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First report the Syntermes molestus Burm. (1839) (Isoptera: Termitidae) causing severe mechanical damage to Solanum tuberosum roots

Termites belong to the order Isoptera with approximately 2.800 species worldwide (Chouvenc et al., 2021CHOUVENC, T., ŠOBOTNÍK, J., ENGEL, M.S. and BOURGUIGNON, T., 2021. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cellular and Molecular Life Sciences, vol. 78, no. 6, pp. 2749-2769. http://dx.doi.org/10.1007/s00018-020-03728-z. PMid:33388854.
http://dx.doi.org/10.1007/s00018-020-037...
). Lower termites (Families Mastotermitidae, Kalotermitidae, Termopsidae, Hodotermitidae, Rhinotermitidae and Serritermitidae) have specific diets restricted to woody tissues, while higher termites (family Termitidae) have diverse feeding habits, which include woody tissues, grass, fungi, lichen, bedding, manure, humus and soil (Vikram et al., 2021VIKRAM, S., ARNEODO, J.D., CALCAGNO, J., ORTIZ, M., MON, M.L., ETCHEVERRY, C., COWAN, D.A. and TALIA, P., 2021. Diversity structure of the microbial communities in the guts of four neotropical termite species. PeerJ, vol. 9, p. e10959. http://dx.doi.org/10.7717/peerj.10959. PMid:33868801.
http://dx.doi.org/10.7717/peerj.10959...
). Kalotermitidae, Serritermitidae, Rhinotermitidae and Termitidae are termite families that occur in Neotropical regions and in Brazil (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the isoptera of the world. Bulletin of the American Museum of Natural History, vol. 2013, no. 377, pp. 200-624.). Kalotermitidae live only in dry wood without contact with the ground (Miyaguni et al., 2021MIYAGUNI, Y., AGARIE, A., SUGIO, K., TSUJI, K. and KOBAYASHI, K., 2021. Caste development and sex ratio of the Ryukyu dry wood termite Neotermes sugioi and its potential mechanisms. Scientific Reports, vol. 11, no. 1, pp. 1-8. PMid:33414495.). Serritermitidae family comprises two subterranean species (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the isoptera of the world. Bulletin of the American Museum of Natural History, vol. 2013, no. 377, pp. 200-624.). Rhinotermitidae are subterranean and xylophagous (Lima and Costa-Leonardo, 2014LIMA, J.T. and COSTA-LEONARDO, A.M., 2014. Foraging in subterranean termites (Isoptera: Rhinotermitidae): How do Heterotermes tenuis and Coptotermes gestroi behave when they locate equivalent food resources? Bulletin of Entomological Research, vol. 104, no. 4, pp. 525-533. http://dx.doi.org/10.1017/S0007485314000297. PMid:24783950.
http://dx.doi.org/10.1017/S0007485314000...
). Termitidae family corresponds to more than 80% of the termite species that occur in Brazil (Azevedo et al., 2019AZEVEDO, R.A.D., DAMBROS, C.D.S. and MORAIS, J.W.D., 2019. A new termite species of the genus Dihoplotermes Araújo (Blattaria, Isoptera, Termitidae) from the Brazilian Amazonian rainforest. Acta Amazonica, vol. 49, no. 1, pp. 17-23. http://dx.doi.org/10.1590/1809-4392201800582.
http://dx.doi.org/10.1590/1809-439220180...
). Termitidae have varied habits and are divided into four subfamilies, three of which occur in Brazil: Apicotermitinae (soldier termites), Nasutermitinae (nasuto termites) and Termitinae (Scheffrahn et al., 2005SCHEFFRAHN, R.H., KRECEK, J., SZALANSKI, A.L. and AUSTIN, J.W., 2005. Synonymy of neotropical arboreal termites Nasutitermes corniger and N. costalis (Isoptera: Termitidae: Nasutitermitinae), with evidence from morphology, genetics, and biogeography. Annals of the Entomological Society of America, vol. 98, no. 3, pp. 273-281. http://dx.doi.org/10.1603/0013-8746(2005)098[0273:SONATN]2.0.CO;2.
http://dx.doi.org/10.1603/0013-8746(2005...
; Brune, 2014BRUNE, A., 2014. Symbiotic digestion of lignocellulose in termite guts. Nature Reviews. Microbiology, vol. 12, no. 3, pp. 168-180. http://dx.doi.org/10.1038/nrmicro3182. PMid:24487819.
http://dx.doi.org/10.1038/nrmicro3182...
; Sousa et al., 2017SOUSA, G., SANTOS, V.C., GONTIJO, N.F., CONSTANTINO, R., SILVA, G.O.P., BAHIA, A.C., GOMES, F.M. and MACHADO, E.A., 2017. Morphophysiological study of digestive system litter-feeding termite Cornitermes cumulans (Kollar, 1832). Cell and Tissue Research, vol. 368, no. 3, pp. 579-590. http://dx.doi.org/10.1007/s00441-017-2584-1. PMid:28285353.
http://dx.doi.org/10.1007/s00441-017-258...
). Despite the great termites diversity, only 10% of the species are considered pests. Termitidae cause damage both in urban areas and in agrosilvopastoral activity, attacking, in adulthood, pineapple, cotton, rice, live eucalyptus (planted forests and seedlings) and aged corn stalks in Brazil. Termite control is difficult and is carried out with insecticides applied in the planting furrow or through seed treatment and usually only reduce the infestation.

