<it>Vetufebrus ovatus </it>n. gen., n. sp. (Haemospororida: Plasmodiidae) vectored by a streblid bat fly (Diptera: Streblidae) in Dominican amber

1756-3305-4-229 1756-3305 Research <it>Vetufebrus ovatus </it>n. gen., n. sp. (Haemospororida: Plasmodiidae) vectored by a streblid bat fly (Diptera: Streblidae) in Dominican amber PoinarOGeorgeJrpoinarg@science.oregonstate.edu

Department of Zoology, Oregon State University, Corvallis, OR 97331, USA

Parasites & Vectors 1756-3305 2011 4 1 229 http://www.parasitesandvectors.com/content/4/1/229 2215268710.1186/1756-3305-4-229 31102011712201171220112011Poinar; licensee BioMed Central Ltd.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Dominican Republic amberFossil bat malariaVetufebrus ovatusn. gen.n. sp

Abstract

Background

Both sexes of bat flies in the families Nycteribiidae and Streblidae (Diptera: Hippoboscoidea) reside in the hair or on the wing membranes of bats and feed on blood. Members of the Nycteribiidae transmit bat malaria globally however extant streblids have never been implemented as vectors of bat malaria. The present study shows that during the Tertiary, streblids also were vectors of bat malaria.

Results

A new haemospororidan, Vetufebrus ovatus, n. gen., n. sp., (Haemospororida: Plasmodiidae) is described from two oocysts attached to the midgut wall and sporozoites in salivary glands and ducts of a fossil bat fly (Diptera: Streblidae) in Dominican amber. The new genus is characterized by ovoid oocysts, short, stubby sporozoites with rounded ends and its occurrence in a fossil streblid. This is the first haemosporidian reported from a streblid bat fly and shows that representatives of the Hippoboscoidea were vectoring bat malaria in the New World by the mid-Tertiary.

Conclusions

This report is the first evidence of an extant or extinct streblid bat fly transmitting malaria. Discovering a mid-tertiary malarial parasite in a fossil streblid that closely resembles members of a malarial genus found in nycteribiid bat flies today shows how little we know about the vector associations of streblids. While no malaria parasites have been found in extant streblids, they probably occur and it is possible that streblids were the earliest lineage of flies that transmitted bat malaria to Chiroptera.

Background

Amber is known for its ability to preserve vertebrate microbial pathogens. Thus far, there are records of malaria, leishmaniasis and trypanosomiasis associated with insect vectors in amber deposits ranging from 20 to 100 million years of age 1. Sporogonic stages of the bird malaria, Plasmodium dominicana, occurred in Culex malariager in Dominican amber 2 and developmental stages of Paleohaemoproteus burmacis (Haemospororida: Plasmodiidae) were reported from an Early Cretaceous Burmese amber biting midge (Diptera: Ceratopogonidae) 3. The present study describes the sporogonic stages of a new genus of bat malaria in a Dominican amber fossil streblid 4. Extant streblids have never been implicated as vectors of bat malaria, however members of the closely related family Nycteribiidae transmit bat malaria globally 56 (Table 1). Since both sexes of streblid bat flies (Diptera: Hippoboscoidea: Streblidae) feed on the blood of bats and reside in the hair or on the wing membranes 789, they would be excellent vectors of bat malaria.

Table 1

Hippoboscoidea vectors of malaria

Vector

Malaria type

Vertebrate

Reference

Hippoboscidae

Icosta hirsuta

Haemoproteus lophortyx

birds

I. rufiventris

H. lophortyx

birds

Lynchia hirsuta

H. lophortyx

birds

Microlynchia pusilla

H. columbae

birds

M. pusulla

H. maccallumi

birds

M. pusilla

H. sacherovi

birds

Ornithomyia avicularia

H. mansoni

birds

Ornithomyia lagopodia

H. mansoni

birds

Pseudolynchia brunnea

H. columbae

birds

P. canariensis

H. columbae

birds

P. canariensis

H. maccallumi

birds

P. capensis

H. columbae

birds

P. maura

H. columbae

birds

Stilbometopa impressa

H. lophortyx

birds

Nycteribiidae

Basilia sp.

Polychromophilus deanei

bats

Listropoda sp.

bats

Nycteribia dentata

Polychromophilus sp.

bats

N. kolenatii

P. murinus

bats

N. parvula

P. melanipherus

bats

Penicillidia fulvida

Polychromophilus sp.

bats

Penicillidia spp.

