Abstract
Scolytinae species that, in high populations, can damage reducing wood production in forest crops. These beetles are monitored with traps baited with ethanol and increasing their efficiency can improve the integrated management of these insects. The objective was to evaluate the increase in the capture efficiency of Scolytinae with a semi-funnel trap model, in two experiments, one including wooden elements and other increasing the flight interception area and to correlate the numbers of these beetles collected with climatic factors. In the experiment 1, Eucalyptus urophylla S. T. Blake slats were directly attached to the collector flask and in another treatment, in addition to these slats, Cedrela sp. strips were inserted inside the bait holding hose. In the experiment 2, the insect interception area in the trap, originally 480 cm2, was expanded to 1,200 cm2 and compared with the model Pet–Santa Maria trap with an interception area of 550 cm2. Weekly collections were carried out between May 2018 and June 2019. The beetles collected were taken to the Wood Biodeterioration Laboratory of the Federal Rural University of Rio de Janeiro (UFRRJ) where they were sorted, identified at family level, counted and their number correlated with climatic factors. Statistical analyzes of the collected data were processed by the BioStat® 5.3 program. In the experiment 1 were collected 869 Scolytinae. The numbers of beetles collected per trap without modification, with E. urophylla slats and E. urophylla slats + Cedrela sp. strips were similar, 7.3 ± 3.8, 7.8 ± 6.2 and 7.7 ± 5.0 respectively. In the experiment 2 were collected 4,398 Scolytinae. Increasing the interception area of the beetles increased the efficiency of the semi-funnel trap, with 42.7 ± 20.5 Scolytinae collected compared to the original semi-funnel trap, 28.6 ± 12.6 and the Pet–Santa Maria, 20.4 ± 10.4, per trap. The number of Scolytinae did not correlate with climatic factors in the experiment 1 and it was correlated with temperature, relative humidity and wind speed, but not with precipitation, in the 2. The incorporation of E. urophylla slats or Cedrela sp. strips in the semi-funnel trap did not increase the number of beetles collected, but, the increase in the flight interception area and the temperature, relative humidity and wind speed were correlated with the number of beetles collected.
Keywords:
climatic factors; ethanol baited traps; interception area; population monitoring
Resumo
Espécies de besouros Scolytinae, em altas populações, podem danificar a madeira e reduzir a produtividade de cultivos florestais. Esses besouros são monitorados com armadilhas iscadas com etanol e o aumento da eficiência das mesmas pode melhorar o manejo integrado desses insetos. O objetivo foi avaliar o aumento da eficiência de captura de Scolytinae com armadilha modelo semifunil, em dois experimentos, um incluindo elementos de madeira e outro aumentando a área de interceptação de voo e correlacionar o número desses besouros coletados com fatores climáticos. No experimento 1, ripas de Eucalyptus urophylla S. T. Blake foram fixadas, diretamente, no frasco coletor e em outro tratamento, além dessas ripas, fitas de Cedrela sp. foram inseridas no interior da mangueira porta isca. No experimento 2, a área de interceptação de insetos na armadilha, originalmente, com 480 cm2, foi ampliada para 1200 cm2 e comparada com a armadilha modelo Pet–Santa Maria com área de interceptação de 550 cm2. Coletas semanais foram realizadas entre maio de 2018 a junho de 2019. Os insetos capturados foram levados ao Laboratório de Biodeterioração da Madeira da Universidade Federal Rural do Rio de Janeiro (UFRRJ) onde foram triados, identificados em nível de família, contados e a abundância correlacionada com fatores climáticos. As análises estatísticas dos dados coletados foram processadas pelo programa BioStat® 5.3. No experimento 1 foram coletados 869 Scolytinae. Os números de besouros coletados por armadilha sem modificação, com ripas de E. urophylla e com ripas de E. urophylla + fita de Cedrela sp. foram semelhantes, 7,3 ± 3,8; 7,8 ± 6,2 e 7,7 ± 5,0 respectivamente. No experimento 2 foram coletados 4398 Scolytinae. O aumento da área de interceptação dos besouros aumentou a eficiência da armadilha semifunil, com 42,7 ± 20,5 Scolytinae coletados por armadilha comparado a semifunil original, 28,6 ± 12,6 e a Pet–Santa Maria, 20,4 ± 10,4. O número de Scolytinae não se correlacionou com os fatores climáticos no experimento 1 e se correlacionou com a temperatura, umidade relativa e velocidade do vento, mas não com a precipitação, no 2. A incorporação de ripas de E. urophylla ou fitas de Cedrela sp. na armadilha semifunil não aumentou o número de besouros coletados, mas, o aumento da área de intercepção de voo e a temperatura, umidade relativa do ar e velocidade do vento se correlacionaram com o número de besouros coletados.
Palavras-chave:
área de interceptação; armadilhas iscadas com etanol; fatores climáticos; monitoramento populacional
1. Introduction
Scolytinae species, in high populations, are pests and can damage trees reducing wood production and increasing fire risks (Li and Li, 2019LI, H. and LI, T., 2019. Bark beetle larval dynamics carved in the egg gallery: a study of mathematically reconstructing bark beetle tunnel maps. Advances in Difference Equations, vol. 2019, no. 1, pp. 513.). Besides, Scolytinae can be vectors of phytopathogenic fungi (Chakraborty et al., 2020CHAKRABORTY, A., MODLINGER, R., ASHRAF, M.Z., SYNEK, J., SCHLYTER, F. and ROY, A., 2020. Core mycobiome and their ecological relevance in the gut of five Ips bark beetles (Coleoptera: Curculionidae: Scolytinae). Frontiers in Microbiology, vol. 11, pp. 568853. http://dx.doi.org/10.3389/fmicb.2020.568853. PMid:33013799.
http://dx.doi.org/10.3389/fmicb.2020.568...
; Contarini et al., 2020CONTARINI, M., VANNINI, A., GIARRUZZO, F., FACCOLI, M., MORALES–RODRIGUEZ, C., ROSSINI, L. and SPERANZA, S., 2020. First record of Xylosandrus germanus (Blandford) (Coleoptera: Curculionidae, Scolytinae) in the Mediterranean scrubland in Southern Italy, and its co‐presence with the co‐generic species X. compactus (Eichhoff) and X. crassiusculus (Motschulsky). Bulletin OEPP. EPPO Bulletin. European and Mediterranean Plant Protection Organisation, vol. 50, no. 2, pp. 311-315. http://dx.doi.org/10.1111/epp.12660.
