Occurrence of gastrointestinal and renal helminths inZenaida auriculata (Des Murs, 1847) trap-captured from Brazil

Ocorrência de helmintos gastrintestinais e renais emZenaida auriculata (Des Murs, 1847) capturados no Brasil

Alessandra Taroda Luiz Daniel de Barros Dauton Luiz Zulpo Ivo Alexandre Leme da Cunha Milaine Cristiane Dantas Custódio Paiva Ana Sue Sammi Joeleni Rosa dos Santos Milton Hissashi Yamamura Odilon Vidotto João Luis Garcia About the authors

Abstracts

This study aimed to determine the prevalence of gastrointestinal and renal helminths from naturally infected Zenaida auriculatacaptured in Londrina, Paraná State. Two hundred and one Eared doves were trapped and the gastrointestinal and renal helminths were collected and identified according to morphological structures. One hundred and sixteen (57.71%) doves were parasitized by helminths with specific prevalences forOrnithostrongylus quadriradiatus in 50 doves (24.88%),Ascaridia columbae in 47 (23.38%), Paratanaisia bragai and P. confusa in 34 (16.92%),Tetrameres fissispina in 17 (8.46%), Synhimantus nasuta in 14 (6.47%), Brachylaima mazzantii in 4 (1.99%) and Raillietina allomyodes in 2 doves (1.00%). Seventy four/201 (37.00%) birds were infected with only one species, and 96/201 (48.00%) pigeons were infected with nematodes. The association between different classes of helminths occurred in 40/201 (20.00%) animals. The results showed statistically differences between the presence of nematode (p = 0.00001) and trematode species (p ≤ 0.05) in the doves, and there was an association between the local of capture and the presence of trematodes and A. columbae (p ≤ 0.05). This study is the first to report the infection of Z. auriculata from Brazil with O. quadriradiatus, A. columbae, T. fissispina, S. nasuta, R. allomyodes, P. bragai and P. confusa.

Pigeon; eared dove; occurrence; worms; systematics


O objetivo deste estudo foi determinar a prevalência de helmintos gastrintestinais e renais de Zenaida auriculata naturalmente infectados capturados em Londrina, Paraná. Duzentos e um pombos-de-bando foram capturados e os helmintos gastrintestinais e renais foram coletados e identificados de acordo com as estruturas morfológicas. Cento e dezesseis (57,71%) pombos estavam parasitados por helmintos com as seguintes prevalências:Ornithostrongylus quadriradiatus em 50 pombos (24,88%), seguido por Ascaridia columbae em 47 (23,38%),Paratanaisia bragai e P. confusa em 34 (16,92%), Tetrameres fissispina em 17 (8,46%),Synhimantus nasuta em 14 (6,47%), Brachylaima mazzantii em 4 (1,99%) e Raillietina allomyodes em 2 pombos (1,00%). Setenta e quatro/201 (37,00%) aves apresentaram-se infectadas por apenas uma espécie, e 96/201 (48,00%) pombos com nematodas. A associação entre diferentes classes de helmintos ocorreu em 40/201 (20,00%) animais. Os resultados mostraram diferenças estatísticas entre a presença de nematodas (p = 0,00001) e trematodas (p ≤ 0,05) em pombos, e houve associação entre o local de captura e a presença de trematodas e A. columbae (p ≤ 0,05). Este trabalho é o primeiro a relatar a infecção de Z. auriculata no Brasil com O. quadriradiatus,A. columbae, T. fissispina, S. nasuta, R. allomyodes, P. bragaie P. confusa.

Pombo; pombo-de-bando; ocorrência; vermes; sistemática


Introduction

Zenaida auriculata (Des Murs, 1847) (Aves: Columbiforme) is endemic to an area ranging from Antilles to Tierra del Fuego, passing through Brazil. This dove is popularly known as the eared dove (CÂNDIDO et al., 2008; SHIBATTA et al., 2009Shibatta OA, Galves W, Carmo WPD, Lima IP, Lopes EV, Machado RA. A fauna de vertebrados do campus da Universidade Estadual de Londrina, região norte do Estado do Paraná, Brasil. Semina: Cienc Biol Saude 2009; 30(1): 3-26.) and is found in fields, farms and urban areas (CÂNDIDO et al., 2008), where it can cause damage and potentially transmit pathogens (SHIBATTA et al., 2009Shibatta OA, Galves W, Carmo WPD, Lima IP, Lopes EV, Machado RA. A fauna de vertebrados do campus da Universidade Estadual de Londrina, região norte do Estado do Paraná, Brasil. Semina: Cienc Biol Saude 2009; 30(1): 3-26.).

