Y.-C., Tian T.-A., Chen Y.-H., Yu L.-C., Hu J.-F., Yu X.-F., Liu J.-F., Yang M.-F. 2021. The biocontrol agent Pyemotes zhonghuajia has the highest lethal weight ratio compared with its prey and the most dramatic body weight change during pregnancy. Insects, 12: 490. https://doi.org/10.3390/insects12060490
  4. Costa Lima A.M. 1917. Relatório sobre a lagarta rósea do capulho nos algodoeiros do Nordeste. Rio de Janeiro: Imprensa Nacional. p. 35-44.
  5. Cross W.H., Chesnut T.L. 1971. Arthropod parasites of the boll weevil, Anthonomus grandis: 1. An annotated list. Ann. Entomol. Soc. Am., 64: 516-527. https://doi.org/10.1093/aesa/64.2.516
  6. Cross E.A., Moser J.C., Rack G. 1981. Some new forms of Pyemotes (Acarina: Pyemotidae) from forest insects, with remarks on polymorphism. Intern. J. Acar., 7: 179-196. https://doi.org/10.1080/01647958108683260
  7. Cunha U.S., Silva E.S., Moraes G.J., Vendramin J.D. 2006. Ocorrência do acaro Pyemotes sp. (Acari: Pyemotidae) em criações de insetos em laboratório. Neotrop. Entomol., 35: 563-565. https://doi.org/10.1590/S1519-566X2006000400023
  8. Guo X., Xu Z., Xiong D. 2009. Study of utilizing Pyemotes zhonghuajia to control Semanotus bifasciatus beetles. Chin. Agric. Sci. Bull., 26: 136-138.
  9. Han J. 2016. Study on controlling effect of Pyemotes sp. on several Hemiptera aphid. Shaanxi Forest. Sci. Technol., 45: 38-39.
  10. He L., Jiao R., Yu L., Xu C., Hao B. 2014. Preliminary report on parasitism of Yponomeuta sp. by Pyemotes zhonghuajia. Hebei Fruits, 6: 8-9. https://doi.org/10.3969/j.issn.1006-9402. 2014.06.005
  11. He L.M., Yan N.G., Yu L.C. 2012. Field study on biological control of Dioryctria sp. by augmentative release of Pyemotes zhonghuajia. Pract. Forest. Technol., 11: 73-75. https://doi.org/10.13456/j.cnki.lykt.2012.11.019
  12. He L., Li L., Yu L., He X.Z., Jiao R., Xu C., Zhang L., Liu J. 2019. Optimizing cold storage of the ectoparasitic mite Pyemotes zhonghuajia (Acari: Pyemotidae), an efficient biological control agent of stem borers. Exp. Appl. Acarol., 78: 327-342. https://doi.org/10.1007/s10493-019-00386-0
  13. Kerr, W.E., Carvalho, G.A., Nascimento, V.A. 1996. Abelha Uruçu, Biologia, Manejo e Conservação. Coleção Manejo da Vida Silvestre. Fundação Acangaú: Belo Horizonte.
  14. Kroemer, J.A., Bonning, B.C., Harrison, R.L. 2015. Expression, delivery and function of insecticidal proteins expressed by recombinant Baculoviruses. Viruses, 7: 422-455. https://doi.org/10.3390/v7010422
  15. Li L., He L., Yu L., He X.Z., Xu C., Jiao R., Zhang L., Liu J. 2019. Preliminary study on the potential of Pyemotes zhonghuajia (Acari: Pyemotidae) in biological control of Aphis citricola (Hemiptera: Aphididae). Syst. Appl. Acarol., 24: 1116-1120. https://doi.org/10.11158/saa.24.6.12
  16. Liu J.-F., Tian T.-A., Li X.-L., Chen Y.-C., Yu X.-F., Tan X.-F., Zhu Y., Yang M.-F. 2020. Is Pyemotes zhonghuajia (Acari: Pyemotidae) a suitable biological control agent against the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae)? Syst. Appl. Acarol., 25: 649-657. https://doi.org/10.11158/saa.25.4.5
  17. Menezes, C., Coletto-Silva, A., Gazeta, G.S., Kerr, W.E. 2009. Infestation by Pyemotes tritici (Acari, Pyemotidae) causes death of stingless bee colonies (Hymenoptera: Meliponina). Genet. Mol. Res. 8: 630-634. https://doi.org/10.4238/vol8-2kerr021
  18. Mullen, G.R., Oconnor, B.M., 2019. Mites (Acari). In: Mullen G.R., Duren L.A. (Eds). Medical and veterinary entomology. Cambridge: Academic Press. p. 533-602. https://doi.org/10.1016/B978-0-12-814043-7.00026-1
