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Reproduction in the spider mite Oligonychus yothersi (Acari: Tetranychidae)

Abstract

In this work we reported injuries caused by the spider mite Oligonychus yothersi on Vitis vinifera leaves and we also investigate the sex ratio of this species under laboratory conditions. To access the aspects regarding reproduction, females were placed individually in arenas made of V. vinifera leaves to oviposit and all progeny were mounted on slides when they reached adulthood to confirm the offspring sex. Our study showed that O. yothersi reproduces by thelytokous /arrhenotokous parthenogenesis, generating low number of males. Additionally, we found vine plants with leaf browning, particularly on the adaxial surface, where mites were usually found.

Key words
Grapevine; parthenogenesis; sex rate; sexual behavior; Vitis vinifera

Brazil is one of the largest grapevines producing countries, and Rio Grande do Sul state accounts for up to 90% of the national production of wines and grape juice and approximately 85% of sparkling wine (Mello & Machado 2020MELLO LMR & MACHADO CAE. 2020. Vitivinicultura brasileira: panorama 2019. Comunicado Técnico 199: 1-7.). European grapes (Vitis vinifera L.) are the most commonly cultivated worldwide. The phytophagous mite families of economic importance in this crop are Tetranychidae, Eriophyidae, Tarsonemidae and Tenuipalpidae (Schruft 1985SCHRUFT GA. 1985. Grape. In: Spider mites: Their biology, natural enemies and control. In Helle W & Sabelis MW (Eds), Spider mites, Their biology, Amsterdan: Elsevier, p. 359-366., Duso & de Lillo 1996DUSO C & DE LILLO DCM. 1996. Grape. In: Lindquist EE, Sabelis MW & Bruin J (Eds), Eriophyoid mites. Amsterdan: Elsevier, p. 571-582.).

Tetranychidae, a mite family of high economic importance, is subdivided into two subfamilies: Bryobriinae and Tetranychinae (Baker & Tuttle 1994BAKER EW & TUTTLE DMA. 1994. Guide to the spider mites (Tetranychidae) of the United States. Michigan: Indira Publishing House, 347 p., Migeon et al. 2020MIGEON A & DORKELD F. 2020. Spider Mites Web: a comprehensive database for the Tetranychidae. [Accessed Oct. 18, 2020]. Available at: http://www.montpellier.inra.fr/CBGP/spmweb.
http://www.montpellier.inra.fr/CBGP/spmw...
). Many tetranychid species have a parthenogenetic reproduction, where unfertilized females produce eggs capable of development (Mittwoch 1978MITTWOCH U. 1978. Parthenogenesis. J Med Genet 15: 165., Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.). Male-producing parthenogenesis (arrhenotoky) is most frequently found, but there are also records of female-producing parthenogenesis (thelytoky) (Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.). The Bryobriinae are unique in showing similar distribution of arrhenotoky and thelytoky in the species where this has been examined (Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.). Arrhenotoky has the most frequent occurrence in the subfamily Tetranychinae (Heinrich 1972HEINRICH WO. 1972. Verificação de telitoquia na sub-família Tetranychinae Berlese, 1913. Biologico 370., Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.). However, the genus Oligonychus is peculiar with most of the species studied being arrhenotokous (Heinrich 1972HEINRICH WO. 1972. Verificação de telitoquia na sub-família Tetranychinae Berlese, 1913. Biologico 370., Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.). In particular, O. ilicis (McGregor) and O. mangiferus Rah. & Punj. exhibit thelytoky/arrhenotoky, while Oligonychus thelytokus Gutierrez is the only species of the genus to exhibit thelytoky exclusively (Gutierrez 1977GUTIERREZ J. 1977. A polyphagous spider mite species of the intertropical zone: Oligonychus thelytokus n. sp. Description and preliminary biological information. Cahiers ORSTOM. Serie Biologie 12: 65-72., Heinrich 1972HEINRICH WO. 1972. Verificação de telitoquia na sub-família Tetranychinae Berlese, 1913. Biologico 370., Helle & Pijnacker 1985HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.).

Oligonychus yothersi (McGregor) (Tetranychidae) has already been registered in Brazil in several crops such as avocado, yerba mate, coffee, mango, grapes and ornamental plants (Flechtmann & Moraes 2017FLECHTMANN CHW & MORAES RCB. 2017. Tetranychidae Database. [Accessed Feb. 10, 2023]. Available at: http://www.lea.esalq.usp.br/tetranychidae.
http://www.lea.esalq.usp.br/tetranychida...
). Only arrhenotokous parthenogenesis has been observed for this species (Alves et al. 2004ALVES LFA, SPONGOSKI S, VIEIRA FDS & MOREAS GD. 2004. Biologia e danos de Oligonychus yothersi (McGregor) (Acari: Tetranychidae) em Ilex paraguariensis. Arquivos do Instituto Biológico 71: 211-214.). Thus, a better understanding of the biology and life cycle of this mite species would facilitate management practices and favor the establishment of a sustainable pest mite control.

We recorded O. yothersi in a backyard vineyard, “BRS Vitória” variety (V. vinifera), planted in 2015 and managed without pesticides and fertilizers, in Arroio do Meio County, Rio Grande do Sul state, Brazil (29.402604066190467°S, 51.94319997583439°W). We found plants with symptoms caused by O. yothersi: leaf browning, particularly on the adaxial surface, where mites were usually found, but were also found on the abaxial surface when population densities were high (Figure 1).

Figure 1
Leaf symptoms caused by Oligonychus yothersi on Vitis vinifera. a - Adaxial surface. b - Abaxial surface. c - On vineyard.

