Composition and structure of the helminth community of Columba livia ( Gmelin , 1798 ) ( Aves , Columbidae ) , in the municipality of Juiz de Fora , Minas Gerais state , Brazil

The objective of the present study was to describe the composition and structure of the helminth community present in domestic pigeons, in the municipality of Juiz de Fora, Minas Gerais, Brazil. The helminthological survey of 35 hosts revealed the presence of two digenetic trematodes, Tanaisia (Paratanaisia) bragai (prevalence 51.42%, mean intensity 288.8 ± 403.86 and mean abundance 148 ± 320.9) and T. inopina (prevalence 2.85% and mean abundance 0.68 ± 4.05); five cestodes, Raillietina allomyodes (prevalence 34.28%, mean intensity 6.66 ± 9.14 and mean abundance 2.28 ± 6.11), Raillietina sp. (prevalence 37.14%, mean intensity 9 ± 10.68 and mean abundance 3.34 ± 7.7), Skrjabinia bonini (prevalence 20%, mean intensity 2.14 ± 1.21 and mean abundance 0.42 ± 1), Skrjabinia sp.( prevalence 5.7%, mean intensity 6 ± 7 and mean abundance 0.34 ± 7) and Fuhrmanneta sp. (prevalence 2.85% and mean abundance 0.028 ± 0.16) and four nematodes, Baruscapillaria obsignata (prevalence 51.42%, mean intensity 29.72 ± 44.2 and mean abundance 15.28 ± 34.7); Ascaridia columbae (prevalence 51.42%, mean intensity 60.55 ± 79.88 and mean abundance 31.14 ± 64.2); Tetrameres fissipina (prevalence 14.28%, mean intensity 346.3 ± 504.4 and mean abundance 49.42 ± 212.1) and Synhimanthus (Dyspharynx) nasuta (prevalence 2.85% and mean abundance 0.028 ± 0.16). Among the examined hosts, 97.2 % were found parasitized by at least one helminth species. In accordance with the prevalence of each species T. bragai, A. columbae and B. obsignata were considered secondary species and T. inopina, T. fissipina, S. nasuta, S. bonini, Skrjabinia sp., R. allomyodes, Raillietina sp. and Fuhrmanneta sp. were considered satellite species. All the species exhibited aggregate distributions, which is the most common distribution pattern in helminth populations.

Recently, the majority of the studies are related to either the pathology in the definitive host or the life cycles of the helminthes of columbiform birds.
Considering the lack of data on the helminth community ecology in C. livia, the objective of this study is to describe the helminth community structure in C. livia at infracommunity and component community levels.

Material and methods
Thirty-five domestic pigeons (C.livia) from the municipality of Juiz de Fora were necropsied and examined for helminth parasites.All organs and corporal cavities were examined.The specimens found were collected and prepared according to the conventional helminthological techniques (Amato et al. 1991) and subsequently identified and quantified.
The ecological terminology employed in this study was that recommended by Bush et al. (1997).The following statistical procedures and ecological indexes were used to define helminth community structure: variance to mean ratio test for each species of helminth, to determine the distribution pattern of the infrapopulations; Simpson's index for concentration for dominance (dominance was assumed when c³ 0.25).The core-satellite species concept first utilized for helminth parasite communities by Bush & Holmes (1986a, 1986b) was applied.The components of the infra communities were classified in core species (present in more than two thirds of the hosts), secondary species (present in one to two thirds of the hosts) and satellite species (present in less than one third of the hosts).
The components were also defined by attributing importance values, based in abundance and prevalence of the species (Thul et al. 1985).Brillouin index (H) for diversity was calculated for each infracommunity, including the species with prevalence higher than 10% (Bush & Holmes 1986).Spearman coefficient of correlation (p<0.05) was calculated to determine the correlation between abundance of the species that occurred in the same organ.

