Abstract
Light-Emitting Diodes (LEDs) have been effective light sources in attracting Anopheles mosquitoes, but the broad-spectrum white light, even with a wide-ranging application in lighting, have not been evaluated yet. In this study, the white light was field evaluated against the green one in the light trapping of anopheline mosquitoes by using two non-suction Silva traps and two CDC-type suction light traps. Anopheline mosquitoes were captured for two 21-night periods of collecting (2022 and 2023). In the first period, two LEDs were used per Silva trap, but three were used in the second one to increase the luminance/illuminance at traps. A CDC-type suction light trap equipped with an incandescent lamp was used in 2022 and a CDC-type suction light trap equipped with a 6 V-white light (higher luminance/illuminance) in 2023. A total of eight species and 3,289 specimens were captured in both periods. The most frequent species were Anopheles triannulatus s.l., An. goeldii, An. evansae and An. argyritarsis. In 2022, white LEDs were less attractive to anopheline mosquitoes than the other light sources, but without statistical difference among treatments (F = 2.703; P = 0.0752; df = 2). In 2023, even with an increased luminance/illuminance at traps, no statistical difference was found between the two LED-baited Silva traps (F = 6.690; P = 0.0024; df = 2), but rather between the 6 V-white-baited CDC-type suction light trap and green-baited Silva traps. Due to some drawbacks and the lower abundance of individuals caught by using white LEDs, the narrow-banded green LEDs is preferable to white ones for attracting anophelines.
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Introduction
Light-emitting diodes (LEDs) are semiconductors that produce light through electroluminescence (Cho et al. 2017) and have been proven to be energy-efficient solutions for home and industrial purposes due to their tremendous energy savings and longer lifetime (David and Whitehead 2018). Due to these attributes, LEDs have been used to replace traditional light sources in several applications, including street light technologies. Since artificial lights are a well-known increasing threat to nocturnal biodiversity, many recent studies have discussed the impact of LEDs on insects (Longcore et al. 2018; Owens and Lewis 2018; Desouhant et al. 2019; Fyie et al. 2021; Stewart 2021). Larval development and diapause (Van Geffen et al. 2014), mating (Van Geffen et al. 2015), flight activity (Wakefield et al. 2016) and pollination (Knop et al. 2017), may be affected by artificial lights. In this context, some comparative studies suggest that broad-spectrum white LEDs used in streetlights has negative impacts on insect biology (Pawson and Bader 2014; Wakefield et al. 2017; Boyes et al. 2021) and may play a role in facilitating disease transmission by attracting insect vectors (Wilson et al. 2021). On the other hand, narrow-banded spectrum LEDs have shown to be highly attractive to a broad range of insect groups (e.g., phlebotomine sand flies, anopheline mosquitoes, Culicoides biting midges, stored-product/agricultural insect pests) (Stukenberg et al. 2014; Silva et al. 2016; Costa-Neta et al. 2017; Park and Lee 2017; Da Rocha Silva et al. 2023).
In field insect vector studies, LEDs are the newest technology used for light trapping and monitoring (Wilson et al. 2021). Light traps have been widely used in insect vector monitoring because of a range of advantages over the other sampling methods. Ease use, safety, compactness, excellent yields, and low cost are some of the specificities that make the use of light traps preferable in some situations, particularly in remote areas such as forested environments (McDermott and Mullens 2018). Even so, light traps have been constantly improved to achieve better performance in terms of efficiency. One of these improvements is the use of LEDs as a replacement for incandescent bulbs routinely applied in standard light traps (Cohnstaedt et al. 2008). LEDs are longer-lived, resistant to mechanical shock and have well-defined wavelengths and intensities. Additionally, LED lights, particularly narrow-banded green and blue wavelengths, have shown to be highly attractive to some dipteran groups of public health importance (Hoel et al. 2007; Rodríguez-Rojas et al. 2016; Venter et al. 2018; Da Rocha Silva et al. 2023), including anopheline mosquitoes (Costa-Neta et al. 2017, 2018, 2023; Da Silva et al. 2019; De Araújo et al. 2023).