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) causing tree death and some species can transmit viruses (Oliveira et al., 2021OLIVEIRA, A.G., SILVA, M.H.M. and GARLET, J., 2021. Coleoborers in Bambusa sp. in the Southern Amazon. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e237813. http://dx.doi.org/10.1590/1519-6984.237813. PMid:34161451.
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). These beetles identify suitable host plants for colonization by detecting semiochemicals released by those physiologically stressed (Özcan et al., 2018ÖZCAN, G.E., ENEZ, K. and ARICAK, B., 2018. Effects of forest roads on Ips sexdentatus infestation in black pine forest. Turkish Journal of Agriculture–Food Science and Technology, vol. 6, no. 7, pp. 828-833. http://dx.doi.org/10.24925/turjaf.v6i7.828-833.1690.
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; Zhao et al., 2020ZHAO, M., LIU, B., SUN, Y., WANG, Y., DAI, L. and CHEN, H., 2020. Presence and roles of myrtenol, myrtanol and myrtenal in Dendroctonus armandi (Coleoptera: Curculionidae: Scolytinae) and Pinus armandi (Pinales: Pinaceae: Pinoideae). Pest Management Science, vol. 76, no. 1, pp. 188-197. http://dx.doi.org/10.1002/ps.5492. PMid:31106502.
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) or recently dead or dying (Aflitto et al., 2015AFLITTO, N., DEGOMEZ, T., HOFSTETTER, R., ANHOLD, J., MCMILLIN, J., WAGNER, M. and SCHNEIDER, E., 2015. Pine bark beetle and dwarf mistletoe infestation in a remnant old–growth stand. Western North American Naturalist, vol. 75, no. 3, pp. 281-290. http://dx.doi.org/10.3398/064.075.0305.
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).
Monitoring of Scolytinae with pheromone-baited traps (Galko et al., 2016GALKO, J., NIKOLOV, C., KUNCA, A., VAKULA, J., GUBKA, A., ZÚBRIK, M., RELL, S. and KONÔPKA, B., 2016. Effectiveness of pheromone traps for the European spruce bark beetle: a comparative study of four commercial products and two new models. Central European Forestry Journal, vol. 62, no. 4, pp. 207-215. http://dx.doi.org/10.1515/forj-2016-0027.
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) or ethanol (Oliveira et al., 2017OLIVEIRA, C.M., SILVA, C.N., FRIZZAS, M.R. and DIANESE, A.C., 2017. Measuring population fluctuation of jatropha stem–borer [Cophes notaticeps (Marshall)] in the Brazilian Cerrado using a new trap. Bulletin of Entomological Research, vol. 107, no. 5, pp. 627-633. http://dx.doi.org/10.1017/S0007485317000116. PMid:28185606.
http://dx.doi.org/10.1017/S0007485317000...
; Skrzecz et al., 2019SKRZECZ, I., WOLSKI, R., SOWINSKA, A., RACZKO, J., JANISZEWSKI, W. and KUZMINSKI, R., 2019. Evaluation of attractants and traps for monitoring small banded pine weevil Pissodes castaneus. Journal of Applied Entomology, vol. 143, no. 4, pp. 397-407. http://dx.doi.org/10.1111/jen.12610.
http://dx.doi.org/10.1111/jen.12610...
) determines population density to assist in the integrated management of these forest pests (Carvalho and Trevisan, 2015CARVALHO, A.G.D. and TREVISAN, H., 2015. Novo modelo de armadilha para captura de Scolytinae e Platypodinae (Insecta, Coleoptera). Floresta e Ambiente, vol. 22, no. 4, pp. 575-578. http://dx.doi.org/10.1590/2179-8087.105114.
http://dx.doi.org/10.1590/2179-8087.1051...
; Borkowski, 2017BORKOWSKI, A., 2017. The colonisation of Scots pine (Pinus sylvestris L.) by Tomicus minor Hartig in southern Poland: modelling and monitoring. European Journal of Forest Research, vol. 136, no. 5-6, pp. 893-906. http://dx.doi.org/10.1007/s10342-017-1078-8.
http://dx.doi.org/10.1007/s10342-017-107...
). The fermentation of extractives from newly cut wood forms this compound (Lemos et al., 2020LEMOS, D.A., SONEGO, J.L., CRUZ, A.J. and BADINO, A.C., 2020. Improvement of ethanol production by extractive fed–batch fermentation in a drop column bioreactor. Bioprocess and Biosystems Engineering, vol. 43, no. 12, pp. 2295-2303. http://dx.doi.org/10.1007/s00449-020-02414-5. PMid:32743720.
http://dx.doi.org/10.1007/s00449-020-024...
; González–Peñas et al., 2020GONZÁLEZ–PEÑAS, H., LU–CHAU, T.A., EIBES, G. and LEMA, J.M., 2020. Energy requirements and economics of acetone–butanol–ethanol (ABE) extractive fermentation: a solvent–based comparative assessment. Bioprocess and Biosystems Engineering, vol. 43, no. 12, pp. 2269-2281. http://dx.doi.org/10.1007/s00449-020-02412-7. PMid:32725441.
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) indicating plants suitable for colonization by Scolytinae and, therefore, used in traps to attract these beetles (Klingeman et al., 2017KLINGEMAN, W.E., BRAY, A.M., OLIVER, J.B., RANGER, C.M. and PALMQUIST, D.E., 2017. Trap style, bait, and height deployments in black walnut tree canopies help inform monitoring strategies for bark and ambrosia beetles (Coleoptera: Curculionidae: Scolytinae). Environmental Entomology, vol. 46, no. 5, pp. 1120-1129. http://dx.doi.org/10.1093/ee/nvx133. PMid:28961948.
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).
The cost of traps, such as the Lindgren funnel or the reed panel, is high (Steininger et al., 2015STEININGER, M.S., HULCR, J., ŠIGUT, M. and LUCKY, A., 2015. Simple and efficient trap for bark and ambrosia beetles (Coleoptera: Curculionidae) to facilitate invasive species monitoring and citizen involvement. Journal of Economic Entomology, vol. 108, no. 3, pp. 1115-1123. http://dx.doi.org/10.1093/jee/tov014. PMid:26470236.
http://dx.doi.org/10.1093/jee/tov014...