Polychromophilus sp.

bats

Methods

Specimen

The fossil streblid is in a piece of amber 5 mm long by 4 mm wide by 4 mm deep (Figure 1). Observations, drawings, and photographs were made with a Nikon SMZ-10 R stereoscopic microscope and Nikon Optiphot compound microscope with magnifications up to 600×.

Figure 1

Two oocysts

Two oocysts. Two oocysts (arrows) of Vetufebrus ovatus n. gen., n. sp. on the gut wall of a Dominican amber streblid bat fly. Bar = 272 μm.

Since it was not possible to photograph the malarial organisms without polishing away portions of the fly, photographs had to be taken through the thickness of the amber matrix as well as the width of the body wall of the vector. Adobe Photoshop was used to enlarge the photos and obtain the clearest images.

Locality

The amber with the bat fly came from La Búcara mine in the Cordillera Septentrional of the Dominican Republic. Dating of Dominican amber is still controversial with the latest purposed age of 20-15 mya based on foraminifera 10 and the earliest as 45-30 mya based on coccoliths 11. In addition, Dominican amber is secondarily deposited in sedimentary rocks, which makes a definite age determination difficult 12. A range of ages for Dominican amber is possible since the amber is associated with turbiditic sandstones of the Upper Eocene to Lower Miocene Mamey Group 13. Dominican amber was produced by the leguminous tree, Hymenaea protera Poinar 14 and a re-construction of the Dominican amber forest based on amber fossils indicated that the environment was similar to that of a present day tropical moist forest 15.

Results and Discussion

Description of malarial pathogen

Phylum Apicomplexa Levine, 1970

Class Aconoidasida Mehlhorn, Peters & Haberkorn, 1980

Order Haemospororida Danilewsky, 1885

The description is based on two oocysts and sporozoites in the oocysts and salivary glands/secretions of a fossil streblid bat fly 4.

Vetufebrus Poinar n. gen. (Figures 1, 2, 3 and 4)

Figure 2

Oocysts A and B of Vetufebrus ovatus

Oocysts A and B of Vetufebrus ovatus. Oocysts A and B of Vetufebrus ovatus n. gen., n. sp. attached to the gut wall of a Dominican amber streblid bat fly. Arrows show developing sporozoites inside oocysts. Bar = 33 μm.

Figure 3

Sporozoites (arrows) of Vetufebrus ovatus

Sporozoites (arrows) of Vetufebrus ovatus. Sporozoites (arrows) of Vetufebrus ovatus n. gen., n. sp. in salivary glands and ducts of a Dominican amber streblid bat fly. Bar = 20 μm.

Figure 4

Oocysts of Vetufebrus ovatus

Oocysts of Vetufebrus ovatus. A and B. Oocysts of Vetufebrus ovatus n. gen., n. sp. containing nucleated cells and developing sporozoites in a Dominican amber streblid bat fly. C. Sporozoites of Vetufebrus ovatus n. gen., n. sp. in a salivary gland secretion of a Dominican amber streblid bat fly. Bar = 27 μm.

Description. Oocysts small, oval, with nucleated cells 3-5 μm in diameter and developing sporozoites 7-10 μm in length; sporozoites in salivary glands and ducts stubby, with rounded ends, 8-10 μm in length; occurs in a Dominican amber streblid bat fly 4.

Type species: Vetufebrus ovatus Poinar

Vetufebrus ovatus Poinar, n. sp.

Description: Oocysts brown; oocyst A, 32 μm × 15 μm; surrounding membrane 1.2 -1.4 μm wide, containing dark nucleated cells 3-5 μm in diameter and developing sporozoites 7-10 μm in length; oocyst B, 29 μm × 17 μm, containing dark nucleated cells 3-5 μm in diameter and developing sporozoites 7-10 μm in length; surrounding membrane 1.2-1.4 μm wide; sporozoites in salivary glands/secretions short, stubby, with rounded ends, 8-10 μm in length.

Etymology: The generic name is from the Latin "vetus" for old and the Latin "febris" for fever. The specific epithet is from the Latin "ovatus" for ovate, referring to the shape of the oocysts.

Holotype. Specimen (accession # D-7-239) deposited in the Poinar amber collection maintained at Oregon State University, Corvallis, Oregon.

Locality: La Búcara amber mine (19°13' × 70°40') in the northern portion of the Dominican Republic.

