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Can dehydrated sewage sludge, used as fertilizer, affect arthropods on Platycyamus regnellii (Fabaceae)?

Sewage sludge is a byproduct of sewage treatment, rich in N and P, which can be used as soil fertilizer in forest plantations and in degraded areas recovery (Mota et al., 2021MOTA, M.V.S., DEMOLIN-LEITE, G.L., GUANABENS, P.F.S., TEIXEIRA, G.L., SOARES, M.A., SILVA, J.L., SAMPAIO, R.A. and ZANUNCIO, J.C., 2021. Chewing insects, pollinators, and predators on Acacia auriculiformis A. Cunn. ex Beth (Fabales: Fabaceae) plants fertilized with dehydrated sewage sludge. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, p. e248305. http://dx.doi.org/10.1590/1519-6984.248305. PMid:34669795.
http://dx.doi.org/10.1590/1519-6984.2483...
). Platycyamus regnellii (Benth) (Fabales: Fabaceae) is a tree used in environmental recovery and its hardwood is used in home construction (Ferreira et al., 2015FERREIRA, M.C., COSTA, S.M.L. and PASIN, L.A.A., 2015. Uso de resíduos da agroindústria de banana na composição de substratos para produção de mudas de pau pereira. Nativa, vol. 3, no. 2, pp. 120-124. http://dx.doi.org/10.14583/2318-7670.v03n02a08.
http://dx.doi.org/10.14583/2318-7670.v03...
). Tree development and growth are essential to assess the recovery of an environment, because the structure, biomass, and diversity of vegetation are related to ecosystem functions and fauna colonization (Monteiro et al., 2019MONTEIRO, L.B., TOMBA, J.A.S., NISHIMURA, G., MONTEIRO, R.S., FOELKEL, E. and LAVIGNE, C., 2019. Faunistic analyses of fruit fly species (Diptera: Tephritidae) in orchards surrounded by Atlantic Forest fragments in the metropolitan region of Curitiba, Paraná state, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 79, no. 3, pp. 395-403. http://dx.doi.org/10.1590/1519-6984.178458. PMid:30231137.
http://dx.doi.org/10.1590/1519-6984.1784...
). The arthropod biodiversity is susceptible to environmental conditions and the presence of some functional groups is an indicator of the success of environmental recovery (Burgio et al., 2015BURGIO, G., SOMMAGGIO, D., MARINI, M., PUPPI, G., CHIARUCCI, A., LANDI, S., FABBRI, R., PERSARINI, F., GENGHINI, M., FERRARI, R., MUZZI, E., VAN LENTEREN, J.C. and MASETTI, A., 2015. The influence of vegetation and landscape structural connectivity on butterflies (Lepidoptera: Papilionoidea and Hesperiidae), carabids (Coleoptera: Carabidae), syrphids (Diptera: Syrphidae), and sawflies (Hymenoptera: Symphyta) in northern Italy farmland. Environmental Entomology, vol. 44, no. 5, pp. 1299-1307. http://dx.doi.org/10.1093/ee/nvv105. PMid:26314007.
http://dx.doi.org/10.1093/ee/nvv105...
). There is a lack of studies evaluating P. regnellii on recovery of degraded areas and the arthropod fauna feeding and/or living on this plant. The objective was to evaluate, for 24 months, the ecological indices of arthropods on P. regnellii saplings (young trees) in a degraded area using or not dehydrated sewage as a fertilizer.

