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Nasal mites (Mesostigmata, Rhinonyssidae) in Sternidae (Aves: Charadriiformes) on the southern Coast of Brazil

Ácaros nasais (Mesostigmata, Rhinonyssidae) em Sternidae (Aves: Charadriiformes) na Costa do Extremo Sul do Brasil

Abstract

Six species of birds of the family Sternidae are often found on the southern coast of South America. Sterna trudeaui, S. hirundinacea, Thalasseus maximus, T. acuflavidus and Sternula superciliaris are South American residents and Sterna hirundo, a Nearctic migrant. At least 500 species of nasal mites have been described around the world, and Rhinonyssidae is the most diverse family. These mites are bloodsucking endoparasites that inhabit the respiratory system of birds. This study aimed to report on occurrences of nasal mites in Sternidae on the southern coast of Brazil. Of the 106 birds analyzed, 8.5% (9 birds) were parasitized by nasal mites. This report provides the first record in the Neotropical region for two mite species, Sternostoma boydi and Larinyssus orbicularis parasitizing Thalasseus acuflavidus and Sternula superciliaris. No nasal mites were found in Sterna trudeaui or Thalasseus maximus. One host individual (T. acuflavidus) was parasitized by two species of nasal mites, S. boydi and L. orbicularis.

Keywords:
Nasal mites; Sternostoma; Larinyssus; birds; Southern Brazil

Resumo

Seis espécies de aves pertencentes à família Sternidae são encontradas frequentemente na costa sul da América do Sul. Sterna trudeaui, S. hirundinacea, Thalasseus maximus, T. acuflavidus e Sternula superciliaris residentes sul-americanos e Sterna hirundo, migrante neártico. Existem pelo menos 500 espécies descritas de ácaros nasais ao redor do mundo, sendo Rhinonyssidae a família mais diversa. Estes ácaros são endoparasitos hematófagos que habitam o sistema respiratório das aves. Este estudo objetivou reportar a ocorrência de ácaros nasais em Sternidae na costa do sul do Brasil. Das 106 aves analisadas, 8,5% (9 aves) estavam parasitadas por ácaros nasais. Este é o primeiro registro para duas espécies de ácaros na região neotropical, Sternostoma boydi e Larinyssus orbicularis, parasitando Thalasseus acuflavidus and Sternula superciliaris. Em Sterna trudeaui e Thalasseus maximus não foram encontrados ácaros nasais. Um único hospedeiro (T. acuflavidus) estava parasitado por duas espécies de ácaros nasais, S. boydi e L. orbicularis.

Palavras-chave:
Ácaros nasais; Sternostoma; Larinyssus; aves; sul do Brasil

At least 500 species of nasal mites have been described around the world, and Rhinonyssidae (Mesostigmata) are the most diverse group (PROCTOR & OWENS, 2000Proctor HC, Owens I. Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 2000; 15(9): 358-364. PMid:10931667. http://dx.doi.org/10.1016/S0169-5347(00)01924-8.
http://dx.doi.org/10.1016/S0169-5347(00)...
; DIMOV & SPICER, 2013Dimov ID, Spicer GS. A new species of nasal mite of the genus Rhinonyssus (Mesostigmata: Rhinonyssidae) from Leningrad Province, Russia. Syst Appl Acarol 2013; 18(3): 291-296. http://dx.doi.org/10.11158/saa.18.3.11.
http://dx.doi.org/10.11158/saa.18.3.11...
). These mites are hematophagous endoparasites that inhabit the respiratory system of birds. They are found preferentially in the membrane that lines the turbinates. However, they are frequently also found in the anterior portion of the nostrils, larynx, trachea, lung, air sacs and conjunctival sacs (AMARAL & REBOUÇAS, 1974Amaral V, Rebouças MM. Métodos para o estudo de ácaros rinonissídeos. São Paulo: Instituto Biológico; 1974.). Transmission occurs through direct contact with parasitized individuals, especially during the reproductive period (AMERSON, 1967Amerson AB Jr. Incidence and transfer of Rhinonyssidae (Acarina: Mesostigmata) in Sooty Terns (Sterna fuscata). J Med Entomol 1967; 4(2): 197-199. PMid:6052126. http://dx.doi.org/10.1093/jmedent/4.2.197.
http://dx.doi.org/10.1093/jmedent/4.2.19...
).