Conclusions

The present study represents the first description of a haemosporidian reported from a streblid bat fly and shows that representatives of the Hippoboscoidea were vectoring bat malaria in the mid-Tertiary. The presence of sporozoites in salivary glands and ducts indicates that the streblid was a successful vector of Vetufebrus.

Bats are infected with four genera of malaria: Plasmodium, Hepatocystis, Nycteria and Polychromophilus 56. Species of the former three genera infect Old World bats while Polychromophilus occurs globally and is the only bat malaria reported from the New World 16. All known strains of Polychromophilus are vectored by nycteriibid flies of the genera Nycteribia, Penicillidia and Basilia (Table 2).

Table 2

Sporogonic stages of bat malaria in Hippoboscoidea (all Nycteriibidae except for Vetufebrus in a fossil streblid).

Malaria

Vector

Oocyst

Sporozoite

Reference

Vetufebrus ovatus

Fossil streblid

35 × 15,29 × 17

oval

7-10, stubby

ends rounded

Present study

P. deanei

Basilia sp.

60, round

8, thick

P. melanipherus

Nycteribia parvula

P. murinus

Nycteribia kolenatii

57-71, round

7.4

Polychromophilus sp.

Nycteribia dentata

7, stubby

ends rounded

Polychromophilus sp.

Penicillidia fulvida

oval, 31 × 10

57 × 47

13, thick,

blunt ends

Polychromophilus sp.

P. dufouri

P. conspicua

stubby,

blunt ends

5 13

Polychromophilus ?

Listropoda sp.

6.3, stubby,

blunt ends

5 27

All measurements in microns.

The sporogonic stages of Polychromophilus are characterized by round, slow growing oocysts attached to the midgut of the vector and short, stubby sporozoites with rounded ends 5. The mature round oocysts of Polychromophilus spp. contrast with the small oval oocysts of Vetufebrus (Table 2)(Figures 2, 4A, B). However, Adam and Landau 17 noted a small (31 × 10 μm), oval Polychromophilus oocyst in the nycteribiid fly, Penicillidia fulvida Bigot, 1889. It is likely that this oval oocyst in the nycteribiid was still developing, which could be the case with the two oocysts of Vetufebrus. While the sporozoites noted in the two oocysts of Vetufebrus are similar in size and shape to those in the salivary glands, it is possible that some of the salivary gland sporozoites originated from an earlier infection.

Short and stubby sporozoites with rounded ends as reported here for Vetufebrus (Figures 3, 4C) are characteristic of Polychromophilus infections 171819(Table 2) and the dimensions of Vetufebrus sporozoites fall within the range of some Polychromophilus spp. (Table 2). While Vetufebrus could represent an early lineage of Polychromophilus, this is unclear due to the small size of the oocysts. Also bat malaria has not been found in extant streblids even though species of the closely related Nycteribiidae carry bat malaria (Table 1). Adam & Landau 17 found no malarial stages in the streblids, Raymondia simplex Jobling 1954, R. seminuda Jobling, 1954 and R. leleupi Jobling 1954 while searching for vectors of Polychromophilus in the Congo Republic. Also, Garnham 5 found no sporogonic stages of malaria in African streblids.

In accordance with section 8.6 of the ICZN's International Code of Zoological

Nomenclature, copies of this article are deposited at the following five publicly accessible libraries: Natural History Museum, London, UK; American Museum of Natural History, New York, USA; Museum National d'Histoire Naturelle, Paris, France; Russian Academy of Sciences, Moscow, Russia; Academia Sinica, Taipei, Taiwan.

Competing interests

The author declares that they have no competing interests.

Authors' contributions

GP discovered the haemosporidian, designed and wrote the paper and supplied the figures.

Acknowledgements

I thank Alex Brown for supplying the specimen and Jake Jacobson and Roberta Poinar for commenting on earlier drafts of the manuscript.