The study was carried out in a degraded area on the campus of the “Universidade Federal de Minas Gerais” in Montes Claros, Minas Gerais, Brazil (latitude 16°51’ S, longitude 44°55’ W, altitude 943 m) from March 2018 to February 2020. The experimental design was completely randomized with two treatments (20 L of dehydrated sewage sludge per plant or without it), with 24 replications and one plant each. Information on climatic conditions, soil, characteristics of the dehydrated sewage sludge, seedling production, spacing between plants in the field, irrigation, and fertilization in this area are available (Gomes, 2018GOMES, J.B., 2018. Estratificação horizontal de insetos fitófagos, inimigos naturais e compostos químicos foliares em Platycyamus regnellii Benth. (Fabaceae) em área degradada. Diamantina: Universidade Federal dos Vales do Jequitinhonha e Mucuri, 50 p. Dissertação de mestrado.). The leaves per branch were measured monthly by visual observation on 48 P. regnellii saplings. Insect defoliation was evaluated visually by the leaf area losses on a 0–100% scale with 5% increments for removed leaf area (Mota et al., 2021MOTA, M.V.S., DEMOLIN-LEITE, G.L., GUANABENS, P.F.S., TEIXEIRA, G.L., SOARES, M.A., SILVA, J.L., SAMPAIO, R.A. and ZANUNCIO, J.C., 2021. Chewing insects, pollinators, and predators on Acacia auriculiformis A. Cunn. ex Beth (Fabales: Fabaceae) plants fertilized with dehydrated sewage sludge. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, p. e248305. http://dx.doi.org/10.1590/1519-6984.248305. PMid:34669795.
http://dx.doi.org/10.1590/1519-6984.2483...
). The sum of data (i.e. 12 leaves/sapling/survey) from a single sapling was used. Ecological indices (abundance, diversity, and species richness) were calculated per group of arthropods (i.e. coleopterans and spiders) and treatment (fertilization or not with dehydrated sewage sludge). Abundance and species richness were the total number of individuals and species, respectively, per sapling. The diversity was calculated using Hill´s formula per sapling. The abundance, diversity, and species richness of arthropods, and leaves per branch were submitted to the non-parametric statistical hypothesis Wilcoxon signed-rank test (P< 0.05).

Platycyamus regnellii saplings fertilized with dehydrated sewage sludge produced significantly (P< 0.05) more leaves/branch per sapling (7.56 ± 0.29) compared to unfertilized ones (5.58 ± 0.23). The defoliation, abundance and species richness of chewing insects, species richness of natural enemies, and number of Eumolpus sp. (Coleoptera: Chrysomelidae), Araneidae (Araneae), Oxyopes salticus Hentz (Araneae: Oxyopidae), and tending ants (Hymenoptera: Formicidae) were higher on P. regnellii saplings fertilized with dehydrated sewage (Table 1).

Table 1
Abundance, diversity, and species richness of arthropods (Indices), the number of individuals/species of herbivore, natural enemies, and pollinators per Platycyamus regnelli/sapling (mean ± SE) fertilized or not, with sewage sludge.