), making it necessary to develop simpler, cheaper and efficient models, such as those made with recycled materials (Murari et al., 2012MURARI, A.B., COSTA, E.C., BOSCARDIN, J. and GARLET, J., 2012. Modelo de armadilha etanólica de interceptação de voo para captura de escolitíneos (Curculionidae: scolytinae). Pesquisa Florestal Brasileira, vol. 32, no. 69, pp. 115-117. http://dx.doi.org/10.4336/2012.pfb.32.69.115.
http://dx.doi.org/10.4336/2012.pfb.32.69...
; Steininger et al., 2015STEININGER, M.S., HULCR, J., ŠIGUT, M. and LUCKY, A., 2015. Simple and efficient trap for bark and ambrosia beetles (Coleoptera: Curculionidae) to facilitate invasive species monitoring and citizen involvement. Journal of Economic Entomology, vol. 108, no. 3, pp. 1115-1123. http://dx.doi.org/10.1093/jee/tov014. PMid:26470236.
http://dx.doi.org/10.1093/jee/tov014...
; Carvalho and Trevisan, 2015CARVALHO, A.G.D. and TREVISAN, H., 2015. Novo modelo de armadilha para captura de Scolytinae e Platypodinae (Insecta, Coleoptera). Floresta e Ambiente, vol. 22, no. 4, pp. 575-578. http://dx.doi.org/10.1590/2179-8087.105114.
http://dx.doi.org/10.1590/2179-8087.1051...
). Strategies to improving and managing traps in the field can increase the efficiency of capturing wood borers (Trevisan et al., 2021TREVISAN, H., SOUZA, T.S. and AMANCIO, J.M.S., 2021. Influence of the color of semi–funnel traps on xylophagous Coleoptera capture efficiency in forest fragments. Bioscience Journal, vol. 37, pp. e37034.).
The objective was to evaluate the capture efficiency of Scolytinae using a semi-funnel trap model, including the incorporation of Eucalyptus urophylla S. T. Blake slats and Cedrela sp strips and the increase the insect interception area and to correlate the number of these beetles collected with climatic factors.
2. Material and Methods
2.1. Experimental area
The experiments were carried out in a secondary forest fragment of the Atlantic Forest with an area of 3.5 ha in the campus of the Federal Rural University of Rio de Janeiro (UFRRJ) in Seropédica, Rio de Janeiro, Brazil (22°44’38”S, 43°42’27”W, 26 m). The region climate is Aw, according to Köppen's classification, with annual rainfall of 1,213 mm concentrated from November to March and average annual temperature of 23.9 ºC (Silva et al., 2016SILVA, C.S.D., PEREIRA, M.G., DELGADO, R.C. and SILVA, E.V.D., 2016. Spatialization of soil chemical and physical attributes in an agroforestry system, Seropédica, Brazil. Cerne, vol. 22, no. 4, pp. 407-414. http://dx.doi.org/10.1590/01047760201622042159.
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).
2.2. Sampling
The Scolytinae were collected with six semi-funnel model traps, suspended randomly in the area at approximately 1.30 m high and 20 m apart from each other. These traps were made with polyethylene bottles (PET) of two liters and 500 g bottles (collector pot) baited with 96% ethanol and a 5 mm diameter hose, where 96% ethanol was placed with the aid of a 20 mL syringe (Carvalho and Trevisan, 2015CARVALHO, A.G.D. and TREVISAN, H., 2015. Novo modelo de armadilha para captura de Scolytinae e Platypodinae (Insecta, Coleoptera). Floresta e Ambiente, vol. 22, no. 4, pp. 575-578. http://dx.doi.org/10.1590/2179-8087.105114.
http://dx.doi.org/10.1590/2179-8087.1051...
).
Two experiments were conducted. One using E. urophylla slats and Cedrela sp. strips were placed in the semi-funnel trap to increase the ethanol volatilization (experiment 1) and in the other, the insect flight intercept area was increased with the incorporation of an extra panel in the trap (experiment 2). The number of traps adopted was based on the methodology proposed by Trevisan et al. (2021)TREVISAN, H., SOUZA, T.S. and AMANCIO, J.M.S., 2021. Influence of the color of semi–funnel traps on xylophagous Coleoptera capture efficiency in forest fragments. Bioscience Journal, vol. 37, pp. e37034..
In the experiment 1, two traps were used per treatment, being: 1) unmodified semi-funnel trap (control) (Carvalho and Trevisan, 2015CARVALHO, A.G.D. and TREVISAN, H., 2015. Novo modelo de armadilha para captura de Scolytinae e Platypodinae (Insecta, Coleoptera). Floresta e Ambiente, vol. 22, no. 4, pp. 575-578. http://dx.doi.org/10.1590/2179-8087.105114.
http://dx.doi.org/10.1590/2179-8087.1051...
); 2) semi-funnel trap with two E. urophylla slats (30 cm long × 10 cm wide × 2.5 cm thick) in the collector pot; and 3) traps with two E. urophylla slats and one Cedrela sp. strip (50 cm long × 3 cm wide x 0.5 mm thick) inside the ethanol hose. The incorporation of wooden elements in the traps aims to increase the volatilization of alcohol in the environment, as this material is hygroscopic and, theoretically, would work as a diffuser of this volatile (Figure 1).
Original semi-funnel model trap (A) in front view with protective plate (a), “semi-funnel” interceptor panel (b), collecting funnel (c), storage bottle (d), fixing wire (e) and bait holding hose (f); (A) with Eucalyptus urophylla slats (B) and Eucalyptus urophylla slats and Cedrela sp. strip (C). Pd= Plastic dish to protect the collecting pot from rainwater; Ho= Hose to adding ethanol; Cp= Collecting pot baited with ethanol; Eu= Eucalyptus urophylla slat and Cs= Cedrela sp. strip.
In the experiment 2, two traps were used per treatment, and the conditions in the were: 1) unmodified semi-funnel trap (480 cm2 of interception area); 2) semi-funnel trap with an extra panel (1,200 cm2 of total interception area); and 3) model Pet–Santa Maria trap (550 cm2 of interception area) (Murari et al., 2012MURARI, A.B., COSTA, E.C., BOSCARDIN, J. and GARLET, J., 2012. Modelo de armadilha etanólica de interceptação de voo para captura de escolitíneos (Curculionidae: scolytinae). Pesquisa Florestal Brasileira, vol. 32, no. 69, pp. 115-117. http://dx.doi.org/10.4336/2012.pfb.32.69.115.
http://dx.doi.org/10.4336/2012.pfb.32.69...
