Introduction
Sand flies (Diptera, Psychodidae, Phlebotominae) are biting flies involved in the transmission of pathogens, including the protozoan parasite Leishmania among human and non-human animals (Rangel and Lainson 2003).
There are approximately 1,000 valid described species of sand flies in the world of which 530 are known to occur in the Americas (Shimabukuro et al. 2017).
The aim of this work is to provide a checklist of Phlebotominae types of the Neotropical and Nearctic regions held in the collections of the Natural History Museum, London (NHMUK), together with electronic links to images of whole slides, with details of the specimen labels, plus detail images of the taxonomically informative morphological structures. This work updates the American portion of the 1990 checklist of types deposited at the NHMUK (Townsend and Lane 1990).
History of the Collection
Owing to the small size and morphological homogeneity of phlebotomine sand flies, few species were described before the turn of the 20th century. Indeed little progress in their taxonomy was made until Adler and Theodor 1926 and Theodor 1932 drew attention to the utility of various internal structures (cibarium & spermathecae) for species differentiation. Currently, taxonomically valid species descriptions of phlebotomine sand flies still rely on adult morphology. Although newer molecular techniques are increasingly used for identifying species, they have yet to be formally used as characters in species descriptions. Type specimens are confined to the adult stage, with few taxa described in the immature stages.
Significant donations to the NHM collection have come from: (i) Graham Bell Fairchild who worked on the Panamanian fauna in the 1950’s and 60’s; (ii) a number of early types described by Robert Newstead in the 1920’s when he was a Professor at the Liverpool School of Tropical Medicine; (iii) and most significantly, the collection of Oskar Theodor, which the museum purchased in 1981 after his retirement from the University of Jerusalem. The NHM has also absorbed the specimen collections of the London School of Tropical Medicine and Hygiene (LSHTM).
The main body of the NHMUK Phlebotominae collection was assembled by Dr D.J. Lewis, who though not a member of staff was based at the museum for 30 years (1956-1986) whilst in the employ of the Medical Research Council in London. All his material was mounted in Berlese media which is not a permanent mountant. There are many examples of deteriorating Lewis slides in the NHMUK collection, as well as instances where Lewis remounted other author's type specimens into Berlese. His distinctive handwriting and messy slides, often bearing multiple specimens, are instantly recognisable.
[An example of a Newstead type remounted into Berlese by D. J. Lewis, showing the characteristic darkening of the mountant as it deteriorates.]
Taxonomic treatment
Phlebotominae taxonomy has a long history of differences in opinion among experts and various conflicting classification schemes. The current situation is no exception, with both the classification of Young and Duncan 1994, which is based on the previous work of Lewis et al. 1977, and that of Galati 2003 in use at the same time for the New World fauna. Currently, the NHMUK collections are arranged according to Young and Duncan 1994, but we have used both naming systems here to reflect the current knowledge of the group.
In their 1994 guide to identification and distribution Young & Duncan adopt the classification of Lewis et al 1977 with only minor changes. They make it clear that their arrangement of taxa does not represent a phylogenetic analysis of the group, and, aside from a few comments in the notes give no information on the relationships between their subgeneric groups. It is clear their groupings have been arrived at through a phenetic review of morphological characters with no attempt made to identify any common ancestry between groups.
Lewis et al. proposed their 1977 classification at a time when those working on sand flies were faced with the choice between two family names, several subfamily names, and, for some species, three possible generic names. Their aim was to create a stable general framework with flexible subdivisions into which, recent and future ideas on the evolutionary relationships within the group, could be assimilated. They present a review of the early literature on the group and, with reference to the ICZN code, proposed the use of the family name Psychodidae (Newman 1834) and the subfamily name Phlebotominae (Rondani 1840), proposals that have been more or less universally accepted. Their proposal for the use of just five genera (Brumptomyia, Lutzomyia, Phlebotomus, Sergentomyia, and Warileya) now seems less successful.
