ABSTRACT
Background: Mosquitoes of the genus Sabethes are widespread in South and Central America, and some species are associated with yellow fever transmission. We aimed to investigate Sabethes fauna in bamboo internodes in remnants of the Atlantic Forest.
Methods: Artificial holes were made in bamboo plants and monitored for the presence of immature mosquitoes for 12 months.
Results: Ten species of the genus Sabethes were identified, including Sa. aurescens, Sa. identicus, Sa. conditus, Sa. shannoni, Sa. albiprivus, Sa. purpureus, Sa. undosus, Sa.ignotus, Sa.soperi, and Sa. whitmani.
Conclusion: Artificial hole placement can increase the number of Sabethes species found in faunal investigations.
Keywords:
Mosquitoes; Atlantic forest; Tree holes; Yellow fever; Ecology
Sabethes Robineau-Desvoidy (Diptera: Culicidae) is a neotropical genus of mosquitoes found in wild environments where they develop in natural breeding sites of phytotelmata, such as tree holes and bamboo internodes1. Some species of this genus, including Sa. chloropterus, Sa. Albiprivus, and Sa. cyaneus, have been shown to be associated with circulation of the yellow fever virus2. Other species of this genus have been isolated from several arboviruses, such as those from Mayaro, Bunia, Ilheus and Saint Louis1.
The presence of Sabethes species in yellow fever transmission zones was documented in an earlier investigation3 of mosquito fauna. However, in ground-level surveys of Culicidae, the presence of Sabethes species is generally low because they are primarily canopy-dwelling4. Breeding site investigations have been shown to complement mosquito fauna surveys and this type of investigation is essential when studying Sabethes mosquitoes5.
In the present study, we discuss the fauna of Sabethes mosquitoes collected from the remnants of the Atlantic Forest in two municipalities in São Paulo State, Brazil. We also describe a strategy in which we used holes that simulated those made by Lepidoptera and Coleoptera insects in bamboo (side holes made with an electric drill, 8 mm in diameter), thereby increasing the number of Sabethes individuals collected in the field. Bamboo internodes were explored and bamboo traps were located at 1-3 m. Immature Sabethes specimens were collected during fieldwork conducted in 2023 (June and November) and 2024 (January to October). For each period, collections were conducted once a month for a total of 12 field samples. Bamboo internodes (Guadua spp.) were examined at three sites. The vegetation in these localities is defined as ombrophilous, dense forest with a submontane profile (Pariquera-Açu) and lowlands (Cananeia) (Figure 1). One site is located in the municipality of Pariquera-Açu (site A, 24°44'43.2"S 47°51'02.9"W), whereas the other two are located in the Cananeia (site B, 24°51'59.2"S 47°52'42.2"W and site C, 24°28'22.4"S 47°32'39.3"W ). Water in bamboo internodes with small holes made by insects was investigated for the presence of Sabethes as a previous study has reported the presence of immature members of this genus at these breeding sites6. The distances of these collection sites to the core of urban areas are: Site A, 5.7 km distant from the urban core of Pariquera-Açu, and Sites B and C, which are 23 km and 35 km, respectively, distant from the urban core of Cananeia.
(A) Natural hole in bamboo made by Curculionidae species; (B) artificial hole made with an electric drill; C) bamboo trap with an artificial hole installed in site (C); (D) specimen of Sa. identicus collected in bamboo internodes with artificial holes.
Although no bamboo plants were noted at site C, many adult individuals of Sabethes were collected using insect nets during exploratory field trips3. At Site A, the aquatic contents were sucked from the bamboo internodes with natural holes and artificial holes were made with an electric drill in some internodes. At Site B, the same procedure was executed. At Site C, four bamboo traps were installed because of the absence of natural bamboo. The artificial small holes resembled the natural holes made by Noctuidae larvae and adults of Curculionidae (Figure 1B). This procedure was used not to monitor and compare the efficiency of natural versus artificial holes, but rather to attempt to increase the number of immature insects collected. The larvae and pupae of Sabethes mosquitoes were collected using suction samplers. These specimens were then sent to the entomology laboratory at the School of Public Health, São Paulo University, and monitored until adults emerged, when they were identified using morphological keys7. The 10 different species of the genus Sabethes collected are listed in Table 1.