). The inclusion of an extra panel in the semi-funnel trap increased the insect interception area and the Pet-Santa Maria, flat trap, served for comparison because its interception area is intermediary in relation to the others (Figure 2).
Modified semi-funnel model, in front view (A); and Pet–Santa Maria trap, in side view (B) (Source: Murari et al., 2012MURARI, A.B., COSTA, E.C., BOSCARDIN, J. and GARLET, J., 2012. Modelo de armadilha etanólica de interceptação de voo para captura de escolitíneos (Curculionidae: scolytinae). Pesquisa Florestal Brasileira, vol. 32, no. 69, pp. 115-117. http://dx.doi.org/10.4336/2012.pfb.32.69.115.
http://dx.doi.org/10.4336/2012.pfb.32.69... ).
2.3. Collections
The insects were collected weekly from May to September 2018 (experiment 1 with 19 collections) and from December 2018 to June 2019 (experiment 2 with 28 collections), when the ethanol from the collector pots and the hose was replenished. The insects collected were taken to the Wood Biodeterioration Laboratory of the Forestry Products Department of the Forests Institute/UFRRJ and screened and counted.
The averages of temperature, precipitation, relative humidity and wind speed were obtained from the Meteorological Station of the National Institute of Meteorology (Agricultural Ecology) located in the Ecology district in Seropédica, Rio de Janeiro, Brazil (22º45'28”S; 43º41' 05”W, 35 m) (INMET, 2019INSTITUTO NACIONAL DE METEREOLOGIA – INMET, 2019 [viewed 01 may 2019]. Estação Meteorológica de Observação de Superfície Automática [online]. Ministério da Agricultura, Pecuária e Abastecimento. Available from: https://portal.inmet.gov.br/.
https://portal.inmet.gov.br/...
).
2.4. Statistical analysis
Data were processed with the BioStat® 5.3 program (Ayres et al., 2007AYRES, M., AYRES JÚNIOR, M., AYRES, D.L. and SANTOS, A.D.A.S. 2007. BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém: Sociedade Civil Mamirauá, Tefé. 364 p.) and their normality assessed by the Lilliefors method (p < 0.05). The total numbers of Scolytinae collected were given by the absolute frequency of these individuals in relation to the total number of other insect group captured in the traps. The numbers of Scolytinae were submitted to the Kruskal–Wallis test (p < 0.05) and the mean numbers analyzed by the Dunn test (p < 0.05). These numbers and climatic factors were analyzed by Pearson correlation. This correlation was interpreted by criteria considering the correlation expressed by R values between 0.10 and 0.29 as low; average between 0.30 and 0.49; and high between 0.50 and 1.0 (Cohen, 1977COHEN, J., 1977. Statistical power analysis for the behavioral sciences. 2nd ed. New York: Academic Press, 567 p.).
3. Results
-
Experiment 1: Semi-funnel model trap with wooden elements
A total of 869 Scolytinae beetles were collected in all traps, with similar values between the traps with E. urophylla slat (Eu), E. urophylla slat and Cedrela sp. strip, and in the control (Table 1).
Total number (absolute frequency – Af), average ± standard deviation and range of variation (maximum and minimum) of Scolytinae data captured in ethanol traps without (control) and with Eucalyptus urophylla slat (Eu) and E. urophylla slat and Cedrela sp. strip (Eu + Cs) in a secondary forest fragment of the Atlantic Forest, Seropédica, Rio de Janeiro, Brazil.
-
Experiment 2: Extension of the trap insect interception area
A total of 4,398 Scolytinae beetles were collected in the traps. The number of individuals of this subfamily captured was higher with the modified semi-funnel (1200 cm2), followed by the original semi-funnel (480 cm2) and the Pet–Santa Maria (550 cm2) traps (Table 2).
Total number (absolute frequency – Fa), average ± standard deviation and data variation range (maximum and minimum) of Scolytinae captured in the semi-funnel, modified semi-funnel and Pet–Santa Maria traps in a secondary forest fragment of Atlantic Forest, Seropédica, Rio de Janeiro Brazil.
3.1. Influence of climate factors
The number of Scolytinae captured was higher in January 2019 (324 beetles), the month with the highest temperature and lowest precipitation. The variation in the average temperature, relative humidity and wind speed was low, but precipitation during the collection period varied (Figure 3).
Number of Scolytinae collected and average temperature (ºC) (A), precipitation (mm) (B), relative humidity (%) (C) and wind speed (m/s) (D) in a secondary forest fragment from Atlantic Forest, Seropédica, Rio de Janeiro, Brazil from May 2018 to June 2019.
The number of individuals of Scolytinae did not correlate with the climatic factors temperature, relative humidity, wind speed and precipitation in the experiment 1, but it correlated with temperature, relative humidity and wind speed, but not with precipitation in the 2 (Table 3).
Pearson correlation coefficients between the number of Scolytinae collected in experiment 1 (ethanol traps with or without Eucalyptus urophylla slat and Cedrela spp. strip) and 2 (semi-funnel, modified semi-funnel and Pet–Santa Maria ethanol traps) and climatic factors (temperature, precipitation, relative humidity and wind speed) in secondary forest fragments of the Atlantic Forest and four climatic variables. Seropédica, Rio de Janeiro, Brazil.
4. Discussion
-
Experiment 1: Semi-funnel model trap with wooden elements
The similar number of individuals of Scolytinae between treatments with the semi-funnel traps indicates that the wooden slats or strips did not increase alcohol volatilization. This could be due to the material used being dry and with humidity in balance with the environment and, therefore, without extractive fermentation, differing from the green material (Yang and Liu, 2020YANG, L. and LIU, H., 2020. Effect of Supercritical CO2 Drying on moisture transfer and wood property of Eucalyptus urophylla. Forests, vol. 11, no. 10, pp. 1115. http://dx.doi.org/10.3390/f11101115.
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) and without the absorption and greater release of alcohol. On the other hand, compounds from green wood ferment after the tree harvest (Routa et al., 2020ROUTA, J., BRÄNNSTRÖM, H. and LAITILA, J., 2020. Effects of storage on dry matter, energy content and amount of extractives in Norway spruce bark. Biomass and Bioenergy, vol. 143, pp. 105821. http://dx.doi.org/10.1016/j.biombioe.2020.105821.
