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Evaluation of light-emitting diodes as attractant for sandflies (Diptera: Psychodidae: Phlebotominae) in northeastern Brazil

Abstract

Hoover Pugedo light traps were modified for use with green and blue-light-emitting diodes to trap phlebotomine sandflies in northeastern Brazil. A total of 2,267 specimens belonging to eight genera and 15 species were sampled. The predominant species were Nyssomyia whitmani(34.41%) and Micropygomyia echinatopharynx(17.25%).The green LED trap prevailed over the blue and control lights; however, no statistically significant difference could be detected among the three light sources. Even without statistical significance, we suggest using LEDs as an attractant for the capture of sandflies because of several advantages over the conventional method with incandescent lamps.

light trapping; vector control; sandfly surveillance


Phlebotomine sandflies are small dipteran insects that are distributed worldwide. The bite of the blood-feeding females is responsible for the transmission of several pathogens among vertebrate hosts, e.g., protozoan Leishmania species, the aetiological agents of the leishmaniasis disease (Ready 2013Ready P 2013. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58: 227-250.). Approximately 56 species of New World (America) phlebotomine sandflies are involved in the transmission of Leishmania species (Maroli et al. 2013Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L 2013. Phlebotomine sandflies and the spreading of leishmaniasis and other diseases of public health concern. Med Vet Entomol 27: 123-147., Brazil et al. 2015Brazil RP, Rodrigues AAF, Andrade-Filho JD 2015. Sand fly vectors ofLeishmania in the Americas - a mini review. Entomol Ornithol Herpetol 4: 144.). In northeastern Brazil, Nyssomyia whitmani(Antunes & Coutinho, 1939) and Lutzomyia longipalpis (Lutz & Neiva, 1912) are the main vectors of Leishmania and are responsible for cutaneous and visceral leishmaniasis, respectively (Silva et al. 2010)Silva FS, Carvalho LPC, Cardozo FP, Moraes JLP, Rebêlo JMM 2010. Sand flies (Diptera: Psychodidae) in a Cerrado area of the Maranhão state, Brazil. Neotrop Entomol 39: 1032-1038..

Phlebotomine vector control is a very important component of many antileishmaniasis programs (Alexander 2000Alexander B 2000. Sampling methods for phlebotomine sandflies.Med Vet Entomol 14: 109-122.). Sandflies are diurnally resting, crepuscular or nocturnally active species. Adults are attracted to artificial light sources, which has led to the widespread use of visible light-based traps for monitoring and mass trapping sandfly species. The Centers for Disease Control (CDC) miniature light traps have long been recognised as the most effective and widely used battery-operated traps for sampling medically important insects, including phlebotomine sandflies, in surveillance studies (Faiman et al. 2009Faiman R, Cuno R, Warburg A 2009. Comparative efficacy of three suction traps for collecting phlebotomine sand flies (Diptera: Psychodidae) in open habitats. J Vector Ecol 34: 114-118.). CDC light trap methods have become more effective over time, such as with the use of attractant-baited and light-emitting diode (LED) light traps (Mann et al. 2009Mann RS, Kaufman PE, Butler JF 2009. Lutzomyia spp (Diptera: Psychodidae) response to olfactory attractant and light emitting diode-modified light mosquito magnet X (MM-X) traps. J Med Entomol 46: 1052-1061., Cohnstaedt et al. 2012Cohnstaedt LW, Rochon K, Duehl AJ, Anderson JF, Barrera R, Su N, Gerry AC, Obenauer PJ, Campbel JF, Lysyk TJ, Allan S 2012. Arthropod surveillance programs: basic components, strategies and analysis. Ann Entomol Soc Am 105: 135-149., Müller et al. 2014Müller GC, Hogsette JA, Kline DL, Beier JC, Revay EE, Xue R 2014. Response of the sand fly Phlebotomus papatasi to visual, physical and chemical attraction features in the field. Acta Trop 141: 32-36.). LEDs with various wavelengths as excitation sources for attracting insects have recently been employed using modified light traps (Bishop et al. 2004Bishop AL, Worrall R, Spohr LJ, McKenzie HJ, Barchia IM 2004. Improving light-trap efficiency for Culicoides spp with light-emitting diodes. Vet Ital 40: 266-269., Hoel et al. 2007Hoel DF, Butler JF, Fawas EY, Watany N, El-Hossary SS, Villinski J 2007. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol 32: 302-308., Jenkins & Young 2010Jenkins AB, Young MB 2010. Investigation ofCulicoides spp preference for colour and source using light emitting diode and fluorescent light. S Afr J Anim Sci 40: 514-518.). There are some advantages, such as cheaper cost, difficulty to shatter, great durability and rare need of replacement, to the general use of LEDs as substitutes for the usual incandescent light sources. Furthermore, incandescent lamps emit light in the infrared range of the spectrum and most (95%) of this energy is emitted as heat (Cohnstaedt et al. 2008)Cohnstaedt L, Gillen JI, Munstermann LE 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24: 331-334., which is invisible to most insects (Briscoe & Chittka 2001)Briscoe AD, Chittka L 2001. The evolution of color vision in insects. Annu Rev Entomol 46: 471-510..