These results may be due to the greater biomass (leaves) as a result of fertilization, a food resource with high quality for these chewing insects, attracting their natural enemies (predator following prey). Insect herbivore populations may also have a positive association with N and P levels in the soil (Joern et al., 2012JOERN, A., PROVIN, T. and BEHMER, S.T., 2012. Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology, vol. 93, no. 5, pp. 1002-1015. http://dx.doi.org/10.1890/11-1142.1. PMid:22764487.
http://dx.doi.org/10.1890/11-1142.1...
). Differences in plant quality reflect the availability of soil nutrients which may affect plant morphology and quality (Chau and Heinz, 2006CHAU, A. and HEINZ, K.M., 2006. Manipulating fertilization: a management tactic against Frankliniella occidentalis on potted chrysanthemum. Entomologia Experimentalis et Applicata, vol. 120, no. 3, pp. 201-209. http://dx.doi.org/10.1111/j.1570-7458.2006.00441.x.
http://dx.doi.org/10.1111/j.1570-7458.20...
). This influences the preference of these insects (Sarfraz et al., 2009SARFRAZ, R.M., DOSDALL, L.M. and KEDDIE, A.B., 2009. Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. European Journal of Entomology, vol. 106, no. 4, pp. 583-594. http://dx.doi.org/10.14411/eje.2009.073.
http://dx.doi.org/10.14411/eje.2009.073...
), attracting a higher number of natural enemies, as on Acacia mangium (Fabaceae) trees fertilized with sewage sludge (Silva et al., 2020SILVA, J.L., LEITE, G.L.D., TAVARES, W.S., SILVA, F.W.S., SAMPAIO, R.A., AZEVEDO, A.M., SERRÃO, J.E. and ZANUNCIO, J.C., 2020. Diversity of arthropods on Acacia mangium (Fabaceae) and production of this plant with dehydrated sewage sludge in degraded area. Royal Society Open Science, vol. 7, no. 2, p. 191196. http://dx.doi.org/10.1098/rsos.191196. PMid:32257306.
http://dx.doi.org/10.1098/rsos.191196...
). Natural enemies (e.g., spiders) prey insects and thus are important, in natural and agricultural systems (Sunderland and Samu, 2000SUNDERLAND, K. and SAMU, F., 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomologia Experimentalis et Applicata, vol. 95, no. 1, pp. 1-13. http://dx.doi.org/10.1046/j.1570-7458.2000.00635.x.
http://dx.doi.org/10.1046/j.1570-7458.20...
), reducing pest numbers such as reported for Epiphyas postvittana Walker (Lepidoptera: Tortricidae) on Malus domestica (Borkh.) Borkh. (Rosales: Rosaceae) (Hogg et al., 2017HOGG, B.N., MILLS, N.J. and DAANE, K.M., 2017. Temporal patterns in the abundance and species composition of spiders on host plants of the invasive moth Epiphyas postvittana (Lepidoptera: tortricidae). Environmental Entomology, vol. 46, no. 3, pp. 502-510. http://dx.doi.org/10.1093/ee/nvx065. PMid:28379400.
http://dx.doi.org/10.1093/ee/nvx065...
). This fact may explain the low rate of herbivory (≈5%) observed in fertilized P. regnellii saplings. Spiders may reduce herbivory, even when they not prey, because herbivore insects avoid plants with a high density of predators, choosing other host plants (Bucher et al., 2015BUCHER, R., MENZEL, F. and ENTLING, M., 2015. Risk of spider predation alters food web structure and reduces local herbivory in the field. Oecologia, vol. 178, no. 2, pp. 571-577. http://dx.doi.org/10.1007/s00442-015-3226-5. PMid:25630957.
http://dx.doi.org/10.1007/s00442-015-322...
). The number of tending ants was higher on fertilized saplings, probably due to the greater number of spiders on these plants. Some ant species recruit workers on plants with clues left by spiders (e.g. silk webs), to protect herbivores from predation in exchange to some resource (e.g. honeydew) (Bucher et al., 2015BUCHER, R., MENZEL, F. and ENTLING, M., 2015. Risk of spider predation alters food web structure and reduces local herbivory in the field. Oecologia, vol. 178, no. 2, pp. 571-577. http://dx.doi.org/10.1007/s00442-015-3226-5. PMid:25630957.
http://dx.doi.org/10.1007/s00442-015-322...
). But plants can suppress herbivore populations through varying levels of nutrients. This can be central in natural systems (Wetzel et al., 2016WETZEL, W.C., KHAROUBA, H.M., ROBINSON, M., HOLYOAK, M. and KARBAN, R., 2016. Variability in plant nutrients reduces insect herbivore performance. Nature, vol. 539, no. 7629, pp. 425-427. http://dx.doi.org/10.1038/nature20140. PMid:27749815.
http://dx.doi.org/10.1038/nature20140...
). Thus, this increase in nutrient heterogeneity can be applied to agricultural crops and contribute to the sustainable control of insect pests in agroecosystems (Wetzel et al., 2016WETZEL, W.C., KHAROUBA, H.M., ROBINSON, M., HOLYOAK, M. and KARBAN, R., 2016. Variability in plant nutrients reduces insect herbivore performance. Nature, vol. 539, no. 7629, pp. 425-427. http://dx.doi.org/10.1038/nature20140. PMid:27749815.
http://dx.doi.org/10.1038/nature20140...
).

The fertilization with dehydrated sewage sludge increases ecological indices of insects, including natural enemies (e.g., spiders), on P. regnellii saplings, with a low rate of herbivory, and should be used in recovering plans of degraded areas.

