Rocha de Almeida, Beatriz ¹ ; de Castro Jacinavicius, Fernando ² ; Pereira Pesenato, Isabella ³ ; Fortunato Dornelas Jr, Leormando ⁴ ; Welbourn, Cal ⁵ ; Ochoa, Ronald ⁶ ; Aranha Camargo, Luis Marcelo ⁷ ; Moraes Barros-Battesti, Darci ⁸ and Bassini-Silva, Ricardo ⁹

¹Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias-UNESP, Jaboticabal, SP, Brazil.
²Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil.
³Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil.
⁴Instituto Leônidas e Maria Deane, Fundação Oswaldo Cruz (FIOCRUZ/ILMD), Manaus, Amazonas, Brazil & Instituto de Ciências Biomédicas V, Universidade de São Paulo (ICB/USP), São Paulo, Brazil.
⁵Smithsonian Institution, National Museum of Natural History, National Insect and Mite Collection, Washington, D.C., USA.
⁶Systematic Entomology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, USA.
⁷Instituto Leônidas e Maria Deane, Fundação Oswaldo Cruz (FIOCRUZ/ILMD), Manaus, Amazonas, Brazil & Instituto de Ciências Biomédicas V, Universidade de São Paulo (ICB/USP), São Paulo, Brazil & Instituto Nacional de Ciência de Tecnologia de Epidemiologia da Amazônia Ocidental (INCT-EPIAMO), Porto Velho, Rondônia, Brazil & Centro de Medicina Tropical de Rondônia (CEPEM) da Secretaria de Estado da Saúde de Rondônia, Monte Negro, Rondônia, Brazil & Centro Universitário UNIFAEMA, Ariquemes, Rondônia, Brazil.
⁸Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias-UNESP, Jaboticabal, SP, Brazil.
⁹Laboratório de Coleções Zoológicas, Instituto Butantan, São Paulo, SP, Brazil.

2024 - Volume: 64 Issue: 4 pages: 1117-1125

ZooBank LSID: 47FCB01E-2E53-47F2-9AD4-280A5247738E

Original research

Keywords

Abstract

Introduction

The Neotropical genus Hooperella Vercammen-Grandjean 1967 has a parasitic preference for bats. Recently, Bassini-Silva et al. (2023) reviewed two species of this genus and concluded that there are four valid species: Hooperella alvarezi (Loomis, 1969), Hooperella saccopteryx (Brennan and Jones, 1960), Hooperella vesperuginis (Brennan and Jones, 1960) and Hooperella yucatanica (Loomis, 1969). Hooperella alvarezi and H. yucatanica are only recorded in Mexico, while the other two species are distributed throughout the Americas.

In Brazil, only the species H. vesperuginis has been recorded. Vercammen-Grandjean (1967) and Bassini-Silva et al. (2023) recorded this species in the states of Rio de Janeiro and Minas Gerais, parasitizing two different species of phyllostomid bats, the little big-eared bat, Micronycteris megalotis (Gray, 1842) and the Seba's short-tailed bat, Carollia perspicillata (L.). Despite the close proximity of Brazil to countries such as Bolivia, Colombia, Costa Rica, Mexico, Peru, Surinam, Trinidad and Tobago, and Venezuela, where Hooperella saccopteryx has been documented (Brennan and Jones 1960, 1961; Loomis 1969; Brennan 1970a, b; Brennan and Bronswijk 1975; Brennan and Reed 1975; Webb and Loomis 1977; Marinkelle and Grose 1981; Hoffmann 1990). This species has not yet been recorded in the national territory.

We present a comprehensive redescription of the species H. saccopteryx based on the type series and newly identified specimens from two different collections. This includes detailed images obtained through Scanning Electron Microscopy and schematic drawings. Besides that, the examined material represents the first records of this species in Brazil, specifically in the states of Pará, Rondônia and São Paulo.

Material and methods

The examined types of H. saccopteryx were deposited in the U.S. National Entomology Collection, Smithsonian Institution, National Museum of Natural History, Washington, DC, USA (USNM), currently located at the Systematic Entomology Laboratory (BARC-USDA-ARS), Beltsville, MD, USA. The slide-mounted material from Belém municipality, Pará State, Brazil, was also deposited in the USNM collection.