Despite the losses and the difficult Termitidae control, their enigmatic existence in tropical regions makes it difficult to know how they choose their food sources (Costa-Leonardo, 2008COSTA-LEONARDO, A.M., 2008. Dinâmica do forrageamento em cupins subterrâneos. In: E.F. VILELA, I.A. SANTOS, J.H. SCHOEREDER, J.E. SERRÃO, L.A.O. CAMPOS and J. LINO-NETO, eds. Insetos sociais: da biologia à aplicação. Viçosa: EditoraUFV, pp. 347-358., 2022COSTA-LEONARDO, A.M., 2022. Cupins-praga: morfologia, biologia e controle. 1. ed. Rio Claro: Universidade Estadual Paulista, 128 p.). In theory, in ideal foraging, animals choose their food according to their nutritional needs (Emlen, 1973EMLEN, J.M., 1973. Ecology: an evolutionary approach. 1st ed. California: Addison-Wesley Publishing Company, 493 p.) to optimize their fitness (Krebs, 1978KREBS, J.R. 1978. Optimal foraging decision rules for predators. In: KREBS, J.R. and DAVIES N.B., eds. Behavioral ecology: an evolutionary approach. Oxford: Blackwell, pp. 23-63.). The termites foraging behavior is a collective activity composed of integrated and dynamic individual actions over time, guided by the food quality and quantity (Grace and Campora, 2005GRACE, J.K. and CAMPORA, C.E. 2005. Food location and discrimination by subterranean termites (Isoptera: Rhinotermitidae). In: C.Y. LEE and W.H. ROBINSON, eds. Proceedings of the 5th International Conference on Urban Pests. Malaysia: Perniagaan Ph'ng P&Y Design Network, pp. 437-441.). In Termitidae, food choice is basically occasional and chronological - the first foods found (Delaplane and La Fage, 1987DELAPLANE, K.S. and LA FAGE, J.P., 1987. Variance in feeding on equivalent wood blocks by the Formosan subterranean termite in laboratory choice tests. Sociobiology, vol. 13, no. 3, pp. 227-233.). However, this factor is a paradigm of the nutritional subterranean termites ecology because it has never been contested (Lima and Costa-Leonardo, 2014LIMA, J.T. and COSTA-LEONARDO, A.M., 2014. Foraging in subterranean termites (Isoptera: Rhinotermitidae): How do Heterotermes tenuis and Coptotermes gestroi behave when they locate equivalent food resources? Bulletin of Entomological Research, vol. 104, no. 4, pp. 525-533. http://dx.doi.org/10.1017/S0007485314000297. PMid:24783950.
http://dx.doi.org/10.1017/S0007485314000...
), generating uncertainty about whether termites move randomly or exhibit food fidelity (Thorne and Long, 2006THORNE, B.L. and LONG, C.E., 2006. Resource fidelity, brood distribution and foraging dynamics in complete laboratory colonies of Reticulitermes flavipes (Isoptera Rhinotermitidae). Etologia Ecologia & Evolução, vol. 18, no. 2, pp. 113-125. ).