References

  • BUCHER, R., MENZEL, F. and ENTLING, M., 2015. Risk of spider predation alters food web structure and reduces local herbivory in the field. Oecologia, vol. 178, no. 2, pp. 571-577. http://dx.doi.org/10.1007/s00442-015-3226-5 PMid:25630957.
    » http://dx.doi.org/10.1007/s00442-015-3226-5
  • BURGIO, G., SOMMAGGIO, D., MARINI, M., PUPPI, G., CHIARUCCI, A., LANDI, S., FABBRI, R., PERSARINI, F., GENGHINI, M., FERRARI, R., MUZZI, E., VAN LENTEREN, J.C. and MASETTI, A., 2015. The influence of vegetation and landscape structural connectivity on butterflies (Lepidoptera: Papilionoidea and Hesperiidae), carabids (Coleoptera: Carabidae), syrphids (Diptera: Syrphidae), and sawflies (Hymenoptera: Symphyta) in northern Italy farmland. Environmental Entomology, vol. 44, no. 5, pp. 1299-1307. http://dx.doi.org/10.1093/ee/nvv105 PMid:26314007.
    » http://dx.doi.org/10.1093/ee/nvv105
  • CHAU, A. and HEINZ, K.M., 2006. Manipulating fertilization: a management tactic against Frankliniella occidentalis on potted chrysanthemum. Entomologia Experimentalis et Applicata, vol. 120, no. 3, pp. 201-209. http://dx.doi.org/10.1111/j.1570-7458.2006.00441.x
    » http://dx.doi.org/10.1111/j.1570-7458.2006.00441.x
  • FERREIRA, M.C., COSTA, S.M.L. and PASIN, L.A.A., 2015. Uso de resíduos da agroindústria de banana na composição de substratos para produção de mudas de pau pereira. Nativa, vol. 3, no. 2, pp. 120-124. http://dx.doi.org/10.14583/2318-7670.v03n02a08
    » http://dx.doi.org/10.14583/2318-7670.v03n02a08
  • GOMES, J.B., 2018. Estratificação horizontal de insetos fitófagos, inimigos naturais e compostos químicos foliares em Platycyamus regnellii Benth. (Fabaceae) em área degradada Diamantina: Universidade Federal dos Vales do Jequitinhonha e Mucuri, 50 p. Dissertação de mestrado.
  • HOGG, B.N., MILLS, N.J. and DAANE, K.M., 2017. Temporal patterns in the abundance and species composition of spiders on host plants of the invasive moth Epiphyas postvittana (Lepidoptera: tortricidae). Environmental Entomology, vol. 46, no. 3, pp. 502-510. http://dx.doi.org/10.1093/ee/nvx065 PMid:28379400.
    » http://dx.doi.org/10.1093/ee/nvx065
  • JOERN, A., PROVIN, T. and BEHMER, S.T., 2012. Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology, vol. 93, no. 5, pp. 1002-1015. http://dx.doi.org/10.1890/11-1142.1 PMid:22764487.
    » http://dx.doi.org/10.1890/11-1142.1
  • MONTEIRO, L.B., TOMBA, J.A.S., NISHIMURA, G., MONTEIRO, R.S., FOELKEL, E. and LAVIGNE, C., 2019. Faunistic analyses of fruit fly species (Diptera: Tephritidae) in orchards surrounded by Atlantic Forest fragments in the metropolitan region of Curitiba, Paraná state, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 79, no. 3, pp. 395-403. http://dx.doi.org/10.1590/1519-6984.178458 PMid:30231137.
    » http://dx.doi.org/10.1590/1519-6984.178458
  • MOTA, M.V.S., DEMOLIN-LEITE, G.L., GUANABENS, P.F.S., TEIXEIRA, G.L., SOARES, M.A., SILVA, J.L., SAMPAIO, R.A. and ZANUNCIO, J.C., 2021. Chewing insects, pollinators, and predators on Acacia auriculiformis A. Cunn. ex Beth (Fabales: Fabaceae) plants fertilized with dehydrated sewage sludge. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, p. e248305. http://dx.doi.org/10.1590/1519-6984.248305 PMid:34669795.
    » http://dx.doi.org/10.1590/1519-6984.248305
  • SARFRAZ, R.M., DOSDALL, L.M. and KEDDIE, A.B., 2009. Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. European Journal of Entomology, vol. 106, no. 4, pp. 583-594. http://dx.doi.org/10.14411/eje.2009.073
    » http://dx.doi.org/10.14411/eje.2009.073
  • SILVA, J.L., LEITE, G.L.D., TAVARES, W.S., SILVA, F.W.S., SAMPAIO, R.A., AZEVEDO, A.M., SERRÃO, J.E. and ZANUNCIO, J.C., 2020. Diversity of arthropods on Acacia mangium (Fabaceae) and production of this plant with dehydrated sewage sludge in degraded area. Royal Society Open Science, vol. 7, no. 2, p. 191196. http://dx.doi.org/10.1098/rsos.191196 PMid:32257306.
    » http://dx.doi.org/10.1098/rsos.191196
  • SUNDERLAND, K. and SAMU, F., 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomologia Experimentalis et Applicata, vol. 95, no. 1, pp. 1-13. http://dx.doi.org/10.1046/j.1570-7458.2000.00635.x
    » http://dx.doi.org/10.1046/j.1570-7458.2000.00635.x
  • WETZEL, W.C., KHAROUBA, H.M., ROBINSON, M., HOLYOAK, M. and KARBAN, R., 2016. Variability in plant nutrients reduces insect herbivore performance. Nature, vol. 539, no. 7629, pp. 425-427. http://dx.doi.org/10.1038/nature20140 PMid:27749815.
    » http://dx.doi.org/10.1038/nature20140

Publication Dates

  • Publication in this collection
    10 June 2022
  • Date of issue
    2024

History

  • Received
    12 Aug 2021
  • Accepted
    23 May 2022
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