Of the numerous health problems that can affect pigeons, parasite infections may be the most important (MARQUES et al., 2007Marques SMT, Quadros RM, Silva CJ, Baldo M. Parasites of pigeons (Columba livia) in urban areas of Lages, Southern Brazil. Parasitol Latinoam 2007; 62(3-4): 183-187.). Little is known of the species of gastrointestinal parasites that infect these birds (MARQUES et al., 2007Marques SMT, Quadros RM, Silva CJ, Baldo M. Parasites of pigeons (Columba livia) in urban areas of Lages, Southern Brazil. Parasitol Latinoam 2007; 62(3-4): 183-187.).

There are very few studies on the presence of gastrointestinal helminths in Z. auriculata; Travassos and Freitas (1942)Travassos L, Freitas JFT. Relatório da sexta excursão do Instituto Oswaldo Cruz, realizada à zona da Estrada de Ferro Noroeste do Brasil, em novembro de 1941. Mem Inst Oswaldo Cruz 1942; 37(3): 259-286. http://dx.doi.org/10.1590/S0074-02761942000300004
http://dx.doi.org/10.1590/S0074-02761942...
documented gastrointestinal helminths of doves in Brazil's Northeast Railroad; Adriano et al. (2001)Adriano EA, Thyssen PJ, Cordeiro NS. Brachylaima mazzantii (Trematoda): first record in Zenaida auriculata (Aves: Columbidae). Bol Chil Parasitol 2001; 56(1-2): 34-35. PMid:12058672. http://dx.doi.org/10.4067/S0365-94022001000100009
http://dx.doi.org/10.4067/S0365-94022001...
reported the presence of the trematode Brachylaima mazzantii in the small intestine of this dove at Junqueirópolis-SP. Additionally, Durette-Desset et al. (2000)Durette-Desset MC, Guerrero RA, Boyer J. Two Trichostrongylina (Nematoda) from Venezuela: a new species of Ornithostrongylus (Heligmosomoidea), parasitic in birds (Columbiformes) and a new species of Molineus (Molineoidea), parasitic in snakes (Squammata). Zoosystema 2000; 22(1): 5-14. described the presence of a new species of helminth, Ornithostrongylus volcani n. sp., in doves in Venezuela. The only study on the prevalence of helminths in Z. auriculata was conducted in Chile by González et al. (2004)González D, Daugschies A, Rubilar L, Pohlmeyer K, Skewes O, Mey E. Fauna parasitaria de la tórtola común (Zenaida auriculata, Des Murs 1847) (Columbiformes: Columbidae) en Ñuble, Chile. Parasitol Latinoam 2004; 59: 37-41. http://dx.doi.org/10.4067/S0717-77122004000100007
http://dx.doi.org/10.4067/S0717-77122004...
; these authors encountered Killigrewia delafondi (9.4%),Raillietina sp. (1.7%), Heterakis gallinarum(0.4%) and Echinostomum sp. (0.9%).

The aim of the present study was to determine the prevalence of gastrointestinal and renal helminths in naturally infected Z. auriculata captured in the city of Londrina, Paraná State.

Materials and Methods

Study area and host data collection

Londrina is located in the north of Paraná state, southern Brazil (23°08′47″ and 23°55′46″ S, 50°52′23″ and 51°19′11″ W) (IBGE, 2010). Two hundred and one doves (Z. auriculata) were captured using gauze-traps from January 2010 to June 2011. These animals were collected from three different areas: 140 birds from a soybean seed industry, 45 from the campus of State University of Londrina, and 16 from a dairy cattle farm. This work was approved by the Brazilian Institute of Environment (IBAMA) SISBIO N. 16428-1 and by the Ethics Committee of Animal Experiments of the State University of Londrina no. 70/2008.

