Share this article    

       

       

Eutrombicula tinami (Oudemans, 1910) (Trombidiformes: Trombiculidae) in Brazil: a neglected ectoparasite of several animals including humans

Bassini-Silva, Ricardo1 ; de Castro Jacinavicius, Fernando2 ; Pinter, Adriano3 ; Fournier, Gislene F. S. R.4 ; Lugarini, Camile5 ; Ferreira, Ariane6 ; Moreira-Lima, Luciano7 ; Hingst-Zaher, Erika8 ; Welbourn, Cal9 ; Ochoa, Ron10 and Moraes Barros-Battesti, Darci11

1Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo-FMVZ-USP, São Paulo, SP, Brazil.
2Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo-FMVZ-USP, São Paulo, SP, Brazil & Laboratório Especial de Coleções Zoológicas, Instituto Butantan, São Paulo, SP; Brazil.
3Superintendência de Controle de Endemias-SUCEN, São Paulo, SP, Brazil.
4Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo-FMVZ-USP, São Paulo, SP, Brazil.
5Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio, Florianópolis, SC, Brazil.
6Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil.
7Museu Biológico, Instituto Butantan, São Paulo, SP, Brazil.
8Museu Biológico, Instituto Butantan, São Paulo, SP, Brazil.
9Florida State Collection of Arthropods, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Gainesville, FL, USA.
10Systematic Entomology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, USA.
11✉ Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo-FMVZ-USP, São Paulo, SP, Brazil & Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias-UNESP, Jaboticabal, SP, Brazil.

2019 - Volume: 59 Issue: 4 pages: 412-423

https://doi.org/10.24349/acarologia/20194343

Original research

Keywords

Chiggers ectoparasites distribution hosts mammals birds trombiculiasis

Abstract

The genus Eutrombicula comprises ca. 80 species worldwide, some of which have been reported as causative agents of severe irritation to the host’s skin, known as trombiculiasis. Six species of Eutrombicula have been recorded from Brazil until present, with two reports of humans as hosts. In this study, Eutrombicula tinami (Oudemans) is redescribed and new records for the states of Minas Gerais, Rio de Janeiro, Santa Catarina and São Paulo as well as new parasite-host associations with Columbiformes, Cuculiformes, Passeriformes, Tinamiformes, Carnivora, Didelphimorphia and Lagomorpha are listed. Besides that, a two detailed report cases of trombiculiasis is provided.


Introduction

Some non-host specific chigger genera (Trombidiformes: Trombiculidae, Leeuwenhoekiidae and Walchiidae) parasitize several vertebrates groups, including humans (Shatrov 2000). Infestation by these mites can causes severe itching known as trombiculiasis, and there is also a possibility disease transmission (Mullen and OConnor 2002). One genus is Eutrombicula Ewing, 1938 with more than 80 species, six of which are recorded in Brazil: Eutrombicula alfreddugesi (Oudemans, 1910), Eutrombicula batatas (Linnaeus, 1758), Eutrombicula bruyanti (Oudemans, 1910), Eutrombicula daemoni (Bassini-Silva and Jacinavicius, 2018), Eutrombicula goeldii (Oudemans, 1910) and Eutrombicula tinami (Oudemans, 1910) (Stekolnikov and González-Acuña 2010; Bassini-Silva et al. 2018, Jacinavicius et al. 2018a).

The Neotropical species E. tinami, was described from Brazil by Oudemans (1910) and later recorded from Panama (Brennan and Lukoschus 1971), Surinam (Brennan and Lukoschus 1971) and Venezuela (Brennan and Reed 1974), parasitizing birds, rodents and marsupials (Oudemans 1910; Brennan and Lukoschus 1971; Brennan and Reed 1974; 1975; Jacinavicius et al. 2018a).

In the northern region of Brazil, locals use the term `micuim' for chiggers, but in the southern region, there is no common name, suggesting most Brazilians including the medical community are unaware of chigger and their medical importance.

Here we redescribe E. tinami, with new locality and host records as well as new human trombiculiasis records.

