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Fulltext Biodiversity, seasonal abundance, and distribution of blackflies (Diptera: Simuliidae) in six different regions of Thailand

Srisuka W, Takaoka H, Otsuka Y, Fukuda M, Thongsahuan S, Taai K, et al.

Parasit Vectors, 2017 Nov 21;10(1):574.
PMID: 29157269 DOI: 10.1186/s13071-017-2492-y

BACKGROUND: Blackflies are an important medical and veterinary group of small blood-sucking insects. Ninety-three blackfly species have been reported in Thailand. However, information on their biodiversity and population dynamics in each region is lacking. The main aim of this study was to assess the regional biodiversity, seasonal abundance and distribution of blackflies in six eco-geographically different regions in the country.
METHODS: Blackfly larvae and pupae were sampled monthly from 58 sites between May 2011 and April 2013. Diversity parameters, seasonal abundance, regional distribution and frequency of species occurrence in stream sites were analyzed.
RESULTS: A total of 19,456 mature larvae representing 57 species, and belonging to six subgenera in the genus Simulium Latreille (s.l.), were found. The five predominant taxa were S. fenestratum (8.6%), the S. asakoae complex (8.3%), S. nakhonense (7.5%), the S. siamense complex (7.4%) and the S. doipuiense complex (6.7%). The most frequent taxa at all sites were the S. asakoae complex (84.5%), followed by S. fenestratum (82.8%), the S. siamense complex (75.9%), S. decuplum (60.3%), S. nakhonense (58.6%) and the S. tani complex (48.3%). The richness of regional species was highest (40 species) in the north and predominated in the cold season. However, blackflies in the south predominated during the hot season. The highest numbers of blackflies collected from central, northeastern, eastern and western regions of the country were observed in the rainy season. Overall, the mean number of blackflies collected across the six regions during the rainy and cold season had no statistically significant difference, but it differed significantly in the hot season.
CONCLUSIONS: Blackflies in Thailand were surveyed in all three seasons across six geographical regions. These findings demonstrated that blackfly communities at each stream site varied with seasonality, and the regional relative abundance of blackflies differed markedly in the hot season. It was also found that the occurrence and distribution of blackflies in each region were associated strongly with elevation.
Reliability of wing morphometrics for species identification of human-biting black flies (Diptera: Simuliidae) in Thailand

Aupalee K, Srisuka W, Limsopatham K, Sanit S, Takaoka H, Saeung A

Parasit Vectors, 2024 Dec 18;17(1):508.
PMID: 39695748 DOI: 10.1186/s13071-024-06597-8

BACKGROUND: Fast and reliable species identification of black flies is essential for research proposes and effective vector control. Besides traditional identification based on morphology, which is usually supplemented with molecular methods, geometric morphometrics (GM) has emerged as a promising tool for identification. Despite its potential, no specific GM techniques have been established for the identification of black fly species.
METHODS: Adult female black flies collected using human bait, as well as those reared from pupae, were used in this study. Here, landmark-based GM analysis of wings was assessed for the first time to identify human-biting black fly species in Thailand, comparing this approach with the standard morphological identification method and DNA barcoding based on the mitochondrial cytochrome c oxidase subunit I (COI) gene. To explore genetic relationships between species, maximum likelihood (ML) and neighbor-joining (NJ) phylogenetic trees were built. Additionally, three different methods of species delimitation, i.e., assemble species by automatic partitioning (ASAP), generalized mixed yule coalescent (GMYC), and single Poisson tree processes (PTP), were utilized to identify the morphologically defined species. The effectiveness of a COI barcode in identifying black fly species was further examined through the best match (BM) and best close match (BCM) methods.
RESULTS: Seven black fly species, namely Simulium tenebrosum Takaoka, Srisuka & Saeung, 2018 (complex), S. doipuiense Takaoka & Choochote, 2005 (complex), S. nigrogilvum Summers, 1911, S. nodosum Puri, 1933, S. asakoae Takaoka & Davies, 1995, S. chamlongi Takaoka & Suzuki, 1984, and S. umphangense Takaoka, Srisuka & Saeung, 2017 were morphologically identified. Compared with the standard method, the GM analysis based on wing shape showed high success in separating species, achieving an overall accuracy rate of 88.54%. On the other hand, DNA barcoding surpassed wing GM for species identification with a correct identification rate of 98.57%. Species delimitation analyses confirmed the validity of most nominal species, with an exception for S. tenebrosum complex and S. doipuiense complex, being delimited as a single species. Moreover, the analyses unveiled hidden diversity within S. asakoae, indicating the possible existence of up to four putative species.
CONCLUSIONS: This study highlights the potential of wing GM as a promising and reliable complementary tool for species identification of human-biting black flies in Thailand.
Metabolomic analysis of larval stages of Onchocerca japonica (Spirurida: Onchocercidae), raised in black fly (Diptera: Simuliidae) vectors, by gas chromatography-tandem mass spectrometry