Anopheline mosquitoes are of major importance to human health due to the ability to transmit several species of Plasmodium, the causative agents of malaria (Varo et al. 2020). Malaria is found almost all over the world, mainly in tropical and sub-tropical countries, with one third of the world´s population being at risk (Rocha et al. 2020; Varo et al. 2020). Even with a reduction in the number of cases by 53% from 2009 to 2020 in the Brazilian Amazon, malaria is still a challenge to the health surveillance programmes to achieve the targets proposed by the WHO GTS (Global Technical Strategy) 2030 milestone in Brazil (Laporta et al. 2022). The primary malaria vector in Brazil is Anopheles (Nyssorhynchus) darlingi (Root, 1926), a nocturnal mosquito with crepuscular activity peaks (Carlos et al. 2019). In the search for blood meals, masses of adult host-seeking females arrive at the feeding areas just after sunset attracted by host-related odour cues (Costa-Neta et al. 2023). Since anopheline mosquitoes are positively phototactic, artificial lights also play a role on attracting them to the vicinity of or into human dwellings (Mmbando et al. 2022). This phototaxis favours the use of light traps as an effective alternative approach to the standard but ethically flawed human landing catch method for sampling host-seeking anopheline mosquitoes (Briët et al. 2015; Eckert et al. 2022; Mawejje et al. 2022).
By using lighted devices, some studies have been performed to evaluate the use of LEDs as attractant for anopheline mosquitoes as compared to widely used incandescent-baited CDC-type suction light traps (Costa-Neta et al. 2017, 2018, 2023; Da Silva et al. 2019; De Araújo et al. 2023). In such studies, green/blue wavelengths have been shown to be suitable light sources for attracting Anopheles species, even more so if LEDs have a higher luminous intensity (Costa-Neta et al. 2018). Nevertheless, a continuous need for light source-based improvement in insect monitoring is always present. In this context, nothing is known about the attractiveness of broad-spectrum white lights, typically used in standard LED-based lamps, to anopheline mosquitoes, even with the growing use of LED technology in lighting systems. Therefore, the present study was aimed to compare the attractiveness of the broad-spectrum white LED with the narrow-banded green wavelength in the light trapping of anopheline mosquitoes in a forested area of northeastern Brazil.
Material and methods
This research was carried out in the municipality of Chapadinha, 230 km away from the capital São Luis, northeastern Brazil. The forested site (3°44´26´´ S, 43°21´33´´ W) is covered by a cerrado vegetation interdigitated by mesophytic and gallery forests. In the region, the predominant climate is Aw (tropical savanna), based on the Köppen classification system (Alvares et al. 2013). There are two well defined periods: the rainy season from January to June and the dry season from July to December, with an annual average precipitation of 1,613.2 mm. The annual average temperature is 27.9°C and the annual relative humidity is 75% (Passos et al. 2016). This study was undertaken in the dry period, between August and October 2022 and in August 2023, where the year-to-year climatic fluctuation (e.g., precipitation, temperature, humidity) in the studied area is less pronounced (Nogueira et al. 2012).
As abovementioned, anopheline mosquitoes were captured within two periods (2022 and 2023), each one having 21 nights of collecting. A total of three light traps was used per night and period: two Silva traps and one CDC-type suction light trap as control. The Silva traps (Horst Armadilhas Ltd-me, São Paulo, Brazil) were equipped with high-intensity round through-hole 5 mm LEDs, one trap with a green (520 nm, 15,000 mcd, 3 V, 20 mA) and the other with a white (broad spectrum, 18,000 mcd, 3 V, 20 mA) LED. Two LEDs of the same color (green or white) were used per Silva trap in the first period (2022), but three were used in the second one (2023) to test the influence of a higher luminance/illuminance level on the attractiveness of the Silva traps to mosquitoes. It is worth saying that the Silva trap is a non-suction updraft trapping device and that the LED beam is directed to a reflective surface at the bottom of the trap (Silva et al. 2019). The incandescent-baited CDC-type suction light trap (Basic Model Bioquip®, 2836BQ, 6 V DC, 4 watt, model CM-47) (Sudia and Chamberlain 1962) was used in the first period. In the second period, to increase the luminance/illuminance in the suction trap and to evaluate whether the efficiency of the incandescent-baited CDC-type suction light trap in capturing anophelines in the first period was due to the trap design, the incandescent-baited CDC-type suction light trap was replaced by a 6 V-white-LED-baited CDC-type suction light trap (wide spectrum, BA9S, DIP, 9 mm, round) (Horst Armadilhas Ltd-me).