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), attracting Scolytinae due to alcohol production (Lemos et al., 2020LEMOS, D.A., SONEGO, J.L., CRUZ, A.J. and BADINO, A.C., 2020. Improvement of ethanol production by extractive fed–batch fermentation in a drop column bioreactor. Bioprocess and Biosystems Engineering, vol. 43, no. 12, pp. 2295-2303. http://dx.doi.org/10.1007/s00449-020-02414-5. PMid:32743720.
http://dx.doi.org/10.1007/s00449-020-024...
). These beetles are attracted to different alcohol types, including methanol and ethanol, 95% ethyl alcohol, P.A. isopropyl alcohol and methyl alcohol (Matos et al., 2019MATOS, J.P.S., SANTOS, A.C.M., CASTRO, M.V., COSTA, N.C.R., ALVES, L.C. and CUNHA, W.V., 2019. Volatilização de álcoois em armadilha para captura de Hypothenemus hampei. Revista do COMEIA, vol. 1, no. 1, pp. 34-40.). Furthermore, the color of the traps affect the collection of Scolytinae, as the number of individuals of the coffee borer, Hypothenemus hampei Ferrari, 1867 (Coleoptera: Curculionidae: Scolytinae) was higher in traps made with a red PET bottle baited with a mixture of ethanol and methanol (1:1 ratio) + benzoic acid than in those with a combination of other volatile mixtures with parts of ethanol, methanol, benzaldehyde and benzoic acid painted in colors green and red + green (Souza et al., 2020SOUZA, R.A.D., PRATISSOLI, D., ARAUJO JUNIOR, L.M.D., PINHEIRO, J.D.A., SOUZA, J.F.V., MADALON, F.Z., DEOLINDO, F.D. and DAMASCENA, A.P., 2020. Hypothenemus hampei Ferrari (Coleoptera: Curculionidae) answer to visual and olfative stimuli in field. Coffee Science, vol. 15, pp. e151656.). Hypothenemus hampei is firstly attracted by the secondary metabolites produced by coffee during the fruit formation and then by the color and shape of this fruit (Leiva-Espinoza et al., 2019LEIVA-ESPINOZA, S., OLIVA-CRUZ, M., RUBIO-ROJAS, K., MAICELO-QUINTANA, J. and MILLA-PINO, M., 2019. Uso de trampas de colores y atrayentes alcohólicos para la captura de la broca del café (Hypothenemus hampei) en plantaciones de café altamente infestadas. Revista Colombiana de Entomologia, vol. 45, no. 2, pp. e8537. http://dx.doi.org/10.25100/socolen.v45i2.8537.
http://dx.doi.org/10.25100/socolen.v45i2...
). Therefore, the red color of the traps is more attractive as it resembles that of the coffee fruit stage in development (Souza et al., 2020SOUZA, R.A.D., PRATISSOLI, D., ARAUJO JUNIOR, L.M.D., PINHEIRO, J.D.A., SOUZA, J.F.V., MADALON, F.Z., DEOLINDO, F.D. and DAMASCENA, A.P., 2020. Hypothenemus hampei Ferrari (Coleoptera: Curculionidae) answer to visual and olfative stimuli in field. Coffee Science, vol. 15, pp. e151656.).
The number of individuals of Scolytinae was similar to that obtained in Eucalyptus camaldulensis Dehnh plantations in Cuiabá, Mato Grosso state, Brazil (Rocha et al., 2011aROCHA, J.R.M., DORVAL, A., SOUZA, M.D.D. and COSTA, R.B.D., 2011a. Análise da ocorrência de coleópteros em plantios de Eucalyptus camaldulensis Dehn. em Cuiabá, MT. Floresta e Ambiente, vol. 18, no. 4, pp. 343-352. http://dx.doi.org/10.4322/floram.2011.054.
http://dx.doi.org/10.4322/floram.2011.05...
). The high number of individuals of Scolytinae captured in traps is due to their attraction to ethanol (Klingeman et al., 2017KLINGEMAN, W.E., BRAY, A.M., OLIVER, J.B., RANGER, C.M. and PALMQUIST, D.E., 2017. Trap style, bait, and height deployments in black walnut tree canopies help inform monitoring strategies for bark and ambrosia beetles (Coleoptera: Curculionidae: Scolytinae). Environmental Entomology, vol. 46, no. 5, pp. 1120-1129. http://dx.doi.org/10.1093/ee/nvx133. PMid:28961948.
http://dx.doi.org/10.1093/ee/nvx133...
; Byers et al., 2020BYERS, J.A., MAOZ, Y., FEFER, D. and LEVI–ZADA, A., 2020. Semiochemicals affecting attraction of Ambrosia Beetle Euwallacea fornicatus (Coleoptera: Curculionidae: Scolytinae) to quercivorol: developing push–pull control. Journal of Economic Entomology, vol. 113, no. 5, pp. 2120-2127. http://dx.doi.org/10.1093/jee/toaa127. PMid:32596735.
http://dx.doi.org/10.1093/jee/toaa127...
). The efficiency of collecting Scolytinae with ethanol (Kamata et al., 2020KAMATA, N., SANGUANSUB, S., BEAVER, R.A., SAITO, T. and HIRAO, T., 2020. Investigating the factors influencing trap capture of bark and ambrosia beetles using long–term trapping data in a cool temperate forest in central Japan. Journal of Forest Research, vol. 25, no. 3, pp. 163-173. http://dx.doi.org/10.1080/13416979.2020.1762288.
http://dx.doi.org/10.1080/13416979.2020....
), a compound released during the fermentation of extractives in stressed or newly harvested trees, is due to the use of this compound by these insects to locate suitable trees for colonization (González-Peñas et al., 2020GONZÁLEZ–PEÑAS, H., LU–CHAU, T.A., EIBES, G. and LEMA, J.M., 2020. Energy requirements and economics of acetone–butanol–ethanol (ABE) extractive fermentation: a solvent–based comparative assessment. Bioprocess and Biosystems Engineering, vol. 43, no. 12, pp. 2269-2281. http://dx.doi.org/10.1007/s00449-020-02412-7. PMid:32725441.
http://dx.doi.org/10.1007/s00449-020-024...