The Origin of insect-borne human diseases as revealed in amberPoinarGJrAmer Entomologist201157170178<it>Plasmodium dominicana </it>n. sp. (Plasmodiidae: Haemospororida) from Tertiary Dominican amberPoinarGOJrSyst Parasitology200561475210.1007/s11230-004-6354-6<it>Paleohaemoproteus burmacis </it>gen. n., sp. n. (Haemospororida: Plasmodiidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae)PoinarGJrTelfordSRParasitology2005131798410.1017/S003118200500729816038399The first fossil streblid bat fly, (Diptera: Hippoboscoidea; Streblidae)PoinarGOJrBrownAESyst Parasitology2012Malaria parasites and other HaemosporidaGarnhamPCCOxford: Blackwell Scientific Publications1966Considérations sur le genre <it>Nycteria </it>(Haemoproteidae) parasite de Microchiroptères africans avec description de quatre espèces nouvellesRosinGLandauIHugotJ-PAnn Parastiologie (Paris)197853447459StreblidaeWenzelRLPetersonBVManual of Nearctic DipteraMonograph 27. Ottawa: Agriculture Canada Research BranchMcAlpine, JF1981112931301Louse flies, keds, and related flies (Hippoboscoidea)LloydJEMedical and Veterinary EntomologyNew York: Academic PressMullen G, Durden L2002349362Bat flies: Obligate ectoparasites of batsDickCWPattersonBDMicromammals and Macroparasites: From Evolutionary Ecology to ManagementToky: Springer-VerlagMorand S, Krasnov BR, Poulin R2006179194Age and Paleogeographic origin of Dominican amberIturralde-VinentMAMacPheeRDEScience19962731850185210.1126/science.273.5283.1850Das Bernstein-KabinettSchleeDStuttg Beitr Naturkunde (C)1990281100Taphonomy of fossilized resins: determining the biostratinomy of amberPoinarGOJrMastalerzMActa Geol Hisp200035171182HispaniolaDraperGMannPLewisJFCaribbean geology: an introductionKingston, Jamaica: The University of the West Indies Publishers' AssociationDonovan S, Jackson TA1994129150<it>Hymenaea protera </it>sp.n. (Leguminosae: Caesalpinoideae) from Dominican amber has African affinitiesPoinarGOJrExperientia199147107510821010.1007/BF01923347PoinarGOJrPoinarRThe Amber ForestPrinceton, NJ: Princeton Univ. Press1999<it>Polychromophilus murinus</it>: a malarial parasite of bats: life- history and ultrastructural studiesGardnerRAMolyneuxDHParasitology19889659160510.1017/S00311820000802153136420Developmental stages of <it>Polychromophilus </it>sp., a parasite of insectivorous bats from the Congo-Brazzaville, in the nycteribiid fly <it>Penicillidia fulvida </it>Bigot 1889AdamJPLandauITrans Royal Soc Trop Med Hyg19736756A contribution to the study of the haematozoon parasites of bats. A new mammalian haemoproteid, <it>Polychromophilus deanei </it>n. spGarnhamPCCLainsonRShawJJMem Inst Oswaldo Cruz19716911912510.1590/S0074-027619710001000094997955A haemosporidian of batsMerGGGoldblumNNature194715944420340259The morphology, transmission, and life-history of <it>Haemoproteus lophortyx </it>O'Roke, a blood parasite of the California Valley QuailO'RokeECUniv California Publ Zool193036151Studies on <it>Haemoproteus </it>of mourning dovesHuffCGAmer J Hyg193216618623The Hipppoboscidae or louse-flies (Diptera) of mammals and birds. Part 1. Structure, physiology and natural historyBequaertJCEntomologica Americana1953321209The transmission of <it>Haemoproteus </it>sp. of English wood-pigeons by <it>Ornithomyia avicularia</it>BakerJRJ Protozology196313406408Remarks on the avian haemoprotozoa of the genus <it>Leucocytozoon </it>DanilewskySanbonLWJ Trop Med Hyg1909123738The sporogony of <it>Haemoproteus columbae</it>AdieHIndian J Med Res19152671680Transmission of <it>Haemoproteus lophortyx </it>O'Roke of the California quail by hippoboscid flies of the species <it>Stilobometopa impressa </it>(Bigot) and <it>Lynchia hirsuta </it>FerrisTarshisIBExp Parasitol1955446449210.1016/0014-4894(55)90038-213262075Alcuni protozoi parassiti di Nycteribiidae del genere <it>Listopoda</it>CorradettiAAnn di Igiene193646444448The zoogeography of <it>Polychromophilus </it>and description of a new species of a gregarine (<it>Lankestria galliardi</it>)GarnhamPCCAnn Parasitol Hum Comp1973482312424206622<it>Polychromophilus </it>species in insectivorous batsGarnhamPCCTrans Royal Soc Trop Med Hyg19736723