Skip to main content
Log in

Two new phlebotomine sandflies (Diptera: Psychodidae) from the forest edge in Madagascar: the anthropophilic Phlebotomus artemievi sp. nov. and Sergentomyia maroantsetra ensis sp. nov.

  • Arthropods and Medical Entomology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A few data are related to the anthropophily of Malagasy Phlebotomine sandflies. Prior studies focussed mainly to inventories and description of new species. Our goal was to emphasize the anthropophily of Malagasy Phlebotomine sandflies. We worked in the Makira region, using two simultaneous methods: human landing catches (HLC) and CDC light traps. We collected sandflies in three rural communities adjacent to the Makira Natural Park. In each community, three different biotopes were sampled: within community settlements; at the edge of forest, typically in agricultural land; and within the forest. We collected 61 sandflies belonging to two new species presently described: Phlebotomus artemievi sp. nov. and Sergentomyia maroantsetraensis sp. nov. These sandflies were caught exclusively in the forest edge biotope. None were captured within communities or within forests. HLC provided 97% of the collected sandflies, corresponding to a human-biting rate of 15 females per human per night. CDC provided only two females. Ph. artemievi sp. nov. was predominantly captured by HLC and appears to be highly anthropophilic. Here, we update the behavioural ecology of sandflies and describe two new species. Further research is required to understand their vector competence and their ability to transmit arboviruses and other pathogens such as Leishmania.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Data availability

The whole datasets provided and analysed during this study are publicly available. Please contact Fano José Randrianambinitsoa and Jérôme Dépaquit.

Abbreviations

CDC:

Centers for Disease Control

HLC:

Human Landing Catches

a.m.:

ante meridian

p.m.:

post meridian

a.s.l.:

above sea level

DNA:

DesoxyriboNucleic Acid

kDNA:

kinetoplast DesoxyriboNucleic Acid

mtDNA:

mitochondrion DesoxyriboNucleic Acid

rDNA:

ribosomal DesoxyriboNucleic Acid

cyt b:

cytochrome b

ITS2:

second Internal Transcribed Spacer

28S:

28 subunit

PNOC:

prepronociceptin

PNOCF:

PNOC Forward

PNOCR:

PNOC Reverse

PCA:

Principal Component Analysis

References

  • Abonnenc E (1969) Sur Phlebotomus squamipleuris Newstead, 1912 et espèces voisines (Diptera: Psychodidae) Cah ORSTOM, Sér Ent Méd Parasitol 7(4):307-323

  • Adams D, Collyer M, Kaliontzopoulou A (2019) Geomorph: Software for geometric morphometric analyses. R package version 3.1.0. https://cran.r-project.org/packages=geomorph

  • Balbino V, Coutinho-Abreu I, Sonoda I, Marques da Silva W, Marcondes C (2005) Phlebotomine sandflies (Diptera: Psychodidae) of the Atlantic forest in Recife, Pernambuco state, Brazil: the species coming to human bait, and their seasonal and monthly variations over a 2-year period. Ann Trop Med Parasitol 99:683–693. https://doi.org/10.1179/136485905X65116

    Article  CAS  PubMed  Google Scholar 

  • Blavier A, Laroche L, Randrianambinintsoa FJ, Lucas V, Gantier JC, Léger N, Robert V, Depaquit J (2019) Phlebotomine sandflies (Diptera, Psychodidae) from the Ankarana tsingy of northern Madagascar: inventory and description of new taxa Parasite 26:38. https://doi.org/10.1051/parasite/2019039

  • Bonfield J, Staden R (1996) Experiment files and their application during large-scale sequencing projects. DNA Seq 6(2):109–117. https://doi.org/10.3109/10425179609010197

    Article  CAS  PubMed  Google Scholar 

  • Buck G, Courdurier J, Dorel R, Quesnel JJ (1951) Premier cas de Leishmaniose canine à Madagascar. Bull Soc Pathol Exot 44:428–430

    CAS  Google Scholar 

  • Campbell-Lendrum D, Pinto M, Brandao-Filho S, de Souza A, Ready P, Davies C (1999) Experimental comparison of anthropophily between geographically dispersed populations of Lutzomyia whitmani (Diptera: Psychodidae). Med Vet Entomol 13(3):299–309. https://doi.org/10.1046/j.1365-2915.1999.00174.x

    Article  CAS  PubMed  Google Scholar 

  • Clerc Y, Rodhain F, Digoutte JP, Tesh R, Heme G, Randriarinoro J (1982) The Perinet virus, Rhabdoviridae, of the Vesiculovirus type isolated in Madagascar from Culicidae. Arch Inst Pasteur Madagascar 49(1):119–129