Helminth data collection

The animals were euthanized in a CO2 chamber, and their gastrointestinal tracts were removed and opened from the esophagus to the cloaca. The esophagi, crops, proventriculi, gizzards, small intestines and large intestines were individualized and placed in Petri dishes with 0.9% saline solution. Each organ was cut lengthwise and scanned for helminths. The helminths were removed from the crop and proventriculus after a detailed examination. The gastrointestinal content was taken from the mucosa, washed and passed through sieves with apertures of 600 µm, 425 µm and 150 µm (PAVANELLI; FERNANDES, 1982Pavanelli GC, Fernandes BF. Helmintofauna de Gallus gallus domesticus (Linneus, 1758) (Galliformes, Phasianidae) de criação extensiva no município de Maringá – PR. Rev Set Cienc Agrar 1982, 4: 55-59.) for the separation of the helminths. The kidneys were removed from the abdominal cavity and cut lengthwise, and the renal tubules were slightly compressed to obtain the helminths.

Permanent slides preparation and identification

To prepare permanent slides of the parasites, the helminths were refrigerated for 24 hours (PAVANELLI; FERNANDES, 1982Pavanelli GC, Fernandes BF. Helmintofauna de Gallus gallus domesticus (Linneus, 1758) (Galliformes, Phasianidae) de criação extensiva no município de Maringá – PR. Rev Set Cienc Agrar 1982, 4: 55-59.). The nematodes were placed in 37 °C Railliet-Henry solution for fixation, while the cestodes and trematodes were pressed between glass slides and dipped in Railliet-Henry solution (TRAVASSOS, 1950). Subsequently, the nematodes were cleared in Hoyer solution and a slide and coverslip were prepared according to the method described by Sloss et al. (1999). The thin nematodes were stained with lactophenol cotton blue (TRAVASSOS, 1950) before the slide preparation. The cestodes and trematodes were washed for five hours in distilled water, stained with Carmine Mayer, then sallowed with acid alcohol and dehydrated in alcoholic series. After the dehydration, the cestodes and trematodes were cleared in Hoyer solution and placed between the slide and coverslip for observation by optic microscopy (PESSOA, 1967). Helminth specimens were identified following taxonomic keys of Travassos (1913Travassos L. Sobre as especies brazileiras da subfamilia Heterakinae Railliet & Henry. Mem Inst Oswaldo Cruz 1913; 5(3): 271-323. http://dx.doi.org/10.1590/S0074-02761913000300005
http://dx.doi.org/10.1590/S0074-02761913...
, 1914Travassos L. Contribuições para o conhecimento da fauna helmintolojica brazileira III. Sobre as espécies do gênero Tetrameres Creplin, 1846. Mem Inst Oswaldo Cruz 1914; 6(3): 150-162., 1919Travassos L. Contribuições para o conhecimento da fauna helmintolojica brazileira VIII. Sobre as espécies do gênero Tetrameres Creplin, 1846. Mem Inst Oswaldo Cruz 1919; 11(1): 71-79., 1921)Travassos L. Contribuições Para O Conhecimento Da Fauna Helmintolojica Brazileira XIII. Ensaio Monográfico Da Família Trichostrongylidae. Mem Inst Oswaldo Cruz 1921; 13(1): 5-135., Yamaguti (1958Yamaguti S. Systema helminthum, Vol. I: The Digenetic Trematodes of Vertebrates. Part I and II. New York: Interscience. Publishers, Inc.; 1958., 1959Yamaguti S. Systema helminthum, Vol. II: The Cestodes of Vertebrates. Part I and II. New York: Interscience. Publishers, Inc.; 1959., 1961)Yamaguti S. Systema helminthum, Vol. III: The Nematodes of Vertebrates. Part I and II. New York: Interscience. Publishers, Inc.; 1961., Travassos and Kohn (1966)Travassos L, Kohn A. Lista dos gêneros incluídos na super-família Brachylaemoidea. Mem Inst Oswaldo Cruz 1966; 64: 11-25. http://dx.doi.org/10.1590/S0074-02761966000100002
http://dx.doi.org/10.1590/S0074-02761966...
, Travassos et al. (1969), Vicente et al. (1995) and Saif et al. (2008).