The examined material recorded in Rondônia and São Paulo States came from the tissue bank of the Acarological Collection of the Instituto Butantan (IBSP), São Paulo, Brazil, which are preserved in ethyl alcohol (100%). The specimens were slide-mounted in Hoyer's medium following the protocols described by Walter and Krantz (2009). For identification, we used the key for genera of Neotropical and Nearctic Trombiculidae (Brennan and Goff 1977) and later, we compared the results with the original descriptions of all species within the identified genus (Hooperella), and the type material. Part of this material from the IBSP Collection (n = 25) was prepared for Scanning Electron Microscopy (SEM), using the Digital Scanning Microscope FEI, Quanta 250, at the Laboratório de Biologia Celular, Instituto Butantan, São Paulo, Brazil.

The examination of morphological characters and measurements of the types and non-types were performed using a Leica DFC 500 digital camera coupled to a Leica DM4000B optical microscope with phase contrast. The microscope images were made with Leica Application Suite v. 2.5.0 software. Drawings and figures were prepared using Inkscape v.1.0.1 and Adobe Photoshop v. 13.0 software. The measurements are in micrometers and are available in the Supplementary Table 1.

In summary, the redescription of the species is based on the type material, new material from Pará and material stored in alcohol from São Paulo and Rondônia. The drawings were made from the holotype and paratypes. SEM imagery was obtained from material preserved in alcohol, originating from the states of São Paulo and Rondônia.

The terminology of the dorsal opisthosomal setae and setae on the prodorsal sclerite follows Grandjean (1939) with adaptations by Kethley (1990) and Grandjean (1935; 1947) for the specialized setae on the legs and palps.

Results

Family Trombiculidae Ewing, 1929

Hooperella saccopteryx (Brennan and Jones, 1960)

Trombicula saccopteryx Brennan and Jones 1960: 530; Brennan and Yunker 1966: 255; Marinkelle and Grose 1981: 18

Tecomatlana (Hooperella) saccopterix Vercammen-Grandjean 1967: 854 misspelled

Tecomatlana (Hooperella) saccopteryx Loomis 1969: 15; Brennan 1970: 35.

Hooperella saccopteryx Brennan 1970:811; Brennan and Reed 1975: 53; Brennan and Bronswijk 1975: 244; Webb and Loomis 1977: 82; Hoffmann 1990: 73; Zajkowska et al. 2018: 110.

(Figures 1-6, and Supplementary Tables 1 and 2)

Diagnosis

Larva. Palpfemur and palpgenu each with a single branched seta; all three palptibial setae nude; adoral setae (cs) nude; cheliceral blade with small set of teeth just below the tricuspid cap; C, D and E rows with eight, six and four setae each; 3 to 7 eupathidia in Ge I, famulus (ε) Ta I and II distal and proximal to solenidion (ω), respectively.

Redescription

Larvae (holotype, 92 paratypes, and 60 non-types).

Gnathosoma — fPp = B/B/NNN/7Bωζ; odontus trifurcate; cheliceral blade with small set of teeth just below the tricuspid cap; gnathobase punctate, subcapitular (bs) setae branched and adoral (cs) setae nude (Figures 1A-B, and 5A).

Idiosoma — eyes 2/2, anterior lens larger, with ocular plate; prodorsal sclerite subtrapezoidal and entirely punctate, anterior margin slightly straight, lateral margins slightly sinuous, and posterior margins converging in the center to slightly ′u′ (Figure 2 and 5B), with flagelliform trichobothria (si), with long and thin setules, and 5 branched normal setae [pair of ve (= AL) seta, a single vi (= AM) seta and pair of se (= PL) seta], si > se ≥ vi > ve; opisthosoma (Figures 3A-B) with 46 to 50 setae (46 in holotype); dorsal opisthosoma with 24 setae (Figure 5C), C row with 4 pairs of setae (c₄ = humeral setae), D row with 3 pairs of setae, E and F rows with 2 pairs of setae each, and H row with one pair of setae, and 22 to 26 ventral opisthosomal setae with 8 setae anterior to the anus and 14 to 18 setae posterior to the anus (14 in the holotype). Two pairs of sternal setae (1a, 3a) between coxal fields I and III (Figure 5D).

Legs femur of legs I-III each divided into basifemur and telofemur, each leg terminates with paired claws, and a claw-like empodium without onychotriches, coxal fields punctate; Leg I - coxal field seta 1b branched (1B); trochanter 1B; basifemur 1B; telofemur 5B; genu 4B, 3 to 7 σ and microseta κ; tibia 8B, 2 φ and κ; tarsus 21B with ω, ε, dorsal eupathidium (ζ′) with companion seta (z) and subterminal eupathidium (ζ), base of famulus (ε) distal to ω, (Figure 4A and 6A). Leg II - coxal field seta 2b (1B); trochanter 1B; basifemur 2B; telofemur 4B; genu 3B, σ; tibia 6B, 2 φ; tarsus 16B with ω, ε and subterminal eupathidium (ζ), base of ε proximal to ω (Figure 4B). Leg III - coxal field seta 3b (1B); trochanter 1B; basifemur 2B; telofemur 3B; genu 3B, σ, tibia 6B, φ; tarsus 14B and one mastisetae (MTa) (Figure 4C and 6B-C).