Material and methods

The Instituto Butantan houses the Acari Collection (IBSP) that receives material from various parts of the country. Specimens deposited in this collection are regularly prepared for identification. Of these, two hundred chiggers belonging to the genus Eutrombicula, previously stored in Ethanol (100%) were slide-mounting in Hoyer's medium and some were prepared for scanning electron microscopy (SEM), both preparations according to Walter and Krantz (2009). Drawings were made with a Leica DFC 500 microscope. Extended focal range images were composed with Leica Application Suite version 2.5.0. The scanning electron microscope photographs were obtained using a Digital FEI-Quanta 250 at the Laboratório de Biologia Celular, Instituto Butantan, São Paulo. The distribution map was prepared using DIVAGIS. All the images were prepared with Adobe Photoshop v. 13.0 and Inkscape V.2. Species identifications involved using the key by Brennan and Reed (1974), and original species descriptions. Additional sources included redescriptions of Eutrombicula by Oudemans (1912), Jenkins (1949) as well as illustrations by Brennan and Reed (1974). The terminology follows Bassini-Silva et al. (2018) and Jacinavicius et al. (2018b).

In the present study we also report the parasitism by E. tinami on two humans, one male 39 y/o and other female 31y/o, who were walking in the Atlantic Rain Forest (45°19'28'' W, 23°33'42'' S) between 9 am and 12 pm on an unspecified day November 2014.

Results

Systematics

The chigger specimens were identified as E. tinami (Oudemans, 1910). Additional specimens from Minas Gerais, Rio de Janeiro, Santa Catarina and São Paulo states were studied and used to improve the redescripition of E. tinami presented below.

Eutrombicula tinami (Oudemans, 1910)

Microthrombidium tinami Oudemans 1910: 84; 1912: 24.

Trombicula tinami: Methlagl 1928: 216, 223 and 224; Ewing 1931: 10.

Eutrombicula tinami: Ewing 1938: 294: Radford, 1942: 67; Fuller, 1952: 133; Brennan and Lukoschus 1971: 44; Brennan and Reed 1974: 710; Brennan and Reed 1975: 52; Loomis and Wrenn, 1984: 158; Jacinavicius et al. 2018a: 9.

Otonyssus tinami: Buitendijk 1945: 338.

Eutrombicula (Eutrombicula) tinami: Vercammen-Grandjean 1965: 32.

Larva

(Figures 1–5, Tables 1 and 2)

Figure 1. Morphological details of Eutrombicula tinami (Oudemans, 1910): A – ventral view of palptarsus; B – dorsal view of gnathosoma; symbols: ω = solenidion of palptarsus; ζ = subterminal eupathid of palptarsus; Od = odontus. Scales: A and B 50 μm.

Diagnosis — Palptibia with nude dorsal and lateral setae, and a branched ventral seta; adoral setae nude; odontus bifurcate with the inner prong smaller than the outer prong; the first row (C) of dorsal opisthosoma setae with 8 setae; the second row (D) with 6 setae; tarsus of leg I with a ε distal to ω, tibia of the leg III with one mastiseta.

Redescription based on examined material (Figures 1-5)

Gnathosoma — palp setal formula B/B/NNB/7Bζω; odontus (= palpal claw) bifurcate; cheliceral blade with tricuspid cap; gnathobase punctate; subcapitular setae branched, elcp not observed (Figs. 1A-B and 5A), adoral (= galeal) setae nude (Fig. 1B).

Figure 2. Morphological details of Eutrombicula tinami (Oudemans, 1910): A – prodorsal sclerite; symbols: ve = external vertical setae; se = external scapular setae; vi = internal vertical setae; si = internal scapular trichobothridial setae. Scales: 50 μm.

Idiosoma — eyes 2/2 set in an ocular plate, anterior eye larger; prodorsal sclerite (= scutum) with 1 pair of flagelliform trichobothridial (= sensilla) setae (si) with widely distributed long and slender setules, and 5 normal setae (a pair of ve (= AL), a pair of se (= PL) and a single vi (= AM) seta), se \textgreater ve \textgreater si \textgreater vi; the anterior margin of the prodorsal sclerite slightly undulating, and the lateral margins slightly concave posteriorly, posterior margin convex (Figs. 2A and 5C). Thirty four opisthosomal setae, dorsal opisthosoma with 4 pairs of setae in the C row, with the c4 pair in an anterior position (= humeral setae), D row with 3 pairs of setae, E row with 1 pair of setae, F row with 1 pair of setae, totaling 18 dorsal opisthosomal setae, and 16 ventral opisthosomal setae (10 setae anterior to the anus and 6 setae posterior) (Figs 3A-B, 5B). Two pairs of sternal setae (1a, 3a) between coxal fields.