The use of LEDs to attract insects of medical importance has recently been reported, e.g., for the capture of phlebotomine sandflies and Culicoides biting midges, showing a preferential attraction of species to specific wavelengths of light (Bishop et al. 2004Bishop AL, Worrall R, Spohr LJ, McKenzie HJ, Barchia IM 2004. Improving light-trap efficiency for Culicoides spp with light-emitting diodes. Vet Ital 40: 266-269., Hoel et al. 2007Hoel DF, Butler JF, Fawas EY, Watany N, El-Hossary SS, Villinski J 2007. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol 32: 302-308., Silva et al. 2015Silva FS, Brito JM, Costa-Neta BM 2015. Field evaluation of light-emitting diode as attractant for blood-sucking midges of the genusCulicoides Latreille (Diptera: Culicomorpha, Ceratopogonidae) in the Brazilian savanna. Entomol News 125: 1-6.). To the best of our knowledge, no comparative research has been carried out in Brazil on the effectiveness of LEDs as substitutes for incandescent lamps in the sandfly collection. This study was therefore conducted to determine the response of some Brazilian sandfly species to LEDs compared to incandescent lamps as an effective low-cost strategy for improving insect trapping efficiency.

The samples were collected from two forested areas in northeastern state of Maranhão (MA), Brazil. Adult sandflies were trapped in one area between November-December 2013 (5 nights) (3º45’46’’S 43°12’44’’W - near the community of Riacho Seco) and in another area between August 2014-January 2015 (14 nights) (3º50’40’’S 43º15’13’’W - near the community of Buritizinho). The two areas were 10 Km from each other. In the region, the climate is tropical and semihumid, with a well-defined wet season between January-June, followed by a drought period until the next rains. The annual average rainfall is 1,500-1,800 mm and the average temperature ranges from 28-30ºC.

Sandflies were sampled from 06:00 pm-06:00 am with three Hoover Pugedo light traps (Pugedo et al. 2005Pugedo H, Barata RA, França-Silva JC, Silva JC, Dias ES 2005. HP: um modelo aprimorado de armadilha luminosa de sucção para a captura de pequenos insetos. Rev Soc Bras Med Trop 38: 70-72.), two of which were modified. In the present study, the only modification was the replacement of the incandescent light bulbs by LEDs (1 LED for each trap). The modified traps held a 5-mm high-intensity LED bulb (Molesmell Technology Co, Ltd, China), one in the green (520 nm, 15,000 mCD, 20-30º, 20 mA, 72 mW - MLL5G30-1416) and the other in the blue (470 nm, 6,000 mCD, 20-30º, 20 mA, 72 mW - MLL5B30-0608) region of the visible spectrum. These colours were chosen from a set of six that were tested in a previous pilot study (data not shown) as the most attractive light sources for sandflies. An incandescent bulb (150 mA, 3 V) was used as a control. Light traps were set 1.5 m above the ground and were spaced 50 m from each other. The trap placement was randomised before each collecting day.

Sandflies were processed and identified to the species level according to Galati (2003)Galati EAB 2003. Morfologia e taxonomia. Morfologia, terminologia de adultos e identificação dos táxons da America. In EF Rangel, R Lainson,Flebotomíneos do Brasil, Fiocruz, Rio de Janeiro, p. 53-175.. The specimens ofMicropygomyia echinatopharynx were identified according to Andrade Filho et al. (2004)Andrade Filho JD, Galati EBG, de Andrade WA, Falcão AL 2004. Description of Micropygomyia (Silvamyia) echinatopharynx sp. nov. (Diptera: Psychodidae) a new species of phlebotomine sand fly from the state of Tocantins, Brazil. Mem Inst Oswaldo Cruz 99: 609-615.. The collected specimens were deposited in the entomological collection of the Federal University of Maranhão, MA. Data were analysed using an ANOVA followed by pair-wise comparisons using the Student’s t test. Data were log transformed prior to analyses to achieve a more symmetric distribution. The differences between the averages are statistically significant when p < 0.05. The statistical analyses were performed using GraphPad Prism software (GraphPad Software Inc, USA).