Component Community
Among the 35 hosts examined, 34 were parasitized by at least one helminth species, corresponding to a prevalence of 97.2%.A total of 8805 helminth specimens were collected, consisting of 225 cestodes, 3356 nematodes and 5224 digenetic trematodes.
We registered an average of 251.5 ± 401.5 parasites per infected host, with abundance amplitude of 1-1517.The infected hosts presented on average 8.3 ± 11.3 cestodes; 95.8 ± 214.1 nematodes and 290 ± 403.3 digenetic trematodes.The digenetic trematodes corresponded to 59.32 % of the total number of helminthes collected and thus it was the most important taxon, with mean abundance of 149.2 ± 320.9.
The cestodes corresponded to 2.55 % of the helminth specimens collected, with mean abundance of 6.42 ± 10.5 and the nematodes corresponded to 38.11 %, with mean abundance of 95.9 ± 214.1.
There was no obvious separation of helminthes into core species.According to the classification proposed by Bush & Holmes (1986), T. bragai, A. columbae and B. obsignata, most prevalent, were considered secondary species and T. inopina, T. fissipina, Synhimanthus (Dyspharynx) sp., S. bonini, Skrjabinia sp., R. allomyodes, Raillietina sp. and Fuhrmanneta sp. were considered satellite species.Among the satellite species, Synhimanthus (Dyspharynx) sp. and Fuhrmanneta sp. were the less prevalent.Only one female specimen of this nematode and fragments of the gravid proglotids of this cestode were found and, for this reason, it was unfeasible to accomplish their identification at species level.
All helminth species of the community showed aggregated distribution (Table 3).There was no significant association among species of helminths.

Helminth infracommunities
Infection by only one helminth species was detected in 10 hosts (29.41% of parasitized hosts).Infections by more than one helminth species were more frequent, occurring in 70.58% of the hosts.Five hosts (14.7%) were infected by two helminth species; seven hosts (20.58%) by three species; five (14.7%) by four species and seven (20.58%) by five helminth species.
Infections by only one nematode species were more frequent (50%) than infections by one cestode species (25%) or one digenetic species (25%).The presence of nematodes was registered in 80%, 87%, 100% e 100% of the infra communities composed by two, three, four and five helminth species, respectively.Co-infection by two nematode species was more frequent (60%) than co-infection by cestode and digenetic species (20%) or by cestode and nematode species (20%).
The helminth community showed low species richness (5).The number of species in the infracommunities varied between 1 to 5 species, 2.8 ± 1.5, in average.The mean diversity was 0.33 ± 0.34 and maximum diversity was 1.06.

Discussion
The component community was characterized by the co-dominance between T. bragai, Raillietina sp., B. obsignata, T. fissipina and A. columbae, the most prevalent and abundant species, and by the presence of unsuccessful or pioneer species: T. inopina, Synhimanthus (Dyspharynx) sp., S. bonini, Skrjabinia sp., R. allomyodes and Fuhrmanneta sp.
The low prevalence of these species probably is related to a low ecological opportunity for infection, since these helminthes use intermediate hosts and thus the conclusion of their life cycles depends on the presence and abundance of these hosts in the environment.The biology of such parasites is influenced by complex ecological interactions and infecting the definitive host may be less favored in specific contexts.
The success of transmission by T. bragai, which also presents indirect life cycle, is enhanced by the capacity of the larval forms, present in the intermediate hosts, to reproduce asexually.The proliferation of the larva enhances the success of the infecting forms in colonizing the definitive host , resulting in an aggregated pattern of distribution of the sexual forms, favoring the genetic diversity and increasing the potential for adaptation to the host.
Helminth species previously described from other hosts, such as R. allomyodes and T. inopina, were also classified as unsuccessful or pioneer species.Raillietina allomyodes was described by Kotlán (1921), infecting Psittaculirostris salvadorii, in New Guinea.Rolas (1976) reported this cestode species parasitizing C. livia in Brazil, however this author did not provide data on the prevalence or intensity of infection.Probably, R. allomyodes is a pioneer species in C. livia typical of infracommunities of other host species, since it was described in other continent, in a host phylogenetically distant of C. livia (Livezey & Zusi, 2007).
The parasitism by T. inopina in C. livia was not previously registered in the literature.This trematode probably is a pioneer species in C. livia, once it was found in low prevalence (only one host infected) and utilizes land snails as intermediate hosts, which also participate in the biological cycle of T. bragai (Maldonado, 1945;Brasil & Amato, 1992;Keller & Araújo, 1992;Brandolini et al. 1997).
The present work register for the first time the occurrence of T. inopina in Minas Gerais State and is the first account for the cooccurrence between T. bragai and T. inopina in the same individual host.
From the 140 adult trematodes found in the kidney collector ducts of one individual host, Revista Brasileira de Zoociências 18(2): 45-54.2017 Helminth community of Columba livia in Juiz de Fora, MG 52.
All the T. inopina specimens showed the uterus completely filled with eggs, indicating that its biological development was not harmed and thus this species probably presents potential for colonizing this new host species.

Table 2 .
Importance value attributed to the components of the helminth infracommunities present in Columba livia, in Municipality of Juiz de Fora, Minas Gerais, Brasil.

Table 3 .
Aggregated distribution pattern of the helminth infrapopulations present in Columba livia, in Municipality of Juiz de Fora, Minas Gerais, Brasil as demonstrated by the dispersion index.