Figure 3. Morphological details of Eutrombicula tinami (Oudemans, 1910); A – dorsal view of idiosoma; B – ventral view of idiosoma. Solid circles = ventral setae; open circles = dorsal setae. Symbols: c1-c4 = C row setae; d1-d3 = D row setae; e1 = E row setae; f1 = F row; 1a = anterior sternal setae; 3a = posterior sternal setae; 1b = coxal field I seta; 2b = coxal field II seta; 3b = coxal field III seta. Scales: A and B 100 μm.

Table 1. Standard measurements of Eutrombicula tinami (n=30).

Legs — femur legs I-III each divided into a basifemur and telofemur, each leg terminated with a pair of claws and a claw-like empodium, without onychotriches, coxal fields striate. Leg I - coxal field with 1 branched seta 1b (1B), elcI not observed; trochanter 1B; basifemur 1B; telofemur 5B; genu 4B, 3 σ with κ; tibia 8B, 2 φ with κ; tarsus 21B, with ω, ε, dorsal eupathidium (ζ') with a companion seta z and terminating with a subterminal eupathidium (ζ''), base of famulus (ε) distal to ω (Figs. 4A). Leg II - coxal field seta 2b (1B); trochanter 1B; basifemur 2B; telofemur 4B; genu 3B, σ; tibia 6B, 2 φ; tarsus 15B, with ω, ε, and subterminal eupathidium (ζ), base of ε proximal to ω (Fig. 4B). Leg III - coxal field seta 3b (1B) on anterior margin, trochanter 1B; basifemur 2B; telofemur 3B; genu 3B, σ, tibia 6B, φ; tarsus 14B and one mastiseta (Figs. 4C and 5E).

Figure 4. Morphological details of Eutrombicula tinami (Oudemans, 1910); A – Leg I; B – Leg II; C – Leg III. Solid circles = ventral leg setae; open circles = dorsal leg setae; symbols: ζ’ = dorsal eupathid tarsus leg I; ζ”, ζ = subterminal eupathid tarsus legs I and II, respecively; ω = solenidion tarsus legs I and II; σ, σ’,σ” and σ’’’ = solenidia on the genu of legs I, II and III; κ = microsetae on genu and tibia of leg I; φ, φ', φ" = solenidia on tibiae legs I, II and III; ε = famulus on tarsi of legs I and II; z = companion seta on tarsi of leg I; 1b = coxal field I seta; 2b = coxal field II seta; 3b = coxal field III seta; MTa = mastisetae on tarsus leg III. Scales: A-C 50 μm.

Figure 5. Scanning electron micrographs of Eutrombicula tinami (Oudemans, 1910); A – ventral view of palptarsus; B – dorsal view of idiosoma; C – prodorsal sclerite; D – genu of leg I; E – genu, tibia and tarsus of the leg III. Symbols: ω = palptarsal solenidion; ζ = palptarsal subterminal eupathid; c1-c4 = C row setae; d1-d3 = D row setae; e1 = E row setae; f1 = F row setae; ve = external vertical setae; se = external scapular setae; vi = internal vertical setae; si = internal scapular trichobothridial setae; σ = solenidia on genu of legs I and III; κ = microsetae on genu of leg I; φ = solenidia on tibiae legs III; MTa = mastisetae on the tarsi legs III. Scales: A and D 20 μm; B 100 μm; C and E 50 μm.

Table 2. Standard measurements of Eutrombicula tinami (n=30).

Distribution (Figure 6) — Minas Gerais (MG) state - Abaeté (45º26'44'' W, 19º09'36'' S); Fazenda Continente, Coronel Pacheco (43º15'56'' W, 21º35'17'' S); Rio de Janeiro state - Angra dos Reis (44º19'04'' W, 23º00'24'' S); Paraty (44º42'46'' W, 23º13'04'' S); Santa Catarina state - Estação Ecológica de Carijós, Florianópolis (48°30'37'' W, 27°27'54'' S); Reserva Biológica Marinha do Arvoredo, Florianópolis (48°21'23'' W, 27°17'57'' S); São Paulo state - Caraguatatuba (45°19'28''W, 23°33'42''S); Reserva Florestal do Morro Grande, Cotia (46°57'48'' W, 23°43'48'' S); Vila Verde condominium, Itapevi (46°57'41'' W, 23°34'47'' S); Sabaúna district, Mogi das Cruzes (46°05'16'' W, 23°29'02'' S); Barra do Una, Peruíbe (47º04'59'' W, 24º27'01'' S); Água doce, Piedade (47º25'40'' W, 23º42'43'' S); Santos (46º20'00'' W, 23º57'39'' S); Água Funda neighborhood, São Paulo (46º37'24'' W, 23º38'04'' S); Instituto Butantan, São Paulo (46°43'21'' W, 23°33'56'' S); Serra da Cantareira, São Paulo (46°31'38'' W, 23°22'44'' S); Vila Albertina neighborhood, São Paulo (46º41'30'' W, 23º30'04'' S).