    CAS  PubMed  Google Scholar 

  • Depaquit J (2014) Molecular systematics applied to Phlebotomine sandflies: review and perspectives. Infect Genet Evol 28:744–756. https://doi.org/10.1016/j.meegid.2014.10.027

    Article  PubMed  Google Scholar 

  • Depaquit J, Ferté H, Léger N, Killick-Kendrick R, Rioux JA, Killick-Kendrick M, Hanafi HA, Gobert S (2000) Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses Of dispersion and speciation. Insect Mol Biol 9(3):293–300. https://doi.org/10.1046/j.1365-2583.2000.00179.x

    Article  CAS  PubMed  Google Scholar 

  • Depaquit J, Léger N, Robert V (2002) Première mention de Phlebotomus à Madagascar (Diptera: Psychodidae). Description de Phlebotomus (Anaphlebotomus) fertei n. sp. et de Phlebotomus (Anaphlebotomus) huberti n. sp. Parasite 9:325-331. https://doi.org/10.1051/parasite/2002094325

  • Depaquit J, Léger N, Ferté H, Robert V (2004) Phlebotomus from Madagascar (Diptera: Psychodidae). II-description of the female Phlebotomus (Anaphlebotomus) fertei Depaquit, Léger & Robert, 2002; description of the male and new data for the female Phlebotomus (Anaphlebotomus) berentiensis (Léger & Rodhain, 1978) comb. nov. Parasite 11:201–209. https://doi.org/10.1051/parasite/2004112201

    Article  CAS  PubMed  Google Scholar 

  • Depaquit J, Léger N, Robert V (2007) Les phlébotomes de Madagascar (Diptera: Psychodidae). V-. Description de Sergentomyia majungaensis n. sp. Parasite 14:219-223. https://doi.org/10.1051/parasite2007143219

  • Depaquit J, Léger N, Robert V (2008) Les Phlébotomes de Madagascar (Diptera : Psychodidae). VI – Un sous-genre nouveau (Vattieromyia) avec trois espèces nouvelles : Sergentomyia (Vat.) sclerosiphon, Se. (Vat.) namo et Se. (Vat.) anka Parasite 15:15-26. https://doi.org/10.1051/parasite/2008151015

  • Dépaquit J, Grandadam M, Fouque F, Andry P, Peyrefitte C (2010) Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: a review. Euro Surveill 15(10):19507

    PubMed  Google Scholar 

  • Depaquit J, Léger N, Randrianambinintsoa FJ (2015) Paraphyly of the subgenus Anaphlebotomus and creation of Madaphlebotomus subg. Nov. (Phlebotominae: Phlebotomus). Med Vet Entomol 29(2):159–170. https://doi.org/10.1111/mve.12098

    Article  CAS  PubMed  Google Scholar 

  • Despommier D, Ellis B, Wilcox B (2006) The role of ecotones in emerging infectious diseases. EcoHealth 3(4):281–289. https://doi.org/10.1007/s10393-006-0063-3

    Article  PubMed Central  Google Scholar 

  • Donque G (1975) Contribution géographique à l'étude du climat de Madagascar. Université de Madagascar, Antananarivo

    Google Scholar 

  • Dujardin JP (2008) Morphometrics applied to medical entomology. Infect Genet Evol 8(6):875–890. https://doi.org/10.1016/j.meegid.2008.07.011

    Article  PubMed  Google Scholar 

  • Dujardin JP, Le Pont F, Matias A, De la Riva JX (2005) Morphometrical evidence for speciation within Bolivian Lutzomyia aragaoi (Diptera: Psychodidae). Infect Genet Evol 5(4):362–365. https://doi.org/10.1016/j.meegid.2004.12.002

    Article  PubMed  Google Scholar 

  • Esseghir S, Ready PD (2000) Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biol J Linn Soc 70(2):189–219. https://doi.org/10.1111/j.1095-8312.2000.tb00207.x

    Article  Google Scholar 

  • Esseghir S, Ready PD, Killick-Kendrick R, Ben-Ismail R (1997) Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol Biol 6(3):211–225. https://doi.org/10.1046/j.1365-2583.1997.00175.x

    Article  CAS  PubMed  Google Scholar 

  • Fontenille D (1989) Transmission cycles of arboviruses in Madagascar. Arch Inst Pasteur Madagascar 55(1):1–317

    CAS  PubMed  Google Scholar 

  • Galati E, Galvis-Ovallos F, Lawyer P, Leger N, Depaquit J (2017) An illustrated guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psychodidae). Parasite 24:26. https://doi.org/10.1051/parasite/2017027

    Article  PubMed  PubMed Central  Google Scholar 

  • Grjebine A (1953) Observations sur les Nématocères vulnérants de Madagascar, régions de Majunga et de la Mandraka. Mem Inst Sci Madagascar, série E 4:443–503