  19. Nogueira-Neto, P.N. 1997. Vida e criação de abelhas indígenas sem Ferrão. Nogueirapis: São Paulo.
  20. Oliveira C.R.F., Matos C.H.C., Hatano E. 2007. Occurrence of Pyemotes sp. on Tuta absoluta (Meyrick). Braz. Arch. Biol. Technol., 50: 929-932. https://doi.org/10.1590/S1516-89132007000700003
  21. Oliveira C.R.F., Sousa A.H., Pimentel M.A.G., Matos C.H.C., Faroni L.R.A. 2010. First record for Cathartus quadricollis and Callosobruchus maculatus cultures attacked by the mite Pyemotes tritici, Idesia, 28: 97-100. https://doi.org/10.4067/S0718-34292010000300012
  22. Pierce W.D., Cushman R.A., Hood C.E. 1912. The insect enemies of the cotton boll weevil. USDA Bur. Entomol. Bull. 100. 99p. https://doi.org/10.5962/bhl.title.64941
  23. Popham H.J.R., Yonghong L.I., Miller L.K., Li Y.H. 1997. Genetic improvement of Helicoverpa zea nuclear polyedrosis virus as a biopesticide. Biol. Control, 10: 83-91. https://doi.org/10.1006/bcon.1997.0552
  24. Ramalho F.S., Gonzaga J.V., Silva J.R.B. 1993. Método para determinação das causas de mortalidade natural do bicudo-do-algodoeiro. Pesq. Agropecu. Bras., 28: 877-887.
  25. Sousa, A.H., Mendonça, G.R.Q., Lopes, L.M., Faroni, L.R.D., 2020. Widespread infestation of Pyemotes tritici (Acari: Pyemotidae) in colonies of seven species of storedproduct insects. Genet. Mol. Res., 19: gmr18548. https://doi.org/10.4238/gmr18548
  26. Tian T.-A., Yu L., Sun G.-J., Yu X.-F., Li L., Wu C.-X., Chen Y.C., Yang M.-F., Liu J.-F. 2020. Biological control efficiency of an ectoparasitic mite Pyemotes zhonghuajia on oriental armyworm Mythimna separata. Syst. Appl. Acarol., 25: 1683-1692. https://doi.org/10.11158/saa.25.9.13
  27. Tomalski M.D., Bruce W.A., Travis J., Blum M.S. 1988. Preliminary characterization of toxins from the straw itch mite, Pyemotes tritici, which induce paralysis in the larvae of a moth. Toxicon, 26: 127-132. https://doi.org/10.1016/0041-0101(88)90164-X
  28. Tomczyk-Socha M., Jędrzejewska-Jurga K., Limburska J., Tomczyk J. 2017. Outbreak of occupational dermatitis associated with Pyemotes ventricosus. JAMA Dermatology 153: 686-688. https://doi.org/10.1001/jamadermatol.2017.0323
  29. Windley, M.J., Herzig V., Dziemborowicz S.A., Hardy M.C., King G.F., Nicholson G.M. 2012. Spider-venom peptides as bioinsecticides. Toxins, 4: 191-227. https://doi.org/10.3390/toxins
  30. Wratten, S.D. 2009. Conservation biological control and biopesticides in agriculture. In: Jorgensen S.E. (Ed). Applications in Ecological Engineering. Maryland Heights: Elsevier Academic Press. p. 130-134.
  31. Yu L.-C., He L.-M., Ouyang G.-C., Liang G.-W., Lu Y.-Y. 2019. Ectoparasitic mite, Pyemotes zhonghuajia (Prostigmata: Pyemotidae), for biological control of Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Liviidae). Syst. Appl. Acarol., 24: 520-524. https://doi.org/10.11158/saa.24.3.15


Comments
Please read and follow the instructions to post any comment or correction.

Article editorial history
Date received:
2021-06-09
Date accepted:
2022-04-11
Date published:
2022-04-14

Edited by:
McCoy, Karen

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License
2022 da Silva, Carlos A. D.; de Moraes, Gilberto J.; Castilho, Raphael C.; Ramalho, Francisco S. and Lima, Tardelly A.
Downloads
 Download article

Download the citation
RIS with abstract 
(Zotero, Endnote, Reference Manager, ProCite, RefWorks, Mendeley)
RIS without abstract 
BIB 
(Zotero, BibTeX)
TXT 
(PubMed, Txt)
Article metrics
Number of distinct pdf views
496

Dimensions

Cited by: view citations with

Search via ReFindit