Figure 6. Geographical distribution of Eutrombicula tinami (Oudemans, 1910) in Brazil. The yellow dot represents a literature record, and red dots are new records.

Type depository — According to the original description and Jacinavicius et al. (2018a), the types for this species are deposited at the Naturalis Biodiversity Center, Leiden, Netherlands [formerly Rijksmuseum van Natuurlijke Historie], but Fuller (1952) reported the types were deposited in the Muséum National d'Histoire Naturelle, Paris, France, however they not available for this study.

Material examined from Brazil

Mammals

Five larvae (IBSP 1648), Santos, São Paulo (SP), 26-II-1939, Homo sapiens L. (Primates: Hominidae), Dr. Tuffy and A. T. Leão coll.; 3 larvae (IBSP 12522), Caraguatatuba, SP, XI-2014, same host, G. F. S. R. Fournier and A. Pinter coll.; 1 larva (IBSP 4673), Instituto Butantan, São Paulo, SP, 1940, same host, A. T. Leão coll.; 1 larva (IBSP 1975), Serra da Cantareira, SP, 12-VIII-1940, Nasua nasua L. (Carnivora: Procyonidae), N. Bolognani coll.; 1 larva (IBSP 1680), Vila Albertina neighborhood, São Paulo, SP, 25-II-1938, Didelphis aurita Wied-Neuwied (Didelphimorphia: Didelphidae), L. F. Martins coll.; 4 larvae (IBSP 10541), Barra do Una, Peruíbe, SP, 05-XI-2010, same host, F. Nieri-Bastos coll.; 2 larvae (IBSP 352), Instituto Butantan, São Paulo, SP, 24-V-1933, same host; 1 larva (IBSP 11255), Vila Verde condominium, Itapevi, SP, 13-XII-2012, same host, F. C. Jacinavicius coll.; 6 larvae (IBSP 10551), same locality and host, 29-IV-2011, A. Marcili coll.; 4 larvae (IBSP 340), Instituto Butantan, São Paulo, SP, 22-X-1933, Sylvilagus brasiliensis (L.) (Lagomorpha: Leporidae); 3 larvae (IBSP 353), same locality and host, 21-V-1932; 1 larva (IBSP 581), same locality and host, VII-1931; 4 larvae (IBSP 1654), Água Funda neighborhood, São Paulo, SP, 07-III-1939, Hydrochoerus hydrochaeris L. (Rodentia: Caviidae), Dr. Vallejo coll.; 1 larva (IBSP 10535C), Serra da Cantareira, São Paulo, SP, 12-IV-2011, Euryoryzomys russatus (Wagner) (Rodentia: Cricetidae), F. Nieri-Bastos coll.; 1 larva (IBSP 358), Angra dos Reis, Rio de Janeiro (RJ), VI-1931, Dasyprocta leporina (L.) (Rodentia: Dasyproctidae), L. Travassos coll.; 1 larva (IBSP 1681), Abaeté, Minas Gerais (MG), 05-VII-1937, Trinomys sp. (Rodentia: Echimyidae), E. Chagas coll.; 2 larvae (IBSP 1684), same locality and host, 01-VI-1937, E. Chagas coll..

Figure 7. Lower leg of female bitten by Eutrombicula tinami (Oudemans, 1910). The arrows show the areas of papular dermatits.