In the two periods, all traps were installed between 18:00 and 06:00h, set at 1.5 m above the soil level and spaced 30 m apart. The traps moved clockwise until they had been run at each collecting site following a 3x3 Latin-square design (De Araújo et al. 2023). A total of seven replications were run, with each replication requiring three days. Following the day after the collections, anopheline mosquitoes were transported to the laboratory to be killed by freezing (-20°C), placed in individually labeled plastic cups and identified morphologically following the identification keys by Consoli and Lourenço de Oliveira (1994) and Sallum et al. (2020).
Statistical analyses were performed to evaluate the attractiveness of the light sources to mosquitoes by using the GraphPad Prism software version 8.0 (San Diego, CA). One-way ANOVA was conducted to compare trap types, and a pos-test (Tukey’s test) was used to separate means. Data distribution was checked using the Kolmogorov-Smirnov test, with differences being considered significant when P < 0.05.
Results and discussion
A total of 3,289 anopheline mosquitoes were caught in both periods, 926 specimens and seven species in the first and 2,363 and five species in the second one (Table 1). The most frequent species in both periods were An. triannulatus s.l. (Neiva and Pinto, 1922) (68.9% of the total catch in 2022 and 95.3% in 2023), An. goeldii (Rozeboom and Gabaldón, 1941) (13.6% and 2.4%), An. evansae (Brethés, 1926) (10.3% and 2.4%) and An. argyritarsis (Robineau Desvoidy, 1827) (5.3% and 1.5%). All species found were recorded in the study area before (Costa-Neta et al. 2017, 2023; De Araújo et al. 2023). It is worth emphasizing that An. triannulatus is thought to be a secondary vector of malaria in the Amazon basin, found naturally infected with plasmodial parasites (Tadei and Thatcher 2000). Among the less abundant species, An. neomaculipalpus (Curry, 1931) and An. mediopunctatus (Lutz, 1903) represent species recently recorded in northeastern Brazil (De Araújo et al. 2023; Costa-Neta et al. 2023).
In 2022, white LEDs (10.52±1.28) were statistically less attractive to anopheline mosquitoes than the other light sources (green = 16.95± 2.60; CDC-type suction light trap = 16.62± 1.83) (Table 1), but without statistical significance difference among treatments (F = 2.703; P = 0.0752; df = 2) (Fig. 1). In the second period, the number of LEDs was changed to three to increase the luminance/illuminance at the trap. Even with an increased luminance/illuminance at traps, no statistically significant difference was found between the Silva traps equipped with two LEDs (green = 56.67±15.06; white = 36.05±6.04) (F = 6.690; P = 0.0024; df = 2), but between the 6 V-white-baited CDC-type suction light trap (19.81±5.28) and Silva traps equipped with green LEDs. The white-LED-baited Silva trap attracted 38.88% of the total number of individuals when comparing with the green LED-baited trap (61.12%), practically the same as in the first period (white: 38.30%; green: 61.70%), but without a significant difference in both periods. This relationship was also found in a 45-night study conducted in a neighbouring municipality, in which a white-baited Silva trap, equipped with only one LED, captured 38.38% of the anopheline mosquitoes in comparison with a Silva trap fitted with one green LED, which captured 61.62% (data not shown). The results indicated that even with the increase of the luminance/illuminance at traps (by increasing the number of LEDs per trap), there was no effect on the attractiveness of the 18,000 mcd-white LEDs in relation to the 15,000 mcd-green LED.