The objective was to register the occurrence of S. molestus causing severe mechanical damage to the S. tuberosum cv. Ágata roots in an anthropized area with a agropastoral exploitation history.

On July 14, 2021, tubers of S. tuberosum attacked by termites were manually harvested in the experimental field of the Departamento de Engenharia Agrícola of the Universidade Federal de Viçosa (UFV). Experimental area was flanked by three active termite mounds measuring ± 40 and 25 cm in diameter and height, respectively, and ± 40, 10 and 3 m away from the cultivation area (Figures 1a, 1b and 1d). The insects were identified as S. molestus by Professor PhD. Wellington Souto Ribeiro from UFV (Figure 1). S. molestus is an adult pest of pineapple, cotton, rice, eucalyptus (planted forests and seedlings) and corn in Brazil, however, it had never been described as a pest or causing damage to S. tuberosum roots. This insect has a recurrent occurrence in the area with predominant activity between July and October. The attack to the roots occurred, for two consecutive cycles, causing deep lesions.

Figure 1
Aerial image from Google Earth (a) showing the positioning of termite mounds in the experimental area. Perspective of the termite mounds in relation to the experimental area (b). Active termite mound (d) and detail of an adult termite (Syntermes molestus Burm.) (c) found in tuber cavities and galleries of S. tuberosum L.

Approximately 20% of the tubers collected had biogenic perforations of 3.09 to 20.17 mm with a clear activity of 2.0 ± 0.2 adult termites (Figure 2). The insects left, with normal mobility, the cavities and biogenic galleries in the tubers. The biogenic cavities and galleries had the same pattern and size as those found in the termite mound (2.21 to 24.18 mm). The attacked tubers were on the edge of the cultivated area and with greening caused by inadequate hilling.

Figure 2
Tubercles of S. tuberosum L. evidencing the biogenic cavities and galleries resulting from the activity of Syntermes molestus Burm. (a, b, c, d); similar in shape and size to those observed in the termite mound (e, f).

Although termites are not considered primary potato pests, the knowledge behind the infestations lacks in-depth investigations into the range and concrete numbers. This information may be related to climate change or anthropization, which for the vast majority of agricultural areas is routine. Farmers need to know, with proportionate urgency, whether unusual insect infestations reflect abnormal contexts.

Termites are considered pests of several vegetables, however, the potato had never been mentioned literally. This fact may be related to a literature lack. Although we reported the termites attack on potato roots at this harvest time, employees and students had already observed, in greater and lesser intensity, the termites attack on potato roots. Thus, constant and more detailed observation can generate more information about the attack dynamics and the post-harvest losses magnitude.

Acknowledgements

We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES - financial code 001) and the Universidade Federal de Viçosa for the financing and technical support for this research.