Birds

Three larvae (IBSP 370), Instituto Butantan, São Paulo, SP, no date, Columbina talpacoti (Temminck) (Columbiformes: Columbidae); 1 larva (IBSP 12732), Paraty, RJ, no date, Geotrygon montana (L.) (Columbiformes: Columbidae), L. Moreira-Lima coll.; 4 larvae (IBSP 468), Serra da Cantareira, São Paulo, SP, 16-I-1936, Leptotila sp. (Columbiformes: Columbidae); 6 larvae (IBSP 12165), Instituto Butantan, São Paulo, SP, 27-II-2015, Leptotila verreauxi (Bonaparte) (Columbiformes: Columbidae), L. Moreira-Lima coll.; 1 larva (IBSP 1689), same locality, 01-IV-1939, Guira guira (Gmelin) (Cuculiformes: Cuculidae), J. Navas and A. T. Leão coll.; 2 larvae (IBSP 10944), same data; 2 larvae (IBSP 1673), Sabaúna district, Mogi das Cruzes, SP, 29-I-1939, Cyanoloxia brissonii (Lichtenstein) (Passeriformes: Cardinalidae), N. Bolognani coll.; 14 larvae (IBSP 12213A), Paraty, SP, 19-III-2015, Formicarius colma Boddaert (Passeriformes: Formicariidae), L. Moreira-Lima coll.; 1 larva (IBSP 1650A), Sabaúna district, Mogi das Cruzes, SP, 29-I-1939, ''unidentified bird'' (Passeriformes: Fringillidae), N. Bolognani coll.; 5 larvae (IBSP 372), Instituto Butantan, São Paulo, SP, 12-III-1933, Mimus saturninus (Lichtenstein) (Passeriformes: Mimidae), J. Cavalheiro coll.; 1 larva (IBSP 13119), Estação Ecológica de Carijós, Florianópolis, Santa Catarina (SC), 16-XI-2015, Geothlypis aequinoctialis (Gmelin) (Passeriformes: Parulidae), C. Lugarini coll.; 1 larva (IBSP 13121), same locality, 9-IV-2016, Zonotrichia capensis (Statius Muller) (Passeriformes: Passerellidae), C. Lugarini coll.; 1 larva (IBSP 371), Instituto Butantan, São Paulo, SP, 26-V-1932, same host, J. Cavalheiro coll.; 6 larvae (IBSP 361), Instituto Butantan, São Paulo municipality, São Paulo state, no date, Chiroxiphia caudata (Shaw and Nodder) (Passeriformes: Pipridae), J. Cavalheiro coll.; 3 larvae (IBSP 12378), Fazenda Continente, Coronel Pacheco, MG, 09-I-2006, same host, E, Daemon coll.; 1 larva (IBSP 12216B), Paraty, RJ, 20-III-2015, Pyriglena leucoptera (Vieillot) (Passeriformes: Thamnophilidae), L. Moreira-Lima coll.; 3 larvae (IBSP 12212), same locality, 16-IV-2015, Tachyphonus coronatus (Vieillot) (Passeriformes: Thraupidae), L. Moreira-Lima coll.; 1 larva (IBSP 13695), Estação Ecológica de Carijós, Florianópolis, SC, 17-IV-2017, same host, C. Lugarini coll.; 1 larva (IBSP 13700), same locality and host, 13-XII-2017; 1 larva (IBSP 13123), same locality and host, 1-XII-2015; 1 larva (IBSP 13699), same locality, 13-XII-2017, Troglodytes musculus Naumann (Passeriformes: Troglodytidae), C. Lugarini coll.; 2 larvae (IBSP 13706B), Reserva Biológica Marinha do Arvoredo, Florianópolis, SC, 24-I-2018, same host; 4 larvae (IBSP 12218), Paraty, RJ, 19-III-2015, Turdus albicollis Vieillot (Passeriformes: Turdidae), L. Moreira-Lima coll.; 1 larva (IBSP 13701), Reserva Biológica Marinha do Arvoredo Florianópolis, SC, 23-I-2018, same host; 1 larva (IBSP 13702), same data; 1 larva (IBSP 13703), same locality and host, 24-I-2018; 1 larva (IBSP 13704), same data; 5 larvae (IBSP 13705), same data; 1 larva (IBSP 363), Instituto Butantan, São Paulo, SP, no date, Turdus amaurochalinus Cabanis (Passeriformes: Turdidae); 7 larvae (IBSP 12017B), same locality, 29-I-2015, Turdus rufiventris Vieillot (Passeriformes: Turdidae), L. Moreira-Lima coll.; 6 larvae (IBSP 12018A), same data; 7 larvae (IBSP 12160A), same locality and host, 26-III-2015; 3 larvae (IBSP 12176), same data; 5 larvae (IBSP 12177), same data; 6 larvae (IBSP 12178), same data; 3 larvae (IBSP 12181A), same data; 2 larvae (IBSP 12162A), same locality and host, 26-II-2015; 3 larvae (IBSP 12166A), same locality and host, 27-II-2015; 2 larvae (IBSP 12167A), same data; 3 larvae (IBSP 12168), same data; 5 larvae (IBSP 12169A), same data; 6 larvae (IBSP 12170), same data; 2 larvae (IBSP 12171), same data; 1 larva (IBSP 12172A), same data; 3 larvae (IBSP 12173), same data; 6 larvae (IBSP 12195A), same data; 2 larvae (IBSP 12196A), same data; 6 larvae (IBSP 12183A), same locality and host, 27-III-2015; 7 larvae (IBSP 12184), same data; 2 larvae (IBSP 376), same locality, 3-II-1933, Tyrannus melancholicus Vieillot (Passeriformes: Tyrannidae); 2 larvae (IBSP 13698), Estação Ecológica de Carijós, Florianópolis, SC, 13-XII-2017, Elaenia obscura (d'Orbigny and Lafresnaye) (Passeriformes: Tyrannidae); 3 larvae (IBSP 1641), Reserva Florestal do Morro Grande, Cotia, SP, 20-II-1939, Crypturellus obsoletus (Temminck) (Tinamiformes: Tinamidae), J. Navas coll.; 3 larvae (IBSP 876), Água doce, Piedade, SP, 12-VII-1936, Tinamus solitarius (Vieillot) (Tinamiformes: Tinamidae).