At that time (1977) the checklist for all Phlebotominae species stood at around 600, with 290 of these in the American genus Lutzomyia. The current checklist for American sand flies alone (Shimabukuro et al 2017) stands at 530, and use of the Lewis et al 1977 concept of the genus Lutzomyia would place 495 of these taxa into a single genus. It now seems likely that, by placing the emphasis on a stable and simple classification over one that best represented the evolutionary history of the group, Lewis et al created a number of polyphyletic groups, particularly their genus Lutzomyia.
The classification of Galati (1995, 2003) is more complex with the genus Lutzomyia (as defined by Lewis et al. 1977 & Young and Duncan 1994) split into 23 genera and 22 sub-generic groupings, and has been increasingly utilised by authors working on the American fauna.
Galati’s 1995 study represented the first comprehensive attempt to perform a phylogenetic analysis of the American Phlebotominae, comprising a cladistic analysis of 88 adult morphology characters, using the Psychodidae subfamily Bruchomyiinae as the principle outgroup. The classification has since been updated by Galati in 2003 and represents our current best understanding of the evolutionary relationships within this important group.
There are some nomenclatural issues with the Galati (1995, 2003) classification as it stands at the present moment (see Shimabukuro et al 2017). Within the classification a number of family group and genus group names are attributed to Artemiev from his 1991 work (Artemiev 1991). In this work Artemiev does not accompany any of his new names with a description, that states in words characters that can be used to differentiate the taxa, thus all his new names fall fowl of ICZN Article 13a(i) and should be considered unavailable nomina nuda. Likewise there are a large number of family group and genus group names in the classification attributed to Galati from her 1995 work. In this 1995 work, though Galati maps her new taxa onto a cladogram, none of her new names are accompanied with a description in words of charatacters that can be used to distinguish them, so they too fail to conform to ICZN Article 13a(i) and should be considered unavailable nomina nuda. Galati’s 2003 work (Galati 2003) contains extensive identification keys for all the taxonomic concepts used, and all the unavailalbe names should take authorship and date from this later act of establishment under ICZN articles 50 and 21.
For a comparison of how the Galati 2003 and Young & Duncan 1994 classifications relate to each other go to the classifications comparison tab in the main menu.
Material and Methods
Checklist
The list contains information compiled from the exam of Nearctic and Neotropical species of sand flies from the Diptera Collection at the NHMUK.
The checklist is arranged according to the classification of Galati 2003, and subgenera, species groups/series and species are listed alphabetically within each genus.
We have excluded from this catalogue two NHMUK specimens bearing “type” labels, for which we can find no record of the given species name in the literature. One labeled as the holotype of Lutzomyia witremundoi (author Feliciangeli), the other labeled as a paratype of L. patiñoi (authors Mangabeira & Galindo). It seems probable that these are unpublished manuscript names, and are therefore unavailable under article 8 of the ICZN code, http://iczn.org/code .
Specimen Images
Photographs were taken with an Olympus BX63-CBH microscope equipped with a DP73 camera, and differential interference contrast (DIC) ilumination. The images were edited in the Cellsens software and stacked images were produced by HeliconFocus 6 software. Whole slide scans were generated using a SatScan instrument at x5 magnification, and images were cropped and processed using the Inselect software, version 0.1.35, available from the Natural History Museum https://naturalhistorymuseum.github.io/inselect/.
Data resources
Most of the original species descriptions are still under copyright to their original publisher. The bibliographical and historical database of scientific articles on leishmaniases and sandflies hosted by the Laboratoire de Parasitologie at the University of Montpellier is an extremely useful resource http://www.leishpub.univ-montp1.fr/
The specimen images are available on the NHM data portal: https://doi.org/10.5519/0051226
The Checklist
This checklist includes 60 species of Phlebotominae, distributed among 17 genera. A total of 176 primary and secondary type specimens were examined and photographed, generating 779 photographs of taxonomically informative adult structures, together with 189 whole slide scans showing details of the slide labelling (where the reverse of a slide had labels attached a scan of the reverse is included).
Acknowledgments
We would like to thank the Sackler Biodiversity Imaging Laboratory (SBIL), NHM, especially Rebecca Summerfield and Dr. Vladimir Blagoderov. Dr Ben Price at the NHM for help with the whole slide scanning, and Ben Scott for help with the Scratchpads website. PHFS would like to thank the British Council/Travel Links (127558970) for funding.