Rhinonyssidae mites are distributed into eight genera with characteristics that vary according to the specificity of their hosts. Some genera are found only in a particular host family, while others parasitize birds of different orders (KNEE et al., 2008Knee W, Proctor H, Galloway T. Survey of nasal mites (Rhinonyssidae, Ereynetidae, and Turbinoptidae) associated with birds in Alberta and Manitoba, Canada. Can Entomol 2008; 140(3): 364-379. http://dx.doi.org/10.4039/n08-017.
http://dx.doi.org/10.4039/n08-017...
).

Parasitism by nasal mites can cause damage to the nasal epithelium. However, typically these mites are not considered to cause any significant pathological condition in their hosts (KNEE et al., 2008Knee W, Proctor H, Galloway T. Survey of nasal mites (Rhinonyssidae, Ereynetidae, and Turbinoptidae) associated with birds in Alberta and Manitoba, Canada. Can Entomol 2008; 140(3): 364-379. http://dx.doi.org/10.4039/n08-017.
http://dx.doi.org/10.4039/n08-017...
).

Six species of birds belonging to family Sternidae are often found on the southern coast of South America. Five of these are South American residents: Sterna trudeaui Audubon, 1838; Sterna hirundinacea Lesson, 1831; Thalasseus maximus Boddaert, 1783; Thalasseus acuflavidus Cabot, 1847; and Sternula superciliaris Vieillot, 1819. The sixth species is Sterna hirundo Linnaeus, 1758, a Nearctic migrant that nests in the United States and Canada and which is found in great numbers on the Brazilian coast outside of the reproductive period (BELTON, 1994Belton W. Aves do Rio Grande do Sul: distribuição e biologia. São Leopoldo: UNISINOS; 1994.).

Of these six species, there are records of parasitism by nasal mites only for S. hirundo and T. maximus around the world. In S. hirundo there are records of the mites Neoboydaia philomachi Fain, 1956, Sternostoma boydi Strandtmann, 1951, Larynissus orbicularis Strandtmann, 1948, Larynissus iohanssenae Dimov, 2013 and Larynissus substerna Butenko, 1975 (PENCE, 1972Pence DB. The nasal mites of birds from Louisiana. I. Dermanyssids (Rhynonyssinae) from shore and marsh birds. J Parasitol 1972; 58(1): 153-168. PMid:5012516. http://dx.doi.org/10.2307/3278266.
http://dx.doi.org/10.2307/3278266...
; FAIN & HYLAND, 1975Fain A, Hyland KE. Speleognathinae collected from birds in North America (Acarina: Ereynetidae). J NY Entomol Soc 1975; 83(3): 203-208.; DIMOV, 2013Dimov I. A New Species of the Genus Larinyssus Strandtmann (Mesostigmata: Rhinonyssidae) from the Common Tern Sterna hirundo (Charadriiformes: Sternidae) in Russia. J Acarol Soc Jap 2013; 22(2): 123-128. http://dx.doi.org/10.2300/acari.22.123.
http://dx.doi.org/10.2300/acari.22.123...
). In T. maximus there is only the record of the mite N. philomachi (FAIN & HYLAND, 1975Fain A, Hyland KE. Speleognathinae collected from birds in North America (Acarina: Ereynetidae). J NY Entomol Soc 1975; 83(3): 203-208.).

This study aimed to report on occurrences of nasal mites in Sternidae (Aves: Charadriiformes) on the southern coast of Brazil. One hundred and six individuals belonging to the genera Sterna, Thalasseus and Sternula (terns) were collected during 2013, 2014 and 2015. Field activities were developed on Cassino beach in the municipality of Rio Grande, State of Rio Grande do Sul, along a 220 km stretch between 32° 16' 39.92” S 52° 10' 14.24” W and 34° 05' 30.28” W 53° 23' 55.48” S (Figure 1). The birds were caught by a licensed hunter using a hunting rifle and were euthanized for other studies to be developed (Ministry of the Environment license no. 39691-3). Birds species were identified following Belton (1994)Belton W. Aves do Rio Grande do Sul: distribuição e biologia. São Leopoldo: UNISINOS; 1994. and Novelli (1997)Novelli R. Aves marinhas costeiras do Brasil: identificação e biologia. Porto Alegre: Cinco Continentes; 1997..