A total of 2,267 specimens belonging to eight genera and 15 species were sampled using the three light traps (Table). The predominant species was N. whitmani, accounting for 34.41% of the collected specimens, followed by M. echinatopharynx (Andrade Filho, Galati, Andrade & Falcão, 2004) (17.25%), Micropygomyia trinidadensis(Newstead, 1922) (11.87%), Lu. longipalpis (8.60%),Evandromyia termitophila (Martins, Falcão & Silva, 1964) (8.25%), Evandromyia evandroi (Costa Lima & Antunes, 1936) (7.41%) and Evandromyia lenti (Mangabeira, 1938) (5.96%). The others accounted for 6.26%.

TABLE
Phlebotomine sandflies collected from light-emitting diode modified light traps in northeastern Brazil

The most frequent species shown here corroborates the finding of previous studies for northeastern MA (Silva et al. 2010Silva FS, Carvalho LPC, Cardozo FP, Moraes JLP, Rebêlo JMM 2010. Sand flies (Diptera: Psychodidae) in a Cerrado area of the Maranhão state, Brazil. Neotrop Entomol 39: 1032-1038., 2012Silva FS, Carvalho LPC, Souza JM 2012. Flebotomíneos (Diptera: Psychodidae) associados a abrigos de animais domésticos em área rural do nordeste do estado do Maranhão, Brasil. Rev Patol Trop 41: 337-347.). One remarkable exception is the presence ofM. echinatopharynx, which was recently described from the state of Tocantins, Brazil (Andrade Filho et al. 2004Andrade Filho JD, Galati EBG, de Andrade WA, Falcão AL 2004. Description of Micropygomyia (Silvamyia) echinatopharynx sp. nov. (Diptera: Psychodidae) a new species of phlebotomine sand fly from the state of Tocantins, Brazil. Mem Inst Oswaldo Cruz 99: 609-615.).M. echinatopharynx was the second-most-common species in the samples and was found only in the Buritizinho.

The green light source represented 38.33% of the sandflies that were collected in the field, followed by blue (34.18%) and incandescent light (27.48%). Although the green LED was the most prevalent wavelength of light attracting sandflies to light traps, there was no statistically significant difference between the numbers of the three light sources that were used here (F2 54 = 0.5909, p = 0.5574). All of the species were LED biased, with the exception of M. echinatopharynx andLu. longipalpis. In addition to these results, there was no significant difference between the most frequent species and the tested light sources.

The green-biased response was expected to occur because nocturnally active insects, such as sandflies, have trichromatic colour vision with photoreceptor sensitivities detecting the ultraviolet, blue and green wavebands (Briscoe & Chittka 2001Briscoe AD, Chittka L 2001. The evolution of color vision in insects. Annu Rev Entomol 46: 471-510., Mellor & Hamilton 2003)Mellor HE, Hamilton JGC 2003. Navigation of Lutzomyia longipalpis (Diptera: Psychodidae) under dusk or starlight conditions. Bull Entomol Res 93: 315-322.. Previous studies examining the attraction of blood-sucking insects to light of various wavelengths have shown that individual responses to light sources may occur (Bishop et al. 2004Bishop AL, Worrall R, Spohr LJ, McKenzie HJ, Barchia IM 2004. Improving light-trap efficiency for Culicoides spp with light-emitting diodes. Vet Ital 40: 266-269., Silva et al. 2015)Silva FS, Brito JM, Costa-Neta BM 2015. Field evaluation of light-emitting diode as attractant for blood-sucking midges of the genusCulicoides Latreille (Diptera: Culicomorpha, Ceratopogonidae) in the Brazilian savanna. Entomol News 125: 1-6.. Hoel et al. (2007)Hoel DF, Butler JF, Fawas EY, Watany N, El-Hossary SS, Villinski J 2007. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol 32: 302-308. found that Phlebotomus papatasi was strongly attracted to red light, followed by the control, blue and green lights and these results were defined by the authors as unexpected. It is possible that the intense brightness of the LEDs that were tested in our study accounted, at least in part, for the different results obtained with green and blue lights (1,500 and 650 mCD, respectively) compared to the control in the study by Hoel et al. (2007)Hoel DF, Butler JF, Fawas EY, Watany N, El-Hossary SS, Villinski J 2007. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol 32: 302-308.. Further studies are needed to better understand the role of brightness differences in the LEDs in attracting adult flying insects.