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Haouas N, Pesson B, Boudabous R, Dedet JP, Babba H, Ravel C (2007) Development of a molecular tool for the identification of Leishmania reservoir hosts by blood meal analysis in the insect vectors. Am J Trop Med Hyg 77(6):1054–1059. https://doi.org/10.4269/ajtmh.2007.77.1054

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape spliting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174

    Article  CAS  Google Scholar 

  • Humbert H (1954) Les Territoires Phytogéographiques de Madagascar. Leur Cartographie Colloque sur les Régions Ecologiques du Globe Annales de Biologie (Paris) 31:195–204

  • Kasap ÖE, Belen A, Kaynas S, Simsek FM, Biler L, Ata N, Alten B (2009) Activity patterns of sand Fly (Diptera: Psychodidae) species and comparative performance of different traps in an endemic cutaneous Leishmaniasis focus in Cukurova plain, southern Anatolia, Turkey. Acta Vet Brno 78:327–335. https://doi.org/10.2754/avb200978020327

    Article  Google Scholar 

  • Koechlin J, Guillaumet J-L, Morat P (1974) Flore et végétation de Madagascar. J. Cramer, Vaduz

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Léger N, Rodhain F (1978) Sergentomyia berentiensis n. sp. (Diptera, Psychodidae). Description à partir d'un exemplaire femelle récolté à Madagascar. Bull Soc Pathol Exot 71:476–479

    Google Scholar 

  • Léger N, Rodhain F, Coulanges P, Clerc Y, Ranaivosata J (1980) Présence de phlébotomes Anthropophiles à Madagascar. Arch Inst Pasteur Madagascar 47:249–250

  • Léger N, Depaquit J, Robert V (2005) Les Phlébotomes de Madagascar (Diptera : Psychodidae). IV - Description de Sergentomyia (Rondanomyia) goodmani n. sp. Rétablissement du sous-genre Rondanomyia Theodor Parasite 12:51-57.https://doi.org/10.1051/parasite/2005121051

  • Newstead R (1912) Notes on Phlebotomus, with descriptions of new species. Part I. Bull Entomol Res 3:361–367

    Article  Google Scholar 

  • Oguz G, Kasap OE, Alten B (2017) Wing morphology variations in a natural population of Phlebotomus tobbi. Adler and Theodor 1930. J Vector Ecol 42(2):223–232. https://doi.org/10.1111/jvec.12262

    Article  PubMed  Google Scholar 

  • Pinto MC, Campbell-Lendrum DH, Lozovei AL, Teodoro U, Davies CR (2001) Phlebotomine sandfly responses to carbon dioxide and human odour in the field. Med Vet Entomol 15(2):132–139. https://doi.org/10.1046/j.1365-2915.2001.00294.x

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818. https://doi.org/10.1093/bioinformatics/14.9.817

    Article  CAS  PubMed  Google Scholar 

  • Prudhomme J, Cassan C, Hide M, Toty C, Rahola N, Vergnes B, Dujardin J-P, Alten B, Sereno D, Bañuls A-L (2016) Ecology and morphological variations in wings of Phlebotomus ariasi (Diptera: Psychodidae) in the region of Roquedur (Gard, France): a geometric morphometrics approach. Parasit Vectors 9:578. https://doi.org/10.1186/s13071-016-1872-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Randrianambinintsoa FJ (2013) Inventory and systematics of phlebotomine sandflies (Psychodidae – Phlebotominae) from Madagascar  and neighboring islands. Dissertation, University of Reims Champagne-Ardenne, France. http://www.theses.fr/2013REIMP206

  • Randrianambinintsoa FJ, Depaquit J (2013) Phlebotomine sand flies from Madagascar (Diptera: Psychodidae). VIII – Phlebotomus (Anaphlebotomus) vincenti n. sp. Bull Soc Pathol Exot 106(3):206–211. https://doi.org/10.1007/s13149-013-0305-x

    Article  CAS  PubMed  Google Scholar 

  • Randrianambinintsoa F, Depaquit J, Brengues C, Dhondt C, Yahaya I, Ouledi A, Léger N, Robert V (2012) First record of Phlebotomine sandflies (Diptera: Psychodidae) in the Comoros archipelago with description of Sergentomyia (Vattieromyia) pessoni n. sp. and Se. (Rondanomyia) goodmani comorensis n. ssp. Parasite 19(3):195–206. https://doi.org/10.1051/parasite/2012193195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randrianambinintsoa FJ, Léger N, Robert V, Depaquit J (2013) Phlebotomine sand flies from Madagascar (Diptera: Psychodidae). VII. An identification key for Phlebotomus with the description of Phlebotomus (Anaphlebotomus) vaomalalae n. sp. Parasite 20:6. https://doi.org/10.1051/parasite/2013005