Figure 1
Collection area of birds (Charadriiformes: Sternidae), Cassino beach, Rio Grande, State of Rio Grande do Sul, Brazil.

Nasal mites were collected using an adaptation of the technique of Fain & Hyland (1975)Fain A, Hyland KE. Speleognathinae collected from birds in North America (Acarina: Ereynetidae). J NY Entomol Soc 1975; 83(3): 203-208., as described by Amaral & Rebouças (1974)Amaral V, Rebouças MM. Métodos para o estudo de ácaros rinonissídeos. São Paulo: Instituto Biológico; 1974.. This consisted of opening the nasal cavities by means of an incision that split the nostril to the external orifice of the ear on the corresponding side, thus allowing the upper head to be opened up. The nasal cavity was washed with distilled water and its contents and mucosa were examined under a stereomicroscope. The mites were mounted in Hoyer's fluid according to Amaral & Rebouças (1974)Amaral V, Rebouças MM. Métodos para o estudo de ácaros rinonissídeos. São Paulo: Instituto Biológico; 1974. and were identified following Pence (1972)Pence DB. The nasal mites of birds from Louisiana. I. Dermanyssids (Rhynonyssinae) from shore and marsh birds. J Parasitol 1972; 58(1): 153-168. PMid:5012516. http://dx.doi.org/10.2307/3278266.
http://dx.doi.org/10.2307/3278266...
and Dimov (2013)Dimov I. A New Species of the Genus Larinyssus Strandtmann (Mesostigmata: Rhinonyssidae) from the Common Tern Sterna hirundo (Charadriiformes: Sternidae) in Russia. J Acarol Soc Jap 2013; 22(2): 123-128. http://dx.doi.org/10.2300/acari.22.123.
http://dx.doi.org/10.2300/acari.22.123...
. The prevalence of mites was calculated using the software Quantitative Parasitology 3.0.

Voucher specimens (male and female) were deposited in the Collection of Arthropods from the Laboratory of Wild Animals Parasitology of the Biology Institute, Federal University of Pelotas (n° 413-416).

Of the 106 birds analyzed, 8.5% (9 birds) were parasitized by nasal mites (49 specimens). Two species were found: S. boydi (12 mites, prevalence 4.7%) and L. orbicularis (37 mites, prevalence 4.7%) (Table 1).

Table 1
Birds of the family Sternidae collected in the southern coast of Brazil parasitized by nasal mites (Rhinonyssidae).

The low prevalence and intensity of nasal mites can be attributed to the collection period. According to Amerson (1967)Amerson AB Jr. Incidence and transfer of Rhinonyssidae (Acarina: Mesostigmata) in Sooty Terns (Sterna fuscata). J Med Entomol 1967; 4(2): 197-199. PMid:6052126. http://dx.doi.org/10.1093/jmedent/4.2.197.
http://dx.doi.org/10.1093/jmedent/4.2.19...
, the highest prevalence of Rhinonyssidae is observed during the reproductive period, until the hatching of the chicks. After this period, the prevalence and intensity of infection tend to decrease. All the birds collected were outside of their reproductive periods.

An exemplar of T. acuflavidus, was parasitized by two mite species simultaneously: L. orbicularis (nine specimens), and S. boydi (two specimens).

Sternostoma and Larinyssus seem to be the most common genera in Sternidae. Amerson (1967)Amerson AB Jr. Incidence and transfer of Rhinonyssidae (Acarina: Mesostigmata) in Sooty Terns (Sterna fuscata). J Med Entomol 1967; 4(2): 197-199. PMid:6052126. http://dx.doi.org/10.1093/jmedent/4.2.197.
http://dx.doi.org/10.1093/jmedent/4.2.19...
analyzed 460 individuals of Sterna fuscata Linnaeus, 1766, in Hawaii, and only found these two genera.