Fukuda M, Otsuka Y, Sakai K, Uni S, Junker K, Saeung A, et al.

Acta Trop, 2025 Feb 09;263:107541.
PMID: 39933644 DOI: 10.1016/j.actatropica.2025.107541

To monitor and prevent the spread of zoonotic onchocerciasis, identification of the natural vectors (blood-sucking insects) of its causative agents, Onchocerca species, is crucial. To date, vector identification depends on the detection of infective third-stage larvae in insects by traditional dissection. We aimed to develop a novel, more efficient method for the discrimination of the four larval stages, i.e. microfilariae (Mf), first-stage larvae (L1), second-stage larvae (L2), and third-stage larvae (L3), of O. japonica by metabolomic analysis. Microfilariae of O. japonica, the causative agent of zoonotic onchocerciasis in Japan, were obtained from skin snips of wild boars and injected into newly-emerged black flies (Diptera: Simuliidae) to enable further larval development. Metabolites obtained from Mf, L1, L2, and L3 were analyzed using a gas chromatography-tandem mass spectrometer. Multivariate analysis of the data of metabolites showed the complete separation of the four larval stages. The highest level of acetoacetic acid and hydroxylamine was found in Mf and L3, respectively. Consequently, we propose that hydroxylamine is a potential marker to detect infective larvae of O. japonica in natural infections and could be a valuable tool in vector surveys, transmission studies and epidemiological surveys.
Fulltext Tests of conspecificity for allopatric vectors: Simulium nodosum and Simulium shirakii (Diptera: Simuliidae) in Asia

Low VL, Adler PH, Sofian-Azirun M, Srisuka W, Saeung A, Huang YT, et al.

Parasit Vectors, 2015 May 29;8:297.
PMID: 26022092 DOI: 10.1186/s13071-015-0911-5

BACKGROUND: Allopatric populations present challenges for biologists working with vectors. We suggest that conspecificity can be concluded in these cases when data from four character sets-chromosomal, ecological, molecular, and morphological-express variation no greater between the allopatric populations than between corresponding sympatric populations. We use this approach to test the conspecificity of Simulium nodosum Puri on the mainland of Southeast Asia and Simulium shirakii Kono & Takahasi in Taiwan. The validity of these two putative species has long been disputed given that they are morphologically indistinguishable.
FINDINGS: The mitochondria-encoded cytochrome c oxidase subunit I (COI), 12S rRNA, and 16S rRNA genes and the nuclear-encoded 28S rRNA gene support the conspecific status of S. nodosum from Myanmar, Thailand, and Vietnam and S. shirakii from Taiwan; 0 to 0.19 % genetic differences between the two taxa suggest intraspecific polymorphism. The banding patterns of the polytene chromosomes of the insular Taiwanese population of S. shirakii and mainland populations of S. nodosum are congruent. The overlapping ranges of habitat characteristics and hosts of S. nodosum and S. shirakii corroborate the chromosomal, molecular, and morphological data.
CONCLUSIONS: Four independent sources of evidence (chromosomes, DNA, ecology, and morphology) support the conspecificity of S. nodosum and S. shirakii. We, therefore, synonymize S. shirakii with S. nodosum. This study provides a guide for applying the procedure of testing conspecificity to other sets of allopatric vectors.
Proteomes of the female salivary glands of Simulium nigrogilvum and Simulium nodosum, the main human-biting black flies in Thailand

Hempolchom C, Reamtong O, Sookrung N, Srisuka W, Sakolvaree Y, Chaicumpa W, et al.