The most abundant species collected was Sa. albiprivus (18 individuals), followed by Sa. aurescens (12 individuals). While Site A exhibited the greatest abundance and richness of Sabethes species, Site C had the lowest values for both parameters. Sa. albiprivus was the only species found at all three localities. Sa. conditus and Sa. purpureus were only collected at Site C, whereas Sa. soperi was collected only at Site A.
The holometabolic cycle of mosquito development depends entirely on water bodies for larval development. These bodies can vary in size, water volume, biotic communities and physicochemical composition1. The finding of immature Sabethes in bamboo internodes in previous studies can be attributed to the fact that such habitats provide suitable physicochemical conditions and microorganisms that serve as nutrients for the larvae of these mosquitoes8.
Some Sabethes species such as Sa. albiprivus and Sa. purpureus are generalists and can be found in bamboo internodes and tree holes9, whereas others, such as Sa. aurescens, are more specialized and are found only in bamboo internodes10. The differences in abundance and diversity between the Sites suggest ecological differences between Sabethes species. Site C has primary Atlantic Forest flora with a greater availability of potential breeding sites (tree holes), Site B is in a human-impacted area with a highway running alongside it, and Site A is an area with transitional forest cover. The finding of a greater number of species and specimens at Site A indicates the capacity of species of this genus to adapt.
The high number of Sabethes species collected in this survey indicates plasticity in the oviposition site selection behavior of some of these species. Sa. albiprivus and Sa. purpureus, which are typically found in tree holes and bamboo internodes, was found only in bamboo internodes. The absence of Sabethes larvae in tree holes indicated the tendency of the species found in this study to oviposit in bamboo internodes, even when tree holes were available. Mangudo et al.9 noted that although only 5% of the trees sampled in their study had water-holding holes, only a few contained Sabethes larvae. These results suggest that (1) there is a low frequency of Sabethes oviposition at ground level, probably due to the greater availability of tree holes at the canopy level, which can contribute to the canopy-dwelling behavior of this genus, and (2) the potential ecological plasticity of these species for efficient use of bamboo internodes. As Sa. albiprivus is considered a potential yellow fever virus vector and naturally infects individuals in Argentina11 and Brazil12, the scenario described above highlights the crucial role of bamboo internodes in epidemiological surveys.
Mangudo et al.9 reported that of all the tree holes in which Sa. purpureus larvae were found in their study, most (86%) were laterally oriented (angular-side entrances on the tree trunk). This corroborates the results of Mattingly13, who showed the tendency of Sabethes species to oviposit in cryptic entrances. Our results support the findings of these studies, as several Sabethes species were collected from study areas where tree-hole breeding sites were less common than bamboo-hole breeding sites. Our findings also showed that the use of artificial holes in bamboo to collect Sabethes species was valid in places where adult individuals were captured, but larvae were not. In addition to increasing the number of species collected, this method is an alternative to mosquito field procedures, in which collectors are exposed to pathogens14.
ACKNOWLEDGMENTS
We offer our deepest thanks to the institutions that provided technical support for the development and implementation of this study.
REFERENCES
- 1 Forattini OP. Culicidologia Médica: identificação, biologia, epidemiologia. 2 Edition, São Paulo: EDUSP. 2002. 549 p.
- 2 Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, Santos AACD, Miranda, RM Bonelly IS, et al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018. Emerg Microbes Infect. 2019;8(1):218-31.
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3 Telles-de-Deus J, Mucci LF, Reginatto SL, Pereira M, Bergo ES, Camargo-Neves VLF. Evaluation of methods to collect diurnal Culicidae (Diptera) at canopy and ground strata, in the Atlantic Forest Biome. Insects. 2022;13(2):202. https://doi.org/10.3390/ insects13020202.