Notes about the trombiculiasis

The subjects came in contact with larval E. tinami in the forest, which were noticed several hours later, around 6:00pm, mainly because of the onset of intense pruritus; at this moment one of the subjects (Author Fournier, G.F.S.R.) had specimens collected by application of adhesive tape, few larvae were collected from the tape at the stereomicroscope and further identified (IBSP 12522).

The clinical signs consisted of areas of papular dermatitis located on the feet, legs, knees, hands, fingers, arms, face and scalp. The lesions were circular, focal and multifocal, with papular inflammatory reaction with a center papule and a hyperemic centrifuge halo of sizes ranging from 1 to 3 cm in diameter, probably caused by exuberant cellular inflammatory reaction with manifests severe pruritus and lasts for over 72 hours as described in other Eutrombicula species. No infection symptoms, such as fever, were present. The pruritus ceased after about five days without any medication. Neither subject consulted a physician or used medicine to kill the parasites or control inflammation. Both subjects used physical removal with a hard bath sponge during a shower about 10 hours after exposure, but it was not evaluated whether this action was efficient or not. Both subjects experienced the same symptoms and skin manifestations. Figure 7 shows the inflammatory papules on the female subject 24 hours after exposure.

Discussion

Host records suggest some Eutrombicula species are not host specific. This applies to E. tinami, which has been reported from multiple species of birds, rodents and marsupials (Oudemans 1910; Brennan and Lukoschus 1971; Brennan and Reed 1974, 1975; Jacinavicius et al. 2018a).

Prior to this study E. tinami had been reported from only five hosts, Dielphis marsupialis from Surinam (Brennan and Lukoschus 1971), Proechimys semispinosus from Panama (Brennan and Lukoschus 1971), Marmosa robinsoni from Venezuela (Brennan and Reed 1974), Didelphis aurita from Brazil (Jacinavicius et al. 2018a) and the original host, Crypturus noctivagus, also from Brazil (Oudemans 1910). In this study, we recorded 207 E. tinami from 70 individual hosts representing 17 mammals and 53 birds sampled in Brazil. Mammals, including humans accounted for only 20% of the E. tinami recovered from hosts. All were new mammalian host records for this species, except for the host species D. aurita. Birds are important hosts for Brazilian E. tinami accounting for 80% of all the specimens recovered with 20 new host records in 15 families. The bird genus Turdus spp. appears to be a common host for E. tinami accounting for about half of all birds with E. tinami and nearly 60% of all specimens recovered.

This species was also found biting humans and joins E. alfreddugesi and E. batatas, in causing human trombiculiasis in Brazil.

Eutrombicula tinami was described for Brazil without specific locality information (Oudemans 1910). The only other published Brazilian record for this species was from a marsupial collected in the São Paulo, SP (Jacinavicius et al. 2018a). Here, we provide new records from the states of Minas Gerais, Rio de Janeiro, Santa Catarina and São Paulo. This species had Previously published records of this species from Panama (Brennan and Lukoschus 1971), Surinam (Brennan and Lukoschus 1971) and Venezuela (Brennan and Reed 1974) indicating perhaps its distribution includes the neighboring countries.