Statistical analysis

The terms prevalence (P), abundance (A) and mean intensity of parasitism (MI) follow the definitions of Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
http://dx.doi.org/10.2307/3284227...
, and these parameters were evaluated in Microsoft Excel 2007 (Microsoft Corporation, Redmond, Washington, USA). Chi square (χ2) test corrected by Yates was used to compare the variables (Epi Info Program, version 6.04). A P-value of ≤0.05 was considered significant.

Results

In the proventriculi, were found Synhimantus nasuta andTetrameres fissispina; in the renal tubules, it was encounteredParatanaisia bragai and P. confusa. No worms were found in the esophagi, crops, gizzards or large intestines. Eighty six (42.79%) small intestines, 34 (16.92%) renal tubules and 23 (11.44%) proventriculi were parasitized. P. bragai and P. confusa were present together in all 23 renal tubules.

Ornithostrongylus quadriradiatus was the most prevalent species and occurred in 24.88% of the eared doves; A. columbae was the second most prevalent species and was encountered in 23.38% of the doves. However,P. bragai + P. confusa had the highest mean intensity of parasitism (220.62). Table 1presents the number of parasitized animals, the prevalence, the abundance, the mean intensity of parasitism and the range of parasitism of the species. There were significant differences when nematodes O. quadriradiatus,A. columbae, S. nasuta and T. fissispina were compared. Adittionally, when the presence of trematodes was studied (Table 1), the doves had 10.03 times-higher P. bragai + P. confusa thanB. mazzantii (OR = 10.03, 3.46<OR<39.51, p<0.05).

Table 1.
Prevalence, abundance, mean intensity of parasitism, the range of parasitism, the total of helminths collected, Odds ratio and p-value inZenaida auriculata in Londrina, 2013.

Of the 201 captured doves, 97/201 (48.26%) were male and 104/201 (51.74%) were female. A total of 49/97 (50.52%) of the males and 67/104 (64.42%) of the females had parasites. Both male and female doves presented each class of helminth in the gastrointestinal tract and renal tubules. However, 25 females had trematodes and only 13 males presented this class (Table 2). There were no differences between male and female doves considering the infection from Class Nematoda (p>0.10) and Class Trematoda (p>0.08).

Table 2.
Prevalence, abundance, mean intensity of parasitism, the range of parasitism, the total of helminthes collected, Odds ratio and p-value in male and female Zenaida auriculata in Londrina, 2013.

Association between the parasites and the locality of trap capture is shown in Table 3. The parasites from Class Nematoda were taking all together and compared with place of trap capture, and no differences were observed (p>0.06), however, A. columbae was more frequent in dairy farms (p = 0.005). In Trematoda class the soybean industry had a higher prevalence than University (OR = 0.21, 0.04<OR<0.74, p = 0.01). This occur by the fact that P. bragai + P. confusawere found just in the industry (p = 0.00025), additionally, no trematodes were observed in dairy farms.

Table 3.
Outcome of association between the local of capture and helminths found in Zenaida auriculata, Londrina, 2013.

It was observed that among the positive birds, they had one to four different species of helminths in the gastrointestinal tract and renal tubules. The majority of infected Z. auriculata 74/201 (37.00%) were parasitized with one species of parasite. The Nematoda class was the most frequently encountered class of parasite, found in 96/201 (48.00%) doves, followed by the Trematoda class in 38/201 (19.00%) doves and the Cestoda class in 2/201 (1.00%) doves.

Discussion

A few studies on Z. auriculata helminths have been conducted worldwide. To the authors' knowledge, however, the data on prevalence, abundance, and mean intensity of parasitism of helminths in Z. auriculata have not previously been collected.

Lee et al. (2004)Lee KA, Franson JC, Kilsella JM, Hollmén T, Hansen SP, Hollmén A. Intestinal helminths in mourning doves (Zenaida macroura) from Arizona, Pennsylvania, South Carolina and Tennessee, U.S.A. Comp Parasitol 2004; 71(1): 81-85. http://dx.doi.org/10.1654/4091
http://dx.doi.org/10.1654/4091...
worked with Z. macroura in the USA and they did not observe differences between local of capture, and sex of those birds compared with the presence of helminths. In a different study, with another species of bird, Z. asiatica, Glass et al. (2002)Glass JW, Fedynich AM, Small MF, Benn SJ. Helminth community structure in an expanding white-winged dove (Zenaida asiatica asiatica) population. J Wildl Dis 2002; 38(1): 68-74. PMid:11838230. showed that helminths may be found equally in both sex. Those results are similar to what we observed in the present study.