» https://doi.org/10.3390/ insects13020202 - 4 Pinto CS, Confalonieri UE, Mascarenhas BM. Ecology of Haemagogus sp. and Sabethes sp. (Diptera: Culicidae) in relation to the microclimates of the Caxiuanã National Forest, Pará, Brazil. Mem Inst Oswaldo Cruz. 2009;104:592-8.
- 5 Almeida JF, Belchior HCM, Ríos-Velásquez CM, Pessoa FAC. Diversity of mosquitoes (Diptera: Culicidae) collected in different types of larvitraps in an Amazon rural settlement. PLoS One. 2020;15(10):e0235726.
- 6 Lozovei AL. Mosquitoes microhabitats (Diptera: Culicidae) in bamboo internodes in Atlantic forest, Paraná, Brazil. Iheringia Ser Zool. 2001;90:3-13.
- 7 Neves MS, Motta MA, Maciel-de-Freitas R, Xavier AD, Lourenco-de-Oliveira R, Silva-do-Nascimento TF. Illustrated identification key to females of the genus Sabethes Robineau-Desvoidy recorded from Brazil (Diptera: Culicidae), in dichotomous and interactive formats, including an updated list of species and new records for the states. Zootaxa. 2024;2:253-87.
- 8 Marcondes C, Fernandes A, Paterno U, Muller GA, Pinho LC, Struffaldi DV. New records of mosquitoes from the southern Brazilian states of Santa Catarina and Rio Grande do Sul, with 18 species new for the States (Diptera: Culicidae). Zootaxa. 2003;347:1-6.
- 9 Mangudo C, Aparicio JP, Rossi GC, Gleise RM. Tree hole mosquito species composition and relative abundances differ between urban and adjacent forest habitats in northwestern Argentina. Bull Entomol Res. 2018;108(2):203-12.
- 10 Müller GA, Mello CF, Bueno AS, Azevedo WTA, Alencar J. Little noticed, but very important: The role of breeding sites formed by bamboos in maintaining the diversity of mosquitoes (Diptera: Culicidae) in the Atlantic Forest biome. PLoS One. 2022;17(9):e0273774.
- 11 Goenaga S, Fabbri C, Dueñas JC, Gardenal CN., Rossi GC, Calderon G, et al. Isolation of yellow fever virus from mosquitoes in Misiones province, Argentina. J Vector Borne Dis. 2012;12(11):986-93.
- 12 Oliveira CH, Andrade MS, Campos FS, Cardoso JC, Gonçalves-dos-Santos ME, Oliveira RS, et al. Yellow fever virus maintained by Sabethes mosquitoes during the dry season in Cerrado, a semiarid region of Brazil, in 2021. Viruses. 2023;15(3):757.
- 13 Mattingly PF. The biology of mosquito-borne disease. 1 Edition. New York and London: Allen and Unwin and Elsevier. 1969.184 p.
- 14 Santos M, Mariscal LC, Henríquez B, Garzón J, González P, Carrera JP, et al. Implementation of bamboo and monkey-pot traps for the sampling cavity-breeding mosquitoes in Darién, Panama. Acta Trop. 2020;205:105352.
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Data Availability Statement:
Data-in-article (Table 1).
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Financial Support:
Fundação de Amparo à Pesquisa do Estado de São Paulo (ref. no. 2021/14677-9; 2023/ 11212-0). State of São Paulo Research Foundation (ref. no. 2021/14677-9, 2023/11212-0). CAPES (ref. no. 88887.939180/2024-0). National Council for Scientific and Technological Development, Brazil (ref. no. 301466/2015-7).
Edited by
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Editor-in-Chief:
Prof. Dalmo Correia Filho. Orcid: https://orcid.org/0000-0002-2174-5058
Data-in-article (Table 1).