Type material

Holotype — larva (USNMENT01759388); near to Guaracara River, San Fernando City, Trinidad and Tobago; 18 March 1958; ex Saccopteryx bilineata (Temminck) (Chiroptera: Emballonuridae); RML 34687.

Paratype — 5 larvae (USNMENT01759389-393); same data as holotype. The other 87 examined paratypes from Trinidad and Tobago are listed in Bassini-Silva et al. (2021), in the pages 94-95.

Additional material examined — (USNM Collection). BRAZIL: 7 larvae; Belém Municipality, Pará State; 25 March 1968; ex Saccopteryx leptura (Schreber, 1774) (Chiroptera: Emballonuridae); T.H.G. Aitken coll.; (RML 49371). (IBSP Collection). BRAZIL: 3 larvae (IBSP 18386); Monte Negro City, Rondônia State (63° 26′ 46" W, 10° 17′ 04" S); 12 May 2021; ex S. bilineata. 18 larvae (IBSP 18387); same locality (63° 26′ 38" W, 10°16′ 38" S) and host; 22 May 2021. 1 larva (IBSP 19274); same locality (63° 23′ 12" W, 10° 25′ 56" S) and host; 10 Dec. 2021. 17 larvae (IBSP 19289); same locality (63° 26′ 52" W, 10° 16′ 58"S) and host; 29 Nov. 2022; L.F. Dornelas Jr. coll. 6 larvae (IBSP 19337); Bebedouro Municipality, São Paulo State; 20 Oct. 2019; ex S. leptura. 8 larvae (IBSP 19338); same data.

Differentials diagnosis

The species Hooperella saccopteryx differs from other species of the genus in having a subtrapezoidal prodorsal sclerite, fewer opisthosomal setae (46 to 50 setae), and a variation of setae on the genu of leg I (3 to 7 σ). While the other species, H. alvarezi, H. vesperuginis and H. yucatanica have a rectangular prodorsal sclerite, more opisthosomal setae (108, 59 to 62, and 125, respectively) and only three σ on genu of leg I. Besides that, H. saccopteryx further differs from H. yucatanica in having 3-pronged odontus (vs. multi-pronged odontus) and nude adoral setae (vs. branched) and from H. alvarezi in having a different palpal formula (B/B/NNN vs. B/B/BBN).

Discussion

Upon examining the type series, we realized the necessity of redescribing the species by consolidating all the morphological data into this study. Additionally, it was only after reviewing the type material that we were able to accurately identify the specimens deposited in the acarological collections we visited (IBSP and USNM). Consequently, we have included the examined material in the updated description of this species.

Comparing the original description made by Brennan and Jones (1960) and the redescriptions made by Vercammen-Grandjean (1967) and Hoffmann (1990) with our current redescription of H. saccopteryx, we were able to add the measurements of all seven leg segments, as well as the ventral and sternal setae, which were previously not included. Additionally, we noticed differences, particularly in the number of specialized setae (σ) on the genu of leg I. Brennan and Jones (1960) and Vercammen-Grandjean (1967) commented about a variation in the quantities of these setae (5, and sometimes 6), while Hoffmann (1990) did not describe this variation, and stated that this species has only five specialized setae. However, we observed that there is a variation wider than stated by these authors, 3 to 7 specialized setae (σ) on genu of leg I; sometimes there is even a difference between the left and right leg of the same specimen. Another subtle difference observed referred to the number of setae in dorsal opisthosomal rows; Brennan and Jones (1960) did not observe two extra setae in the F row, contrary to the state by us and in the redescription made by Vercammen-Grandjean (1967). The Supplementary Table 2 a quantification of the number the ventral setae located both posterior and anterior to the anus of each examined specimen. Besides that, this supplementary table shows the amount of σ on genu of leg I on both sides of symmetry axis in each specimen.

Regarding the measurements, as previously stated, many are new. While Brennan and Jones (1960) provided only the measurements of the holotype for the prodorsal sclerite and the specialized setae of legs I-III, Vercammen-Grandjean (1967) reported variations in the measurements of the prodorsal sclerite, opisthosomal setae, leg lengths, and the combined length of the three legs for four specimens. The previously presented measurements are consistent with those in this study, with no significant variation to note, as the small differences observed in some structures are probably due to the differing quality of the microscopes used. The Supplementary Table 1 presents the measurements for specimen examined in this study, both for type and non-type specimens.