Oligonychus yothersi (Figure 2) is characterized by: female with empodium clawlike (Figure 3a) and two pairs of duplex setae distal and approximate on tarsus I (Figure 3b). Longitudinal pregenital striae and 2 pairs of para-anal and anal setae (Figure 3c). Males are similar to females, with aedeagus bent portion slightly fattened then abruptly tapered to the tip (Figure 3d) (Baker & Tuttle 1994BAKER EW & TUTTLE DMA. 1994. Guide to the spider mites (Tetranychidae) of the United States. Michigan: Indira Publishing House, 347 p.).

Figure 2
Stereomicroscope. Oligonychus yothersi. a - Adult females. b - Egg. c - Immature stage.
Figure 3
Phase contrast microscope. Female of O. yothersi. a - Empodium of leg I. b - Duplex setae on the tarsus of leg I. c - Anogenital region. d - Male aedeagus.

We observed that males were rare on the field, thus we assessed the sex ratio in a laboratory experiment. To do so, 36 females were placed individually in arenas to oviposit. The arenas were made of V. vinifera leaves, placed on a moistened sponge with the adaxial surface upwards, and their borders were protected with cotton wool. Distilled water was added on a daily basis to the sponge in order to keep the leaves hydrated and to the cotton wool to prevent mites from escaping. The experiment was conducted at 25±1°C, 80±5% relative humidity and 12 hours of photoperiod in the laboratory. After laying one egg each, the females were removed. All of the eggs were observed once a day until adulthood. After reaching the adult stage, all females oviposited throughout adulthood until death. The offspring were counted and placed in new arenas until they reached adulthood, when all of them were mounted on slides to confirm the sex. All slides were examined using a phase contrast microscope (Axio Scope. A1 – Zeiss) and they were identified with a proper dichotomous key (Baker & Tuttle 1994BAKER EW & TUTTLE DMA. 1994. Guide to the spider mites (Tetranychidae) of the United States. Michigan: Indira Publishing House, 347 p.). Sex ratio was calculated as follows: Number of females/(number of females + number of males).

There was a total of 522 offspring, which the sex ratio was 99.4% females (n= 519) and 0.6% males (n= 3). Our study showed that unfertilized O. yothersi female, under laboratory conditions reproduces by thelytokous /arrhenotokous parthenogenesis, generating low number of males. It is important to emphasize the difference in the previous study where arrhenotoky was observed by Alves et al. (2004)ALVES LFA, SPONGOSKI S, VIEIRA FDS & MOREAS GD. 2004. Biologia e danos de Oligonychus yothersi (McGregor) (Acari: Tetranychidae) em Ilex paraguariensis. Arquivos do Instituto Biológico 71: 211-214.. Studies involving sex chromosomes should be done to confirm which form of parthenogenesis occurs in O. yothersi and if it may be variable. Aspects regarding the impact of the environment on reproduction merits attention especially aiming for proper biological control practices.

ACKNOWLEDGMENTS

The authors are grateful to Professor Carlos H. W. Flechtmann, for revising the manuscript, providing scientific literature and for taxonomical help. This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq, 312784/2021-0), and Universidade do Vale do Taquari – Univates.

REFERENCES

  • ALVES LFA, SPONGOSKI S, VIEIRA FDS & MOREAS GD. 2004. Biologia e danos de Oligonychus yothersi (McGregor) (Acari: Tetranychidae) em Ilex paraguariensis. Arquivos do Instituto Biológico 71: 211-214.
  • BAKER EW & TUTTLE DMA. 1994. Guide to the spider mites (Tetranychidae) of the United States. Michigan: Indira Publishing House, 347 p.
  • DUSO C & DE LILLO DCM. 1996. Grape. In: Lindquist EE, Sabelis MW & Bruin J (Eds), Eriophyoid mites. Amsterdan: Elsevier, p. 571-582.
  • FLECHTMANN CHW & MORAES RCB. 2017. Tetranychidae Database. [Accessed Feb. 10, 2023]. Available at: http://www.lea.esalq.usp.br/tetranychidae
    » http://www.lea.esalq.usp.br/tetranychidae
  • GUTIERREZ J. 1977. A polyphagous spider mite species of the intertropical zone: Oligonychus thelytokus n. sp. Description and preliminary biological information. Cahiers ORSTOM. Serie Biologie 12: 65-72.
  • HEINRICH WO. 1972. Verificação de telitoquia na sub-família Tetranychinae Berlese, 1913. Biologico 370.
  • HELLE W & PIJNACKER LP. 1985. Parthenogenesis, chromosomes and sex ratio. In HELLE W & SABELIS MW. Spider mites, Their biology, Amsterdan: Elsevier, p. 129-139.
  • MELLO LMR & MACHADO CAE. 2020. Vitivinicultura brasileira: panorama 2019. Comunicado Técnico 199: 1-7.
  • MIGEON A & DORKELD F. 2020. Spider Mites Web: a comprehensive database for the Tetranychidae. [Accessed Oct. 18, 2020]. Available at: http://www.montpellier.inra.fr/CBGP/spmweb
    » http://www.montpellier.inra.fr/CBGP/spmweb
  • MITTWOCH U. 1978. Parthenogenesis. J Med Genet 15: 165.
  • SCHRUFT GA. 1985. Grape. In: Spider mites: Their biology, natural enemies and control. In Helle W & Sabelis MW (Eds), Spider mites, Their biology, Amsterdan: Elsevier, p. 359-366.

Publication Dates

  • Publication in this collection
    09 Sept 2024
  • Date of issue
    2024

History

  • Received
    27 June 2023
  • Accepted
    07 Apr 2024
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