Although E. tinami has been reported from several countries, the two limited redescriptions (Oudemans 1912; Fuller 1952), more than 50 years ago, did not provide enough morphological detail to identify this species. In this study, we provide new figures, SEM images and additional metric data to help identify this species.

The human bite symptoms reported here are similar to those reported by Chaccour (2005) and Faccini et al. (2017). The under reporting of trombiculiasis in Brazil is probably due to the difficulty of finding chiggers on a human host or identifying them when they are found. Fonseca (1932) suggested chiggers may vector pathogens in Brazil. Surveys of Brazilian and South America chiggers their hosts and host symptoms are needed to help understand the potential health risks chiggers may present to humans and domestic animals.

Acknowledgements

To Gabrielle Ribeiro de Andrade and Maria Cristina Ferreira do Rosário for technical contribution (CNPq no. 377343/2015-3 and 377342/2015-7, respectively), Beatriz Mauricio of the Laboratory of Cellular Biology of the Instituto Butantan for the images obtained through the Scanning Electron Microscopy, Debra Creel, Andrew Ulsamer (SEL-USDA), and Armando Rosario-Lebron (APHIS-USDA) for their help with references and technical support. The Smithsonian Natural History Museum and National Agricultural Library (NAL-USDA), SEL-USDA for support and assistance with specimens and references. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq no. 454907/2014-1 and 440639/2015-8 to DMB-B, 377976/2014-8 to FCJ), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP no. 2010/51875-9 to DMB-B and 2017/01416-7 to RB-S). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA; USDA is an equal opportunity provider and employer.

Authors' contribution

RB-S, FCJ and DMB-B writing and development of the entire manuscript. AP and GFSRF collected material and aided in reporting on the case report of trombiculiasis, providing crucial information for this record. CL, AF, LM-L and EH-Z collected the recent material, with them it was possible to make the SEM images. In addition, identified all the hosts, of the recent collections as of the old collections. CW and RO contributed to the organization and improved the English and provided valuable insights from their experiences for this manuscript.

References

Bassini-Silva R., Jacinavicius F.C., Muñoz-Leal S., Maturano R., Welbourn C., Ochoa R., Bauchan G., Barros-Battesti D.M. 2018. A new species of the genus Eutrombicula Ewing, 1938 (Trombidiformes: Trombiculidae) and new records for the species Eutrombicula batatas (Linnaeus, 1758) in Brazil. Acarologia, 58: 976-986.

Brennan J.M., Lukoschus F. 1971. Parasitic of Surinam. VIII. A new genus and species of chigger, Fauranius atecmartus, and additional records of species (Acarina: Trombiculidae). Bull. South. Calif. Acad. Sci., 70: 42-45.

Brennan J.M., Reed J.T. 1974. The genus Eutrombicula in Venezuela (Acarina: Trombiculidae). J. Parasitol., 60: 699-711. doi:10.2307/3278741

Brennan J.M., Reed J.T. 1975. A list of Venezuela chiggers, particularly of small mammalian hosts (Acarina: Trombiculidae). Brigham Young Univ Sci Bull, 20: 45-75.

Buitendijk A.M. 1945. Voorloopige catalogus van de acari in de Collectie-Oudemans. Zool. Med. (Leiden), 24: 281-391.

Ewing H.E. 1931. A catalogue of the Trombiculinae, or chigger Mites, of the New World, with new genera and species and a key to the genera. Proc. U. S. Nat. Mus., 80: 1-23. doi:10.5479/si.00963801.80-2908.1

Ewing H.E. 1938. A key to the genera of chiggers with descriptions of new genera and species. J. Wash. Acad. Sci., 28: 288-295.

Chaccour C.J. 2005. Trombiculiasis: reporte de dos casos y revisión de la literatura. Rev. Der. Ven., 43: 18-21.

Faccini J.L.H., Santos A.C.G., Santos S.B., Jacinavicius F.C., Bassini-Silva R., Barros-Battesti D.M. 2017. Trombiculiasis in domestic goats and humans in the state of Maranhão, Brazil. Rev. Bras. Parasitol. V., 26: 104-109. doi:10.1590/s1984-29612016088

Fonseca F. 1932. Notas de Acareologia V. Trombicula butantanensis sp. n. (Acarina, Trombidiidae). Mem. Inst. Butantan (São Paulo), 7: 148-150.