Acta Trop, 2019 Jun;194:82-88.
PMID: 30922801 DOI: 10.1016/j.actatropica.2019.03.026

Although several studies have reported pharmacological and immunological activity, as well as the role of black flies in transmitting pathogens to vertebrate hosts through salivary glands (SG) during blood feeding, SG proteomes of the anthropophilic black flies in Thailand have never been reported. Therefore, this study determined the SG proteomes of female S. nigrogilvum and S. nodosum. Sodium dodecylsulfate polyacrylamide gel electrophoresis (SDS-PAGE) and two-dimensional (2-DE) gels containing separated SG proteins of individual species were subjected to liquid chromatography-tandem mass spectrometry (LCMS/MS) and an orthologous protein search from eukaryotic organism, nematocera and simuliidae databases for total protein identification. SDS-PAGE and protein staining revealed at least 13 and 9 major protein bands in the SGs of female S. nigrogilvum and S. nodosum, respectively, as well as several minor ones. The 2-DE demonstrated a total of 56 and 41 protein spots for S. nigrogilvum and S. nodosum, respectively. Most of the proteins obtained in both species were enzymes involved in blood feeding, including proteases, apyrases, hyaluronidases, aminopeptidase and elastase. The results obtained in this study provided a new body of knowledge for a better understanding on the role of salivary gland proteins in these black fly species in Thailand.
Characterization of IgE-binding proteins in the salivary glands of Simulium nigrogilvum (Diptera: Simuliidae)

Hempolchom C, Sookrung N, Srisuka W, Reamtong O, Sakolvaree Y, Chaicumpa W, et al.

Parasitol Res, 2019 Aug;118(8):2353-2359.
PMID: 31263951 DOI: 10.1007/s00436-019-06383-x

Simulium dermatitis is an IgE-mediated skin reaction in animals and humans caused by the bites of black flies. Although Simulium nigrogilvum has been incriminated as the main human-biting black fly species in Thailand, information on its salivary allergens is lacking. Salivary gland extract of S. nigrogilvum females was subjected to sodium dodecylsulfate-polyacrylamide gel electrophoresis, and the separated components were applied onto nitrocellulose membranes for immunoblotting, which was performed by probing the protein blots with sera from 17 individuals who were allergic to the bites of S. nigrogilvum. IgE-reactive protein bands were characterized further by liquid chromatography-mass spectrometry (LC-MS/MS) analysis. Nine protein bands (79, 42, 32, 25, 24, 22, 15, 13, and 11 kDa) were recognized in the serum of the subjects. Four of the nine protein bands (32, 24, 15, and 11 kDa) showed IgE reactivity in all (100%) of the tested sera, and they were identified as salivary secreted antigen 5-related protein, salivary serine protease, erythema protein, and hypothetical secreted protein, respectively. Three other proteins, salivary serine protease (25 kDa), salivary D7 secreted protein (22 kDa), and hypothetical protein (13 kDa), reacted with > 50% of the sera. The relevance of the identified protein bands as allergens needs to be confirmed by using pure recombinant proteins, either in the in vivo skin prick test or in vitro detection of the specific IgE in the serum samples of allergic subjects. This will be useful for the rational design of component-resolved diagnosis and allergen immunotherapy for the allergy mediated by the bites of black flies.
Diversity of nematodes infecting the human-biting black fly species, Simulium nigrogilvum (Diptera: Simuliidae) in central Thailand

Huang F, Srisuka W, Aupalee K, Streit A, Fukuda M, Pitasawat B, et al.