; Soares Gusmão et al., 2020SOARES GUSMÃO, R., PERES FILHO, O., DORVAL, A., SOUZA, M.D.D. and NASCIMENTO, D.A.D., 2020. Uso de trampas de etanol con y sin cebo para subfamilia Scolytinae (Coleoptera: Curculionidae) en bosques de eucalipto en la Región de Cerrado. Idesia, vol. 38, no. 1, pp. 99-104.; Zhao et al., 2020ZHAO, M., LIU, B., SUN, Y., WANG, Y., DAI, L. and CHEN, H., 2020. Presence and roles of myrtenol, myrtanol and myrtenal in Dendroctonus armandi (Coleoptera: Curculionidae: Scolytinae) and Pinus armandi (Pinales: Pinaceae: Pinoideae). Pest Management Science, vol. 76, no. 1, pp. 188-197. http://dx.doi.org/10.1002/ps.5492. PMid:31106502.
http://dx.doi.org/10.1002/ps.5492...
).
-
Experiment 2: Extension of the trap insect interception area
The greatest number of Scolytinae individuals, collected with the semi-funnel trap (1,200 cm2), agrees with report of greater efficiency of window (4,284 cm2) and cross-barrier (5,500 cm2) traps than those with multiple funnels (3,863 cm2) with smaller interception areas (Chen et al., 2010CHEN, G., ZHANG, Q.H., WANG, Y., LIU, G.T., ZHOU, X., NIU, J. and SCHLYTER, F., 2010. Catching Ips duplicatus (Sahlberg) (Coleoptera: Scolytidae) with pheromone‐baited traps: optimal trap type, colour, height and distance to infestation. Pest Management Science, vol. 66, no. 2, pp. 213-219. http://dx.doi.org/10.1002/ps.1867. PMid:19862793.
http://dx.doi.org/10.1002/ps.1867...
). The lowest number of Scolytinae captured with the Pet–Santa Maria trap, the second with the largest interception area (550 cm2), differs from the theory of greater efficiency of flat traps to capture these insects than cross or cylindrical traps, due to the higher ratio between the effective interception area and the trap surface (Safranyik et al., 2004SAFRANYIK, L., SHORE, T.L. and LINTON, D.A., 2004. Measuring trap efficiency for bark beetles (Col., Scolytidae). Journal of Applied Entomology, vol. 128, no. 5, pp. 337-341. http://dx.doi.org/10.1111/j.1439-0418.2004.00851.x.
http://dx.doi.org/10.1111/j.1439-0418.20...
; Allison and Redak, 2017ALLISON, J.D. and REDAK, R.A., 2017. The impact of trap type and design features on survey and detection of bark and woodboring beetles and their associates: a review and meta–analysis. Annual Review of Entomology, vol. 62, no. 1, pp. 127-146. http://dx.doi.org/10.1146/annurev-ento-010715-023516. PMid:27813665.
http://dx.doi.org/10.1146/annurev-ento-0...
). The insect flight angle in relation to the impact surface affects the capture of Scolytinae, as an insect flying parallel to the flat panel of the trap will not be captured due to an angle equal to or close to 0º (Safranyik et al., 2004SAFRANYIK, L., SHORE, T.L. and LINTON, D.A., 2004. Measuring trap efficiency for bark beetles (Col., Scolytidae). Journal of Applied Entomology, vol. 128, no. 5, pp. 337-341. http://dx.doi.org/10.1111/j.1439-0418.2004.00851.x.
http://dx.doi.org/10.1111/j.1439-0418.20...
). This may explain differences between the results of the original and the modified semi-funnel traps, both with angled panels compared to the Pet–Santa Maria.
The greater number of Scolytinae captured in the semi-funnel trap than in the Pet–Santa Maria agrees with report for wood borers collected with these traps and also with the Marques–Pedrosa and Carvalho–47 types in an agroforestry corridor in the municipality of Seropédica, Rio de Janeiro, Brazil (Bossoes, 2011BOSSOES, R.R., 2011. Avaliação e adaptação de armadilhas para captura de insetos em corredor agroflorestal. Seropédica: Universidade Federal Rural do Rio de Janeiro, 46 p. Dissertação de Mestrado em Fitossanidade e Biotecnologia Aplicada.). The cost of the Pet–Santa Maria trap is lower and it is more practical than the Marques–Pedrosa, Escolitídeo–Curitiba, Marques–Carrano and Roechling traps, but these first two were more efficient in capturing Scolytidae in native forest in the municipality of Itaara, Rio Grande do Sul, Brazil (Pelentir, 2007PELENTIR, S.C.S. 2007. Eficiência de cinco modelos de armadilhas etanólicas na coleta de Coleoptera: Scolytidae, em floresta nativa no município de Itaara, RS. Santa Maria: Universidade Federal de Santa Maria, 74 p. Dissertação de Mestrado em Engenharia Florestal.). The relationship between the distance where the insect starts its flight to the trap and the proportion of individuals captured among those attracted also affect the success of capturing them in the traps (Allison and Redak, 2017ALLISON, J.D. and REDAK, R.A., 2017. The impact of trap type and design features on survey and detection of bark and woodboring beetles and their associates: a review and meta–analysis. Annual Review of Entomology, vol. 62, no. 1, pp. 127-146. http://dx.doi.org/10.1146/annurev-ento-010715-023516. PMid:27813665.
http://dx.doi.org/10.1146/annurev-ento-0...
).
4.1. Influence of climate factors
The largest number of individuals of Scolytinae in drier and warmer months, differs from that reported for Cryptocarenus diadematus Eggers, 1937 and Cryptocarenus heveae Hagedorn, 1912 (Coleoptera: Curculionidae: Scolytinae) with higher numbers in the rainier periods in Eucalyptus urophylla x Eucalyptus grandis W. Hill ex Maiden plantation in Alta Floresta, Mato Grosso state, Brazil (Monteiro et al., 2018MONTEIRO, M., CARVALHO, C.C. and GARLET, J., 2018. Escolitíneos (Curculionidae: Scolytinae) associados a plantio de Eucalyptus urophylla x Eucalyptus grandis na amazônia meridional em Alta Floresta, Mato Grosso. Ciência Florestal, vol. 28, no. 3, pp. 913-923. http://dx.doi.org/10.5902/1980509833355.
http://dx.doi.org/10.5902/1980509833355...