Based on our examination of the material from both collections, H. saccopteryx appears to have a strong preference for parasitizing bats of the genus Saccopteryx. However, this does not exclude the possibility of being found on other hosts, as indicated by various authors (Brennan and Jones 1960, 1961; Loomis 1969; Brennan 1970a, b; Brennan and Bronswijk 1975; Brennan and Reed 1975; Webb and Loomis 1977; Marinkelle and Grose 1981; Hoffmann 1990), and compiled by Zajkowska et al. (2018) and Ševčík (2023). Until a thorough review of all materials is completed, it remains clear that this species has a broad distribution, being found from Mexico (Hoffmann 1990) to the southeastern region of Brazil (this study), and shows a preference for parasitizing phyllostomid bats.

Acknowledgments

To Gabrielle Ribeiro de Andrade, Maria Cristina Ferreira do Rosário from the Laboratório de Coleções Zoológicas, Instituto Butantan, for technical contribution; to Beatriz Mauricio from the Laboratório de Biologia Celular, Instituto Butantan, for the images obtained through Scanning Electron Microscopy; to Andrew Ulsamer (SEL-USDA) for his help with references and technical support. Also, to 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 under the Grant CNPq no. 402575/2021-0 (FCJ), and the Productivity Grant to DMB-B (CNPq Process #303802/2021-9), as well as by the Fundação de Amparo à Pesquisa do Estado de São Paulo under the Grants FAPESP no. 2023/09381-9 (BRA), 2019/19853-0, 2024/01231-0 (FCJ), 2022/11576-0 (IPP), and 2020/11755-6 (RB-S), and also 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 to provide specific information and does not imply recommendation or endorsement by the USDA; USDA is an equal opportunity provider and employer.