Statistically, the incandescent-baited CDC-type suction light trap was equally attractive to mosquitoes in the first period, but, when it was replaced by the white bulb-baited CDC-type suction light trap in the second one, this trap type captured the lowest number of individuals. The suction trap was statistically inferior to the Silva trap equipped with three green LEDs (Fig. 1), but not to the Silva trap equipped with three white LEDs. The incandescent-baited CDC-type suction light trap is efficient in capturing anopheline mosquitoes, but only 6% of the incandescent bulb energy is released in the visible light spectrum (blue, green and red) and 94% as heat (infrared) (Cohnstaedt et al. 2008). However, heat may be used as a host cue for anopheline mosquitoes, as observed by Hawkes et al. (2017), in which heated traps and host odour caught the most mosquitoes. The incandescent-baited CDC-type suction light trap was also more attractive than a solar-powered suction trap (the Silver Bullet light trap) fitted with three white LEDs in the study by Mbare and Njoroge (2023) in western Kenya. On the other hand, the 6 V-white-baited CDC-type suction light trap was less effective in sampling mosquitoes, due to both a higher luminance/illuminance at the Silva traps and the overall lower attractiveness of white light to Anopheles mosquitoes, as indicated in the present study.
The findings of the present study corroborate the works previously reported in the studied area. The non-suction Silva trap equipped with two blue LEDs have already been field-evaluated in comparison with standard CDC-type suction light traps, with no statistically significant difference being found between them (Silva et al. 2019), showing that both traps capture anopheline mosquitoes equally well. However, when the Silva trap equipped with three green LEDs was compared to an incandescent-baited CDC-type suction light trap (De Araújo et al. 2023), a significant difference was found, thus emphasizing a possible role of the increased luminance/illuminance on the attractiveness of lighted traps. Further studies are needed to determine whether the number of LEDs has a direct influence on the catch size of Anopheles mosquitoes.
LED chips, like the green LED in this study (520 nm), emit a radiation within a narrow wavelength range, resulting in a nearly monochromatic light, but white light (broadband emission) is achieved by a combination of narrow-band emissions. In most cases, a phosphor (e.g., yellow phosphor) is used to react with a blue chip (primary emission) to form white light (Cho et al. 2017; David and Whitehead 2018). In this study, it was shown that the 5 mm white LED emission also acts as a light attractant for anopheline mosquitoes, but it may not be interesting when considering light trapping. In addition, during the field tests, the white LEDs had to be replaced by new ones every three nights of collecting because its brightness decreased slightly and irreversibly (own observation). The main difference between the 5 mm type green and the similar 5 mm white LED is the phosphor embedded in an encapsulant that surround the LED chip, factors other than the phosphor are rather the cause of the white light output reduction (Appaiah et al. 2015). Therefore, due to the abovementioned drawbacks and the lower abundance of individuals caught by using white LEDs, the narrow-banded green LEDs is preferable to white ones for attracting anophelines. Even as an attractant, nothing is known yet concerning the impact of the broad-spectrum white LEDs used in houses and streetlights on the attraction of anopheline mosquitoes, so further investigations are needed.
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FSS wrote, revised and edited the manuscript; FSS, JCV designed the study; JCV, FFC and GBA performed the field experiments; BMCN and JCV processed and identified the material; FSS, BMCN and JMB contributed to data analysis. All authors read and approved the final version of the manuscript.
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Silva, F.S., da Costa Viana, J., de França da Costa, F. et al. Field comparison of broad-spectrum white LED-baited traps with narrow-spectrum green LED-baited traps in the capture of Anopheles mosquitoes (Diptera: Culicidae). Parasitol Res 123, 194 (2024). https://doi.org/10.1007/s00436-024-08217-x
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DOI: https://doi.org/10.1007/s00436-024-08217-x