). The precipitation in this region is very high, which may have induced these beetles to start flying in the rainy season (Monteiro et al., 2018MONTEIRO, M., CARVALHO, C.C. and GARLET, J., 2018. Escolitíneos (Curculionidae: Scolytinae) associados a plantio de Eucalyptus urophylla x Eucalyptus grandis na amazônia meridional em Alta Floresta, Mato Grosso. Ciência Florestal, vol. 28, no. 3, pp. 913-923. http://dx.doi.org/10.5902/1980509833355.
http://dx.doi.org/10.5902/1980509833355...
). The relative humidity variation was low with an average of 74.20%, during the collections of the largest number of individuals in the months of December and January, when the relative humidity was 67.75%, 8.7% lower than the average recorded during the experiment. However, C. diadematus was more collected in periods with lower relative humidity in Eucalyptus urophylla x Eucalyptus grandis plantations in Mato Grosso state, Brazil (Martins e Silva et al., 2021MARTINS E SILVA, M.H., GARLET, J., SILVA, F.L. and SILVA PAULA, C., 2021. Coleoborers (Curculionidae: Scolytinae) in native and homogeneous systems of Brazil nut (Bertholletia excelsa bonpl.) in the Southern Amazon, Brazil. PLoS One, vol. 16, no. 1, pp. e0234287. http://dx.doi.org/10.1371/journal.pone.0234287. PMid:33428621.
http://dx.doi.org/10.1371/journal.pone.0...
). The average wind speed, during the experiment was 1.82 m/s to 2.17 m/s in the months with the highest Scolytinae collection. Generally, wind speed is inversely correlated with the collection of these insects, but they can fly in the presence or absence of wind (Wijerathna and Evenden, 2020WIJERATHNA, A. and EVENDEN, M., 2020. Effect of environmental conditions on flight capacity in Mountain Pine Beetle (Coleoptera: Curculionidae: Scolytinae). Journal of Insect Behavior, vol. 33, no. 5-6, pp. 201-215. http://dx.doi.org/10.1007/s10905-020-09760-y.
http://dx.doi.org/10.1007/s10905-020-097...
). Climatic variations influence plant development, directly affecting the diversity and number of Scolytinae due to the associations between these beetles and their host plants (Cajaiba et al., 2018CAJAIBA, R.L., SILVA, W.B. and PÉRICO, E., 2018. Diversity of Scolytinae (Coleoptera: Curculionidae) in different landscapes in northern Brazil. Neotropical Biology and Conservation, vol. 13, no. 1, pp. 10-16. http://dx.doi.org/10.4013/nbc.2018.131.02.
http://dx.doi.org/10.4013/nbc.2018.131.0...
).
The lack of correlation between the number of Scolytinae captured and the temperature in the experiment 1 and precipitation in both experiments is similar to that reported for Crypturgus spp., Dryocoetes autographus Ratzeburg, 1897, Hylurgops palliatus Gyll, 1813, Orthotomicus spp. and Pityophthorus pityographus Ratzeburg, 1897 (Coleoptera: Curculionidae: Scolytinae) in wild pine forests in alpine valleys of Central Europe (Wermelinger et al., 2021WERMELINGER, B., RIGLING, A., SCHNEIDER MATHIS, D., KENIS, M. and GOSSNER, M.M., 2021. Climate change effects on trophic interactions of bark beetles in Inner Alpine Scots Pine forests. Forests, vol. 12, no. 2, pp. 136. http://dx.doi.org/10.3390/f12020136.
http://dx.doi.org/10.3390/f12020136...
). The positive mean correlation between the number of Scolytinae collected and the temperature in the experiment 2 is similar to that reported for Xyleborus affinis Eichhoff, 1868 (Coleoptera: Curculionidae: Scolytinae) in periods with warmer temperatures in Santa Cruz, Rio de Janeiro state, Brazil (Silva et al., 2020SILVA, C.O., TREVISAN, H., SOUZA, T.S. and CARVALHO, A.G., 2020. Occurrence of Scolytinae in mangrove with impact trap and in wood of five forest species. Bioscience Journal, vol. 36, no. 1, pp. 256-265. http://dx.doi.org/10.14393/BJ-v36n1a2020-47920.
http://dx.doi.org/10.14393/BJ-v36n1a2020...
).
The negative correlation, in the experiment 1 and 2 between the number of Scolytinae collected and the precipitation corroborates that reported for X. affinis in a preserved fragment of savannah in Coxipó-da-Ponte, Cuiabá, Mato Grosso, Brazil (Goulart et al., 2018GOULART, A.L., RODRIGUES, M.L. and FERNANDES, N.M.Q., 2018. Diversity of Curculionidae (Coleoptera) in forested savanna fragment in the urban perimeter of Cuiabá-MT. Journal of Biodiversity, vol. 17, pp. 22-31.). High rainfall can reduce alcohol volatilization and, consequently, Scolytinae flight (Sanguansub et al., 2020SANGUANSUB, S., BURANAPANICHPAN, S., BEAVER, R.A., SAOWAPHAK, T., TANAKA, N. and KAMATA, N., 2020. Influence of seasonality and climate on captures of wood–boring Coleoptera (Bostrichidae and Curculionidae (Scolytinae and Platypodinae)) using ethanol–baited traps in a seasonal tropical forest of northern Thailand. Journal of Forest Research, vol. 25, no. 4, pp. 223-231. http://dx.doi.org/10.1080/13416979.2020.1786897.
http://dx.doi.org/10.1080/13416979.2020....
). The increase in the temperature and precipitation improve the quality of the host tree phloem and the positive or negative correlation of these factors with the number of Scolytinae captured varies with the evolutionary success of these beetles, the host tree and its monoterpene contents (Wermelinger et al., 2021WERMELINGER, B., RIGLING, A., SCHNEIDER MATHIS, D., KENIS, M. and GOSSNER, M.M., 2021. Climate change effects on trophic interactions of bark beetles in Inner Alpine Scots Pine forests. Forests, vol. 12, no. 2, pp. 136. http://dx.doi.org/10.3390/f12020136.
http://dx.doi.org/10.3390/f12020136...
).