References

  • AZEVEDO, R.A.D., DAMBROS, C.D.S. and MORAIS, J.W.D., 2019. A new termite species of the genus Dihoplotermes Araújo (Blattaria, Isoptera, Termitidae) from the Brazilian Amazonian rainforest. Acta Amazonica, vol. 49, no. 1, pp. 17-23. http://dx.doi.org/10.1590/1809-4392201800582
    » http://dx.doi.org/10.1590/1809-4392201800582
  • BRUNE, A., 2014. Symbiotic digestion of lignocellulose in termite guts. Nature Reviews. Microbiology, vol. 12, no. 3, pp. 168-180. http://dx.doi.org/10.1038/nrmicro3182 PMid:24487819.
    » http://dx.doi.org/10.1038/nrmicro3182
  • CHOUVENC, T., ŠOBOTNÍK, J., ENGEL, M.S. and BOURGUIGNON, T., 2021. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cellular and Molecular Life Sciences, vol. 78, no. 6, pp. 2749-2769. http://dx.doi.org/10.1007/s00018-020-03728-z PMid:33388854.
    » http://dx.doi.org/10.1007/s00018-020-03728-z
  • COSTA-LEONARDO, A.M., 2008. Dinâmica do forrageamento em cupins subterrâneos. In: E.F. VILELA, I.A. SANTOS, J.H. SCHOEREDER, J.E. SERRÃO, L.A.O. CAMPOS and J. LINO-NETO, eds. Insetos sociais: da biologia à aplicação Viçosa: EditoraUFV, pp. 347-358.
  • COSTA-LEONARDO, A.M., 2022. Cupins-praga: morfologia, biologia e controle 1. ed. Rio Claro: Universidade Estadual Paulista, 128 p.
  • DELAPLANE, K.S. and LA FAGE, J.P., 1987. Variance in feeding on equivalent wood blocks by the Formosan subterranean termite in laboratory choice tests. Sociobiology, vol. 13, no. 3, pp. 227-233.
  • EMLEN, J.M., 1973. Ecology: an evolutionary approach 1st ed. California: Addison-Wesley Publishing Company, 493 p.
  • GRACE, J.K. and CAMPORA, C.E. 2005. Food location and discrimination by subterranean termites (Isoptera: Rhinotermitidae). In: C.Y. LEE and W.H. ROBINSON, eds. Proceedings of the 5th International Conference on Urban Pests. Malaysia: Perniagaan Ph'ng P&Y Design Network, pp. 437-441.
  • KREBS, J.R. 1978. Optimal foraging decision rules for predators. In: KREBS, J.R. and DAVIES N.B., eds. Behavioral ecology: an evolutionary approach. Oxford: Blackwell, pp. 23-63.
  • KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the isoptera of the world. Bulletin of the American Museum of Natural History, vol. 2013, no. 377, pp. 200-624.
  • LIMA, J.T. and COSTA-LEONARDO, A.M., 2014. Foraging in subterranean termites (Isoptera: Rhinotermitidae): How do Heterotermes tenuis and Coptotermes gestroi behave when they locate equivalent food resources? Bulletin of Entomological Research, vol. 104, no. 4, pp. 525-533. http://dx.doi.org/10.1017/S0007485314000297 PMid:24783950.
    » http://dx.doi.org/10.1017/S0007485314000297
  • MIYAGUNI, Y., AGARIE, A., SUGIO, K., TSUJI, K. and KOBAYASHI, K., 2021. Caste development and sex ratio of the Ryukyu dry wood termite Neotermes sugioi and its potential mechanisms. Scientific Reports, vol. 11, no. 1, pp. 1-8. PMid:33414495.
  • SCHEFFRAHN, R.H., KRECEK, J., SZALANSKI, A.L. and AUSTIN, J.W., 2005. Synonymy of neotropical arboreal termites Nasutitermes corniger and N. costalis (Isoptera: Termitidae: Nasutitermitinae), with evidence from morphology, genetics, and biogeography. Annals of the Entomological Society of America, vol. 98, no. 3, pp. 273-281. http://dx.doi.org/10.1603/0013-8746(2005)098[0273:SONATN]2.0.CO;2
    » http://dx.doi.org/10.1603/0013-8746(2005)098[0273:SONATN]2.0.CO;2
  • SOUSA, G., SANTOS, V.C., GONTIJO, N.F., CONSTANTINO, R., SILVA, G.O.P., BAHIA, A.C., GOMES, F.M. and MACHADO, E.A., 2017. Morphophysiological study of digestive system litter-feeding termite Cornitermes cumulans (Kollar, 1832). Cell and Tissue Research, vol. 368, no. 3, pp. 579-590. http://dx.doi.org/10.1007/s00441-017-2584-1 PMid:28285353.
    » http://dx.doi.org/10.1007/s00441-017-2584-1
  • THORNE, B.L. and LONG, C.E., 2006. Resource fidelity, brood distribution and foraging dynamics in complete laboratory colonies of Reticulitermes flavipes (Isoptera Rhinotermitidae). Etologia Ecologia & Evolução, vol. 18, no. 2, pp. 113-125.
  • VIKRAM, S., ARNEODO, J.D., CALCAGNO, J., ORTIZ, M., MON, M.L., ETCHEVERRY, C., COWAN, D.A. and TALIA, P., 2021. Diversity structure of the microbial communities in the guts of four neotropical termite species. PeerJ, vol. 9, p. e10959. http://dx.doi.org/10.7717/peerj.10959 PMid:33868801.
    » http://dx.doi.org/10.7717/peerj.10959

Publication Dates

  • Publication in this collection
    20 Mar 2023
  • Date of issue
    2023

History

  • Received
    06 Nov 2022
  • Accepted
    16 Feb 2023
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
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