Fuller H.S. 1952. The mite larvae of the family Trombiculidae in the Oudemans collection: Taxonomy and medical importance). ‎Zool. Verhandel. (Leiden), 18: 1-261.

Jacinavicius F.C., Bassini-Silva R., Mendoza-Roldan J.A., Pepato A.R., Ochoa R., Welbourn C., Barros-Battesti D.M. 2018a. A checklist of chiggers from Brazil, including new records (Acari: Trombidiformes: Trombiculidae and Leeuwenhoekiidae). ZooKeys, 743: 1-41. doi:10.3897/zookeys.743.22675

Jacinavicius F.C., Bassini-Silva R., Amorim M., Gazêta G.S., Siqueira L.R., Welbourn C., Barros-Battesti D.M. 2018b. Description of Parasecia fernandae sp. n. (Trombidiformes: Trombiculidae) and new records of chiggers from rodents in Rio de Janeiro State, Brazil. Acarina, 26: 205-211. doi:10.21684/0132-8077-2018-26-2-205-211

Jenkins D.W. 1949. Trombiculid mites affecting man. IV. Revision of Eutrombicula in the American Hemisphere. Ann. Entomol. Soc. Am., 42: 289-318. doi:10.1093/aesa/42.3.289

Loomis R.B., Wrenn W.J. 1984. Systematics of the pest chigger genus Eutrombicula (Acari: Trombiculidae). In: Griffiths D.A., Bowman C.E. (Eds). Proceedings of the VI International Congress of Acarology. Ellis Horwood, Chichester. p. 152-159.

Methlagl A. 1928. Über die Trombidiose in den Österreichischen Alpenländern. Denkschriften Osterreichischen Akademie der Wissenschaften (Wien). Math.-Naturwiss. Kl., 101: 213-250.

Mullen G.R., OConnor B.M. 2002. Mites (Acari). In: Durden L., Mullen G. (Eds). Veterinary Entomology. Academic Press/Elsevier, Amsterdam. p. 449-516. doi:10.1016/B978-012510451-7/50025-6

Oudemans A.C. 1910. Acarologische aanteekeningen XXXIII. Entomol. Ber. (Amsterdam), 3: 83-90. doi:10.5962/bhl.part.1133

Oudemans A.C. 1912. Die bis jetzt bekannten larven von Trombidiidae and Erythraeidae mit besonderer berkucksichtigung der fur den menschen schadlichen Arten. Zoologische Jahrbucher: Supplement, 1: 1-230.

Shatrov A.B. 2000. Trombiculid mites and their parasitism on vertebrate hosts. Tr. Zool. Inst., 285: 1-328.

Radford C. D. 1942. The larval Trombiculinae (Acarina, Trombidiidae) with descriptions of twelve new species. J. Parasitol., 34: 55-81. doi:10.1017/S0031182000015997

Stekolnikov A.A., González-Acuña D. 2010. Four new species of chigger mites (Acari: Trombiculidae) of the genus Eutrombicula from Chile. Int. J. Acarol., 36: 313-325. doi:10.1080/01647951003685667

Vercammen-Grandjean P.H. 1965. Trombiculinae of the World: synopsis with generic, subgeneric, and group diagnoses (Acarina, Trombiculidae). George Williams Hooper Foundation, University of California, San Francisco, CA.

Walter D.E., Krantz G.W. 2009. Chapter 7: Collecting, rearing, and preparing specimens. In: Krantz G.W., Walter D.E. (Eds). A manual of acarology. Lubbock, Texas: Tech University Press. p. 83-96.



Comments
Please read and follow the instructions to post any comment or correction.

Article editorial history
Date received:
2019-06-13
Date accepted:
2019-09-24
Date published:
2019-10-10

Edited by:
Mąkol, Joanna

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License
2019 Bassini-Silva, Ricardo; de Castro Jacinavicius, Fernando; Pinter, Adriano; Fournier, Gislene F. S. R.; Lugarini, Camile; Ferreira, Ariane; Moreira-Lima, Luciano; Hingst-Zaher, Erika; Welbourn, Cal; Ochoa, Ron and Moraes Barros-Battesti, Darci
Downloads
 Download article

Download the citation
RIS with abstract 
(Zotero, Endnote, Reference Manager, ProCite, RefWorks, Mendeley)
RIS without abstract 
BIB 
(Zotero, BibTeX)
TXT 
(PubMed, Txt)
Article metrics
Number of distinct pdf views
300

Dimensions

Cited by: view citations with

Search via ReFindit