The low and negative correlation, in the experiment 1, and medium, in the 2, of the number of Scolytinae captured with the relative humidity of the air agrees with that reported for C. diadematus, Cryptocarenus seriatus Eggers, 1933 and Hypothenemus obscurus Fabricius, 1801 (Coleoptera: Curculionidae: Scolytinae) in Eucalyptus spp. plantations in Cuiabá, Mato Grosso state, Brazil (Dorval et al., 2004DORVAL, A., PERES FILHO, O. and MARQUES, E.N., 2004. Levantamento de Scolytidae (Coleoptera) em plantações de Eucalyptus spp. em Cuiabá, estado de Mato Grosso. Ciência Florestal, vol. 14, no. 1, pp. 47-58. http://dx.doi.org/10.5902/198050981780.
http://dx.doi.org/10.5902/198050981780...
). On the other hand, it differs from that reported for Coptoborus ochromactonus, n. sp. (Coleoptera: Curculionidae: Scolytinae) with higher numbers of individuals collected in commercial plantations of Ochroma pyramidale (Cav. Ex. Lam.) Urb. with increasing relative humidity in Ecuador (Martínez et al., 2020MARTÍNEZ, M., COGNATO, A.I., GUACHAMBALA, M., URDANIGO, J.P. and BOIVIN, T., 2020. Effects of climate and host age on flight activity, infestation percentage, and intensity by Coptoborus ochromactonus (Coleoptera: Curculionidae: Scolytinae) in commercial balsa plantations of Ecuador. Journal of Economic Entomology, vol. 113, no. 2, pp. 824-831. http://dx.doi.org/10.1093/jee/toz303. PMid:31751469.
http://dx.doi.org/10.1093/jee/toz303...
). High temperature and humidity improve the growth of symbiotic fungi on their host plants and, consequently, of Scolytinae populations (Atkinson, 2019ATKINSON, T.H., 2019. Escarabajos descortezadores y ambrosiales (Coleoptera: Curculionidae: Scolytinae, Platypodinae) de Sonora, México. Dugesiana, vol. 26, no. 1, pp. 41-49. http://dx.doi.org/10.32870/dugesiana.v26i1.7068.
http://dx.doi.org/10.32870/dugesiana.v26...
).
The low and negative correlation between the number of Scolytinae captured and the wind speed, in the experiment 1, can be explained by the reduced variation in this parameter during the period of collection of these insects (Martínez et al., 2020MARTÍNEZ, M., COGNATO, A.I., GUACHAMBALA, M., URDANIGO, J.P. and BOIVIN, T., 2020. Effects of climate and host age on flight activity, infestation percentage, and intensity by Coptoborus ochromactonus (Coleoptera: Curculionidae: Scolytinae) in commercial balsa plantations of Ecuador. Journal of Economic Entomology, vol. 113, no. 2, pp. 824-831. http://dx.doi.org/10.1093/jee/toz303. PMid:31751469.
http://dx.doi.org/10.1093/jee/toz303...
). On the other hand, the high and positive correlation in the experiment 2 was expected as this variable increases the dispersion of attractive substances and, consequently, the attraction of Scolytinae (Salom and McLean 1991SALOM, S.M. and MCLEAN, J.A., 1991. Flight behavior of scolytid beetle in response to semiochemicals at different wind speeds. Journal of Chemical Ecology, vol. 17, no. 3, pp. 647-661. http://dx.doi.org/10.1007/BF00982133. PMid:24258813.
http://dx.doi.org/10.1007/BF00982133...
; Wijerathna and Evenden, 2020WIJERATHNA, A. and EVENDEN, M., 2020. Effect of environmental conditions on flight capacity in Mountain Pine Beetle (Coleoptera: Curculionidae: Scolytinae). Journal of Insect Behavior, vol. 33, no. 5-6, pp. 201-215. http://dx.doi.org/10.1007/s10905-020-09760-y.
http://dx.doi.org/10.1007/s10905-020-097...
). The influence of environmental variables depends on Scolytinae species and where these insects are collected (Rocha et al., 2011aROCHA, J.R.M., DORVAL, A., SOUZA, M.D.D. and COSTA, R.B.D., 2011a. Análise da ocorrência de coleópteros em plantios de Eucalyptus camaldulensis Dehn. em Cuiabá, MT. Floresta e Ambiente, vol. 18, no. 4, pp. 343-352. http://dx.doi.org/10.4322/floram.2011.054.
http://dx.doi.org/10.4322/floram.2011.05...
, bROCHA, J.R.M., DORVAL, A., PERES FILHO, O. and SILVA, A.L., 2011b. Coleópteros (Bostrichidae, Platypodidae e Scolytidae) em um fragmento de cerrado da baixada cuiabana. Ambiência, vol. 7, no. 1, pp. 89-101. http://dx.doi.org/10.5777/ambiencia.2011.01.07.
http://dx.doi.org/10.5777/ambiencia.2011...
). Environmental factors, in addition to tree health, wood density, moisture content in the host tissue and vegetation composition affect the collection of these insects (Martínez et al., 2019MARTÍNEZ, M., COGNATO, A.I., GUACHAMBALA, M. and BOIVIN, T., 2019. Bark and ambrosia beetle (Coleoptera: Curculionidae: Scolytinae) diversity in natural and plantation forests in Ecuador. Environmental Entomology, vol. 48, no. 3, pp. 603-613. http://dx.doi.org/10.1093/ee/nvz037. PMid:31002740.
http://dx.doi.org/10.1093/ee/nvz037...
).
Implementing strategies to increase the capture efficiency of Scolytinae from traps made with recyclable materials are extremely important for population monitoring of these insect pests. Thus, the results of this work show, in practice, that the use of wooden elements in the traps does not significantly affect the capture efficiency of Scolytinae. On the other hand, expanding the insect interception area provides an efficient strategy to optimize the capture of Scolytinae beetles. Therefore, the results presented in this work demonstrate that the population monitoring of Scolytinae can be improved using traps with larger insect interception areas, especially in the semi-funnel trap model.
5. Conclusions
The incorporation of E. urophylla slats and Cedrela sp. in the semi-funnel trap model did not increase the number of Scolytinae captured. The expansion of the insect interception area, with an extra panel, increased the number of these beetles captured in the semi-funnel trap model. The number of beetles collected was positively correlated with temperature and wind speed and negatively with relative air humidity in the experiment 2 with the increasing of insect flight intercept area in the semi-funnel trap.
Acknowledgements
To “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES- Finance Code 001), “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)” for financial support.
-
#In Memorian
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Publication Dates
-
Publication in this collection
08 June 2022 -
Date of issue
2024
History
-
Received
13 Dec 2021 -
Accepted
10 May 2022