Our results showed that LED traps were as efficient as and even superior to incandescent lights for collecting sandflies. Thus, we suggest using LEDs as attractants for sandfly captures because this technology provides the above-mentioned advantages over the conventional method with incandescent lamps. Moreover, LEDs provide a much longer battery life, overcoming one of the constraints in conventional CDC light trapping. Further studies are needed to improve the use of LED light-trap catches in order to offer better alternatives for sandfly monitoring purposes.

REFERENCES

  • Alexander B 2000. Sampling methods for phlebotomine sandflies.Med Vet Entomol 14: 109-122.
  • Andrade Filho JD, Galati EBG, de Andrade WA, Falcão AL 2004. Description of Micropygomyia (Silvamyia) echinatopharynx sp. nov. (Diptera: Psychodidae) a new species of phlebotomine sand fly from the state of Tocantins, Brazil. Mem Inst Oswaldo Cruz 99: 609-615.
  • Bishop AL, Worrall R, Spohr LJ, McKenzie HJ, Barchia IM 2004. Improving light-trap efficiency for Culicoides spp with light-emitting diodes. Vet Ital 40: 266-269.
  • Brazil RP, Rodrigues AAF, Andrade-Filho JD 2015. Sand fly vectors ofLeishmania in the Americas - a mini review. Entomol Ornithol Herpetol 4: 144.
  • Briscoe AD, Chittka L 2001. The evolution of color vision in insects. Annu Rev Entomol 46: 471-510.
  • Cohnstaedt L, Gillen JI, Munstermann LE 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24: 331-334.
  • Cohnstaedt LW, Rochon K, Duehl AJ, Anderson JF, Barrera R, Su N, Gerry AC, Obenauer PJ, Campbel JF, Lysyk TJ, Allan S 2012. Arthropod surveillance programs: basic components, strategies and analysis. Ann Entomol Soc Am 105: 135-149.
  • Faiman R, Cuno R, Warburg A 2009. Comparative efficacy of three suction traps for collecting phlebotomine sand flies (Diptera: Psychodidae) in open habitats. J Vector Ecol 34: 114-118.
  • Galati EAB 2003. Morfologia e taxonomia. Morfologia, terminologia de adultos e identificação dos táxons da America. In EF Rangel, R Lainson,Flebotomíneos do Brasil, Fiocruz, Rio de Janeiro, p. 53-175.
  • Hoel DF, Butler JF, Fawas EY, Watany N, El-Hossary SS, Villinski J 2007. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol 32: 302-308.
  • Jenkins AB, Young MB 2010. Investigation ofCulicoides spp preference for colour and source using light emitting diode and fluorescent light. S Afr J Anim Sci 40: 514-518.
  • Mann RS, Kaufman PE, Butler JF 2009. Lutzomyia spp (Diptera: Psychodidae) response to olfactory attractant and light emitting diode-modified light mosquito magnet X (MM-X) traps. J Med Entomol 46: 1052-1061.
  • Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L 2013. Phlebotomine sandflies and the spreading of leishmaniasis and other diseases of public health concern. Med Vet Entomol 27: 123-147.
  • Mellor HE, Hamilton JGC 2003. Navigation of Lutzomyia longipalpis (Diptera: Psychodidae) under dusk or starlight conditions. Bull Entomol Res 93: 315-322.
  • Müller GC, Hogsette JA, Kline DL, Beier JC, Revay EE, Xue R 2014. Response of the sand fly Phlebotomus papatasi to visual, physical and chemical attraction features in the field. Acta Trop 141: 32-36.
  • Pugedo H, Barata RA, França-Silva JC, Silva JC, Dias ES 2005. HP: um modelo aprimorado de armadilha luminosa de sucção para a captura de pequenos insetos. Rev Soc Bras Med Trop 38: 70-72.
  • Ready P 2013. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58: 227-250.
  • Silva FS, Brito JM, Costa-Neta BM 2015. Field evaluation of light-emitting diode as attractant for blood-sucking midges of the genusCulicoides Latreille (Diptera: Culicomorpha, Ceratopogonidae) in the Brazilian savanna. Entomol News 125: 1-6.
  • Silva FS, Carvalho LPC, Cardozo FP, Moraes JLP, Rebêlo JMM 2010. Sand flies (Diptera: Psychodidae) in a Cerrado area of the Maranhão state, Brazil. Neotrop Entomol 39: 1032-1038.
  • Silva FS, Carvalho LPC, Souza JM 2012. Flebotomíneos (Diptera: Psychodidae) associados a abrigos de animais domésticos em área rural do nordeste do estado do Maranhão, Brasil. Rev Patol Trop 41: 337-347.

Publication Dates

  • Publication in this collection
    Sept 2015

History

  • Received
    31 Mar 2015
  • Accepted
    20 July 2015
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