Sternostoma is among the genera with lower specificity in Rhinonyssidae. There are records of this genus in Passeriformes, Piciformes and Charadriiformes. The species S. boydi was mentioned by Pence (1972)Pence DB. The nasal mites of birds from Louisiana. I. Dermanyssids (Rhynonyssinae) from shore and marsh birds. J Parasitol 1972; 58(1): 153-168. PMid:5012516. http://dx.doi.org/10.2307/3278266.
http://dx.doi.org/10.2307/3278266...
in S. hirundo in North America, but the present study provides the first record of S. boydi in the Neotropical region and the first record of this parasite in T. acuflavidus and S. superciliaris.

Larinyssus is among the more specific genera of Rhinonyssidae. It only occurs in the family Laridae. The species L. orbicularis was also found in North America, in S. hirundo (PENCE, 1972Pence DB. The nasal mites of birds from Louisiana. I. Dermanyssids (Rhynonyssinae) from shore and marsh birds. J Parasitol 1972; 58(1): 153-168. PMid:5012516. http://dx.doi.org/10.2307/3278266.
http://dx.doi.org/10.2307/3278266...
). The present report provides the first record of L. orbicularis in the Neotropical region and the first record of this mite parasitizing S. hirundinacea and T. acuflavidus.

References

  • Amaral V, Rebouças MM. Métodos para o estudo de ácaros rinonissídeos São Paulo: Instituto Biológico; 1974.
  • Amerson AB Jr. Incidence and transfer of Rhinonyssidae (Acarina: Mesostigmata) in Sooty Terns (Sterna fuscata). J Med Entomol 1967; 4(2): 197-199. PMid:6052126. http://dx.doi.org/10.1093/jmedent/4.2.197
    » http://dx.doi.org/10.1093/jmedent/4.2.197
  • Belton W. Aves do Rio Grande do Sul: distribuição e biologia São Leopoldo: UNISINOS; 1994.
  • Dimov I. A New Species of the Genus Larinyssus Strandtmann (Mesostigmata: Rhinonyssidae) from the Common Tern Sterna hirundo (Charadriiformes: Sternidae) in Russia. J Acarol Soc Jap 2013; 22(2): 123-128. http://dx.doi.org/10.2300/acari.22.123
    » http://dx.doi.org/10.2300/acari.22.123
  • Dimov ID, Spicer GS. A new species of nasal mite of the genus Rhinonyssus (Mesostigmata: Rhinonyssidae) from Leningrad Province, Russia. Syst Appl Acarol 2013; 18(3): 291-296. http://dx.doi.org/10.11158/saa.18.3.11
    » http://dx.doi.org/10.11158/saa.18.3.11
  • Fain A, Hyland KE. Speleognathinae collected from birds in North America (Acarina: Ereynetidae). J NY Entomol Soc 1975; 83(3): 203-208.
  • Knee W, Proctor H, Galloway T. Survey of nasal mites (Rhinonyssidae, Ereynetidae, and Turbinoptidae) associated with birds in Alberta and Manitoba, Canada. Can Entomol 2008; 140(3): 364-379. http://dx.doi.org/10.4039/n08-017
    » http://dx.doi.org/10.4039/n08-017
  • Novelli R. Aves marinhas costeiras do Brasil: identificação e biologia Porto Alegre: Cinco Continentes; 1997.
  • Pence DB. The nasal mites of birds from Louisiana. I. Dermanyssids (Rhynonyssinae) from shore and marsh birds. J Parasitol 1972; 58(1): 153-168. PMid:5012516. http://dx.doi.org/10.2307/3278266
    » http://dx.doi.org/10.2307/3278266
  • Proctor HC, Owens I. Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 2000; 15(9): 358-364. PMid:10931667. http://dx.doi.org/10.1016/S0169-5347(00)01924-8
    » http://dx.doi.org/10.1016/S0169-5347(00)01924-8

Publication Dates

  • Publication in this collection
    19 Feb 2018
  • Date of issue
    Jan-Mar 2018

History

  • Received
    28 July 2017
  • Accepted
    13 Nov 2017
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