  • Randrianambinintsoa FJ, Léger N, Robert V, Depaquit J (2014) Paraphyly of the subgenus Sintonius (Diptera, Psychodidae, Sergentomyia): status of the Malagasy species. Creation of a new subgenus and description of a new species. PLoS One 9(6):e98065. https://doi.org/10.1371/journal.pone.0098065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randrianambinintsoa FJ, Robert V, Blavier A, Leger N, Depaquit J (2020) Two new Phlebotomine sandfly species (Diptera: Psychodidae) from the highlands of Madagascar. Acta Trop 202:105260. https://doi.org/10.1016/j.actatropica.2019.105260

    Article  CAS  PubMed  Google Scholar 

  • Raynal J, Le Gac P (1937) Phlébotomes dans le nord de Madagascar, Phlebotomus squamipleuris Newstead 1912. Bull Soc Pathol Exot 30:76–90

    Google Scholar 

  • Rodgers MR, Popper SJ, Wirth DF (1990) Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp Parasitol 71:267–275

    Article  CAS  Google Scholar 

  • Rodrigues de Oliveira A, Pinheiro GRG, Tinoco HP, Loyola ME, Coelho CM, Dias ES, Monteiro ÉM, de Oliveira Lara E Silva F, Pessanha AT, Souza AGM, Pereira NCL, Gontijo NF, Fujiwara RT, Alves da Paixão T, Santos RL (2019) Competence of non-human primates to transmit Leishmania infantum to the invertebrate vector Lutzomyia longipalpis. PLoS Negl Trop Dis 13(4):e0007313. https://doi.org/10.1371/journal.pntd.0007313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohlf FJ (2015) The tps series of software. Hystrix. It J Mamm 26(1):9–12. https://doi.org/10.4404/hystrix-26.1-11264

    Article  Google Scholar 

  • Rondani C (1840) Sopra una specie di Insetto Diptero. Memoria prima per servire alla Ditterologia italica. Parma 13

  • Savage AF, Robert V, Goodman SM, Raharimanga V, Raherilalao MJ, Andrianarimisa A, Ariey F, Greiner EC (2009) Blood parasites in birds from Madagascar. J Wildl Dis 45:907–920

    Article  Google Scholar 

  • Sawalha SS, Shtayeh MS, Khanfar HM, Warburg A, Abdeen ZA (2003) Phlebotomine sand flies (Diptera: Psychodidae) of the Palestinian West Bank: potential vectors of leishmaniasis. J Med Entomol 40(3):321–328. https://doi.org/10.1603/0022-2585-40.3.321

    Article  PubMed  Google Scholar 

  • Team RDC (2018) R: a language and environment for statistical computing. R Foundation Statistical Computing. http://www.R-project.org

Download references

Acknowledgements

We thank Dr. Benjamin Rice for critical reading of the manuscript. We would like to thank the Madagascar Health and Environmental Research (MAHERY) team and the Institut Pasteur of Madagascar for all of their logistical and intellectual support. We would also like to thank the residents of all communities in which we worked for hosting us during our research missions.

Funding

Field data collection was funded by the Madagascar Health and Environmental Research (MAHERY) team and the Institut Pasteur de Madagascar.

Author information

Authors and Affiliations

Authors

Contributions

FJR, VR, JD, and MLT wrote the first draft of the paper. FJR, JPM, and JD performed the morphological, molecular identification of the Phlebotomine sandflies in laboratory. MLT and CDG captured Phlebotomine sandflies in the field. CDG and SB facilitated the field study. FJR, JPM, JD, and VR facilitated the laboratory study. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fano José Randrianambinintsoa.

Ethics declarations

Conflict of interests

The authors declare that they have no competing interests.

Declarations

Ethics approval and consent to participate: Institutional Ethical Clearance for the Phlebotomine sandflies collection had been obtained from the Harvard TH Chan School of Public Health (IRB# 14–0127), Office of Human Research Administration 90 Smith Street, 3rd Floor Boston, MA 02215.

Additional information

Section Editor: Domenico Otranto

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Randrianambinintsoa, F.J., Depaquit, J., Martinet, JP. et al. Two new phlebotomine sandflies (Diptera: Psychodidae) from the forest edge in Madagascar: the anthropophilic Phlebotomus artemievi sp. nov. and Sergentomyia maroantsetra ensis sp. nov.. Parasitol Res 119, 1177–1199 (2020). https://doi.org/10.1007/s00436-020-06639-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06639-x

Keywords

Navigation