acarologia_4750_Supplementary-table-1.xlsx

acarologia_4750_Supplementary-table-2.xlsx

References

1. Bassini-Silva, R., Jacinavicius, F.C., Maturano, R., Muñoz-Leal, S., Ochoa, R., Bauchan, G., Labruna, M.B., Barros-Battesti, D.M. 2018. Blankaartia sinnamaryi (Trombidiformes: Trombiculidae) parasitizing birds in southeastern Brazil, with notes on Rickettsia detection. Rev. Bras. Parasitol. Vet., 27: 354-362. https://doi.org/10.1590/s1984-296120180057
2. Bassini-Silva, R., Jacinavicius, F.C., Welbourn, C., Barros-Battesti, D.M., Ochoa, R. 2021. Complete type catalog of Trombiculidae sensu lato (Acari: Trombidiformes) of the U.S. National Entomology Collection, Smithsonian Institution. Smithson. Contrib. Zool., 652: 1-141. https://doi.org/10.5479/si.13546616.v1
3. Bassini-Silva, R., Jacinavicius, F.C., Muñoz-Leal, S., Maturano, R., Takatsu, J.C., Tolesano-Pascoli, G.V., Alquezar, R.D., Lugarini, C., Ferreira, A., Moreira-Lima, L., Welbourn, C., Ochoa, R., Hingst-Zaher, E., André, M.R., Labruna, M.B., Barros-Battesti, D.M. 2023. Bacterial pathogens' screening in Brazilian chigger mites (Trombidiformes: Trombiculidae), with the first report of ′Candidatus Rickettsia colombianensi′‑like in avian‑associated chiggers. Arch. Microbiol., 205: 51. https://doi.org/10.1007/s00203-022-03393-9
4. Brennan, J.M. 1970a. Chiggers from the Bolivian-Brazilian border (Acarina: Trombiculidae). J. Parasitol., 56: 807-812. https://doi.org/10.2307/3277728
5. Brennan, J.M. 1970b. A small collection of chiggers from Surinam (Acarina: Trombiculidae). Bull. South. Calif. Acad. Sci., 69: 32-37.
6. Brennan, J.M., van Bronswijk, J.E.M.H. 1975. Parasitic mites of Surinam XXI. New records of Surinam and certain French Guiana chiggers with the description of a new species of Loomisia Brennan & Reed, 1972 (Acarina: Trombiculidae). J. Med. Entomol., 12: 243-249. https://doi.org/10.1093/jmedent/12.2.243
7. Brennan, J.M., Goff, M.L. 1977. Keys to the genera of chiggers of the Western Hemisphere (Acarina: Trombiculidae). J. Parasitol., 63: 554-566. https://doi.org/10.2307/3280021
8. Brennan, J.M., Jones, E.K. 1960. Chiggers of Trinidad, BWI (Acarina: Trombiculidae). Acarologia, 2: 493-540. https://doi.org/10.1093/aesa/53.2.183
9. Brennan, J.M., Jones, E.K. 1961. Chiggers of Peru (Acarina: Trombiculidae). Acarologia, 3: 172-205.
10. Brennan, J.M., Reed, J.T. 1975. A list of Venezuela chiggers, particularly of small mammalian hosts (Acarina: Trombiculidae). Brigh. Young Univ. Sci. Bull., 20(1): 45-75.
11. Brennan, J.M., Yunker, C.E. 1966. The Chiggers of Panama (Acarina: Trombiculidae). In Wenzel, R.L., Tipton, V.J. (Eds). Ectoparasites of Panama. Chicago: Field Museum of Natural History. pp. 221-266.
12. Grandjean, F. 1935. Les poils et les organes sensitifs portés par les pattes et le palpe chez les oribates. Bull. Soc. Zool. Fr., 60: 6-39.
13. Grandjean, F. 1939. Les segments postlarvaires de l′hysterosoma chez les oribates (Acariens). Bull. Soc. Zool. Fr., 64: 273-284.
14. Grandjean, F. 1947. L'origine pileuse des mors et la chaetotaxie de la mandibule chez les Acariens actinochitineux. C. R. Hebd. Seances Acad. Sci., 224: 1251-1254.
15. Jacinavicius, F.C., Bassini-Silva, R., Muñoz-Leal, S., Welbourn, C., Ochoa, R., Labruna, M.B., Barros-Battesti, D.M. 2019. Molecular detection of Rickettsia genus in chigger mites (Trombidiformes: Trombiculidae) collected on small mammals in southeastern Brazilian. Rev. Bras. Parasitol. Vet., 28(4): 563-568. https://doi.org/10.1590/s1984-29612019069
16. Hoffmann, A. 1990. Los trombicúlidos de México (Acarida: Trombiculidae). Mexico: Universidad Autónoma de México. pp. 275.
17. Jones, B.M. 1950. The penetration of the host tissue by the harvest mite, Trombicula autumnalis Shaw. J. Parasitol., 40: 247-260. https://doi.org/10.1017/S0031182000018096
18. Kethley, J. 1990. Acarina: Prostigmata (Actinedida). In: Dindal, D.L. (ed.). Soil Biology Guide. New York: John Wiley & Sons. pp. 667-756.
19. Loomis, R.B. 1969. Chiggers (Acarina, Trombiculidae) from vertebrates of the Yucatan Peninsula. Mexico. Miscellaneous Publication - University of Kansas, Museum of Natural History 50: 1-22.
20. Marinkelle, C.J., Grose, E.S. 1981. A list of ectoparasites of Colombian bats. Rev. Biol. Trop., 29: 11-20.
21. Ševčík, M. 2023. Príspevky k taxonómii, biogeografii, ekológii a patogénom parazitov (Diptera, Acari) netopierov Starého sveta / Contributions to the taxonomy, biogeography, ecology and pathogens of parasites (Diptera, Acari) of Old World bats. Unpubl. PhD Thesis. Faculty of Science, Charles University, 166 pp. http://hdl.handle.net/20.500.11956/188779
22. Vercammen-Grandjean, P.H. 1967. Revision of the genus Tecomatlana Hoffmann, 1947 (Acarina: Trombiculidae). Acarologia. 9: 848-863.
23. Walter, D.E., Krantz, G.W. 2009. Collecting, rearing, and preparing specimens. In: Krantz, G.W., Walter, D.E., eds. A manual of acarology. Lubbock: Tech University Press; p. 83-96.
24. Webb, J.P., Loomis, R.B. 1977. Ectoparasites. In: Baker, R., Jones, K.J., Jr., Carter D.C. (eds), Biology of bats of the new world family Phyllostomidae. Part II. Special Publications, Museum of Texas Technical University. 13: 57-119.
25. Zajkowska, P., Moniuszko, H., Mąkol, J. 2018. Host-parasite associations between bats (Mammalia: Chiroptera) and chiggers (Trombidiformes: Trombiculidae)-a review and checklist. Ann. Zool. 68: 97-178. https://doi.org/10.3161/00034541ANZ2018.68.1.006
26. Zhang, Z.-Q. 2011. Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa, 3148: 7-12. https://doi.org/10.11646/zootaxa.3148.1.3

instructions