The presence of A. columbae in doves from dairy farm was higher than other localities in our study, and this was observed previously (GLASS et al., 2002Glass JW, Fedynich AM, Small MF, Benn SJ. Helminth community structure in an expanding white-winged dove (Zenaida asiatica asiatica) population. J Wildl Dis 2002; 38(1): 68-74. PMid:11838230.). In fact, the environment is more complex in farms and the presence of others intermediate hosts, which are important for such parasites, could explain this. However, we need further evaluation.

Helminth prevalences described in Zenaida doves ranged from 2.75% to 93.34% in Z. macroura doves (BARROWS; HAYES, 1977Barrows PL, Hayes FA. Studies on endoparasites of the mourning dove (Zenaida macroura) in the Southeast United States. J Wildl Dis 1977; 13(1): 24-28. PMid:402483.; CONTI; FORRESTER, 1981; LEE et al., 2004Lee KA, Franson JC, Kilsella JM, Hollmén T, Hansen SP, Hollmén A. Intestinal helminths in mourning doves (Zenaida macroura) from Arizona, Pennsylvania, South Carolina and Tennessee, U.S.A. Comp Parasitol 2004; 71(1): 81-85. http://dx.doi.org/10.1654/4091
http://dx.doi.org/10.1654/4091...
), and from 50.29% to 95.6% inZ. asiatica doves (CONTI; FORRESTER, 1981; GLASS et al., 2002Glass JW, Fedynich AM, Small MF, Benn SJ. Helminth community structure in an expanding white-winged dove (Zenaida asiatica asiatica) population. J Wildl Dis 2002; 38(1): 68-74. PMid:11838230.). González et al. (2004)González D, Daugschies A, Rubilar L, Pohlmeyer K, Skewes O, Mey E. Fauna parasitaria de la tórtola común (Zenaida auriculata, Des Murs 1847) (Columbiformes: Columbidae) en Ñuble, Chile. Parasitol Latinoam 2004; 59: 37-41. http://dx.doi.org/10.4067/S0717-77122004000100007
http://dx.doi.org/10.4067/S0717-77122004...
studied Z. auriculatain Chile but reported the prevalence of each species of helminths rather than the prevalence of infected doves.

We observed a higher number of parasites of the Trematoda class in doves captured at the soybean industry; this finding could be related to a higher occurrence of intermediate hosts at this site, but other studies must be conducted to confirm this hypothesis. According to Freitas (1979), gastropod mollusks are intermediate hosts in the life cycles of cestodes and trematodes. Sick (1997) affirmed that Z. auriculata feeds on mollusks and diplopods during the reproduction season, suggesting that these birds require the ingestion of animal protein and calcium during this period.

The majority of the animals infected with helminths in this study had single infections (37.00%); only 21% of the birds had multiple infections. The most found mixed infection was between A. columbae and O quadriradiatus. Lee et al. (2004)Lee KA, Franson JC, Kilsella JM, Hollmén T, Hansen SP, Hollmén A. Intestinal helminths in mourning doves (Zenaida macroura) from Arizona, Pennsylvania, South Carolina and Tennessee, U.S.A. Comp Parasitol 2004; 71(1): 81-85. http://dx.doi.org/10.1654/4091
http://dx.doi.org/10.1654/4091...
also reported this helminth association in Z. macroura.

Conclusions

This study is the first to describe the occurrence of A. columbae, T. fissispina, S. nasuta,R. allomyodes, P. bragai and P. confusa in Z. auriculata from Brazil. More studies should be conducted to determine whether these doves represent sources of infection for other birds because none of the parasites observed in this study were species specific.

This study received financial support from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, AUXPE-PARASITOLOGIA-1345/2011,10259/12-0). J.L. Garcia and O. Vidotto are recipients of CNPq fellowships.

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Publication Dates

  • Publication in this collection
    Jul-Sep 2013

History

  • Received
    30 May 2013
  • Accepted
    23 July 2013
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