Acta Trop, 2021 Dec;224:106140.
PMID: 34562429 DOI: 10.1016/j.actatropica.2021.106140

Black flies (Diptera: Simuliidae) are known as vectors of disease agents in humans and livestock, with some species being vectors of Onchocerca volvulus, the filarial nematode that is the causative agent of human onchocerciasis. Nematode infections in adult female black flies have been reported from some areas in northern and western Thailand, but not from other regions of Thailand. In this study, wild-caught adult female black flies from the central region of Thailand were examined for infections with nematodes. Collections of adult females were carried out at Khlong Lan district, Kamphaeng Phet province, central Thailand. A molecular approach, based on the mitochondrial (cox1, 12S rRNA) and nuclear (18S rRNA) genes, was used to identify the species of nematodes recovered from the specimens collected. A total of 911 wild-caught adult black flies were collected. Simulium nigrogilvum was the most abundant species (n = 708), followed by S. doipuiense complex (n = 179), S. chamlongi (n = 11), S. umphangense (n = 10), S. chumpornense (n = 1), S. multistriatum species-group (n = 1), and S. maewongense (n = 1). Nematode infections were detected in nine specimens of S. nigrogilvum, of which two were positive for filarial worms (one worm each, infection rate 0.28%) and seven were positive for non-filarial nematodes (11 worms in total, infection rate 0.99%). The two filarial nematodes (third-stage larvae) were identified molecularly as Onchocerca species type I, while the 11 non-filarial nematodes were classified into ascaridoid (n = 2), tylenchid (n = 6) and mermithid (n = 3) nematodes. The results of this study demonstrated that adult female S. nigrogilvum were parasitized with diverse nematodes (filarial and non-filarial). Detection of the infective larvae of Onchocerca sp. type I in S. nigrogilvum confirms that occurrence of zoonotic onchocerciasis is highly possible in Thailand. Additional in-depth investigation of the morphology, life cycle and host-parasite relationship of nematodes that parasitized this black fly host is still needed.
Scanning electron microscopy of antennal sensilla of the eight Anopheles species of the Hyrcanus Group (Diptera: Culicidae) in Thailand

Hempolchom C, Yasanga T, Wijit A, Taai K, Dedkhad W, Srisuka W, et al.

Parasitol Res, 2017 Jan;116(1):143-153.
PMID: 27752768

Antennal sensilla were first investigated in the eight medically and veterinary important Anopheles mosquito species (Anopheles argyropus, Anopheles crawfordi, Anopheles nigerrimus, Anopheles nitidus, Anopheles paraliae (= Anopheles lesteri), Anopheles peditaeniatus, Anopheles pursati, and Anopheles sinensis) of the Hyrcanus Group in Thailand, using scanning electron microscopy (SEM). Four types of sensilla, including sensilla chaetica (large and small), sensilla trichodea (sharp- and blunt-tipped), sensilla basiconica or grooved pegs (types I, II, and III), and sensilla coeloconica (large and small), were observed on the female antennae of the eight species. The greatest number of sensilla found along the flagellum of all the Anopheles species consisted of sensilla trichodea. Grooved pegs type II were not found on the antennae of An. peditaeniatus. Interestingly, clusters of 10-15 grooved pegs type III, with blunt-tipped and unevenly grooved-lengthwise sensilla, and a sunken group of 7-12 grooved pegs type III, with slightly curved and point-tipped sensilla, were found distally on flagellomeres 3-7 of An. argyropus and An. peditaeniatus, respectively. In addition, the key for species identification, based on fine structure and morphometrics of antennal sensilla among the eight species, was constructed and differentiated successfully. However, in order to focus intensively on the exact function of these sensilla, further electrophysiological study is needed in understanding their significant role in mosquito behavior, especially when these insects seek hosts for transmitting pathogens to humans.