Helminths Assemblage of the bare-faced ibis, Phimosus infuscatus (Lichtenstein, 1823) (Pelecaniformes: Threskiornithidae), in southern Brazil

Birds act as hosts for a variety of parasites, many of these are unreported. The literature provides scant information on the helminth fauna of Phimosus infuscatus. The presence of helminths were investigate in 28 birds from Pelotas, Capão do Leão, and Rio Grande in Rio Grande do Sul. The preparation and identification of helminths followed protocols. Prevalence (P%), mean intensity of infection (MII), and mean abundance (MA) were estimated. The following helminths were found: Hystrichis acanthocephalicus, Dioctophyme renale (larva), Porrocaecum heteropterum, Baruscapillaria sp., Aproctella carinii, Paradeletrocephalus minor, and Cyathostoma sp. (Nematoda); Echinostomatidae gen. sp., Tanaisia valida, and Athesmia sp. (Trematoda: Digenea) and Megalacanthus sp. (Cestoda). The most prevalent species were H. acanthocephalicus, P. heteropterum, Megalacanthus sp., and Echinostomatidae gen. sp. and Megalacanthus sp. had the highest MII and MA. There was a significant difference in the prevalence of H. acantocephalicus between female and male bird hosts. We report Echinostomatidae gen. sp., T. valida, Athesmia sp., Cyathostoma sp., A. carinii, P. minor, D. renale (larva), Baruscapillaria sp., and Megalacanthus sp. for the first time in P. infuscatus in Brazil.


Introduction
Wildlife birds act as hosts for a wide variety of parasites.To date, many of which are unreported birds, especially the aquatic ones, constitute one of the fundamental groups for ecosystems, and act as excellent environmental sentinel species.They provide nourishment for other species, and help in the control of invasive plants, seed dispersal, and contribute to pollination (SICK, 2001).Moreover, aquatic birds can also disseminate pathogens including viruses, bacteria, and parasites.It is estimated that birds are the ones with the highest parasite diversity among all vertebrates (DOBSON et al., 2008), often these organisms are not seen as Helminths Assemblage of the bare-faced ibis, Phimosus infuscatus (Lichtenstein, 1823) (Pelecaniformes: Threskiornithidae), in southern Brazil
There are reports of helminths parasitizing birds from the Threskiornithidae in different parts of the world.However, the helminth fauna of Phimosus infuscatus is little known (Table 1).
The objective of this study was to investigate the prevalence, mean abundance and mean intensity of infection of helminth parasites in P. infuscatus, and compare infections between male and female hosts.
Although H. acanthocephalicus occurred in 89.28% of the birds, it had low levels of MII (3.87) and MA (3.17).In contrast, Megalacanthus sp.presented the highest parasitological indexes of  2).
With regard to the prevalence of helminth infections in male birds and female birds, it was observed that H. acanthocephalicus, P. heteropterum, Baruscapillaria sp., Echinostomatidae gen.sp., and Megalacanthus sp. were common in both males and females.There were no significant difference in the P% and MII of these helminths according to the host's genders, except for H. acanthocephalicus, which was significantly more prevalent in females (P=100%) than in males (P=66.7%)(Table 3).The helminths Cyathostoma sp., T. valida, and Athesmia sp. were found only in females, whereas D. renale (larva), P. minor, and A. carinii were found only in males with low infection rates (Table 3).

Discussion
The P%, MII, and MA indexes of H. acanthocephalicus, P. heteropterum, Echimostomatidae gen.sp., and Megalacanthus sp.suggest that these helminths are common in P. infuscatus.
These indexes may reflect prey-predator interactions as these helminths have an indirect life cycle in which intermediate hosts and/or paratenic hosts are involved and may be part of the bird's diet.
Porrocaecum spp.are ascarids that occur in the digestive tract of birds, reptiles, fish, and mammals (HARTWICH, 2009).According to Digiani & Sutton (2001), there are approximately 40 species of Porrocaecum reported to date, with the highest prevalence in wading birds from the Threskiornithidae that inhabit the Neotropical region.
Echinostomatidae Looss, 1899, consists of intestinal digeneans that occur in birds, mammals, and humans, and has a broad geographic distribution.It comprises 355 species and 50 genera.Due to its diversity, many authors report difficulties in the taxonomic identification of members of this family (KOSTADINOVA, 2005).All specimens found parasitizing P. infuscatus belong to the same species, however it was not possible their identification into genus level with the references available.In Argentina, Digiani (2000) reported Dietziella egregia (Dietz, 1909) in P. chihi (n = 62) with prevalence of 46.7%, and MII = 82.35.Dronen & Blend (2008) described Patagifer lamothei in Eudocimus albus Linnaeus, 1758 (Pelecaniformes: Threskiornithidae) (n = 8) in the State of Texas, USA with P = 25% and MII = 6.Both birds have very similar habits to those of the avian host studied in our survey.The other helminths found in P. infuscatus had low parasitological indexes.Cyathostoma sp., P. minor, D. renale (larva), T. valida, and Athesmia sp. were found infecting one host.This finding suggests that infections may have been accidental through ingestion of intermediate or paratenic hosts.The diet of P. infuscatus is composed of annelids, molluscs, and insects (BELTON, 2003), and these invertebrates may participate in the life cycle of these helminths (Table 4).
Nematodes Syngamidae Leiper, 1912, may be present in the respiratory and digestive tracts and body cavities of mammals, rodents, and birds.They are known to live in copula, except for Cyathostoma (BORGSTEEDE & OKULEWICZ, 2001).According to Kanarek (2009), there are six species of Cyathostoma that occur in birds of different orders such as Anseriformes, Charadriiformes, Casuariiformes, Ciconiiformes, Columbiformes, Coraciiformes, Galliformes, Gaviiformes, Gruiformes, Falconiformes, Passeriformes, Pelecaniformes, Psittaciformes, Strigiformes, Struthioniformes, and Sphenisciformes.Cyathostoma phenisci (Baudet, 1937) was reported in Pelecanus erythrorhynchus Gmelin, 1789 (Pelecanidae), in North America (OVERSTREET & CURRAN, 2005).Nevertheless, these studies did not report infection rates.In the State of Florida, USA, Courtney & Forrester (1974) reported the occurrence of C. phenisci in Pelecanus occidentalis Linnaeus, 1766 (Pelecanidae) (n = 57), with an intensity of one to four nematodes which were present in the trachea, lungs, and air sacs.The results of the present study are similar to those reported by Courtney & Forrester (1974) since the prevalence of the infection by this nematode was considered low.The life cycle of Cyathostoma include paratenic hosts that can be ingested by P. infuscatus (Table 4).
Deletrocephalidae Chitwood, 1969, comprises Deletrocephalus Diesing, 1851, and Paradeletrocephalus Freitas & Lent, 1947, which include species commonly found in the large intestine of ratites.They have been often reported in the greater rhea Rhea americana (Linnaeus, 1758) (Rheiformes: Rheidae) in Brazil, Argentina, and Europe (GORDO et al., 2002;ACOMOLLI et al., 2006;HOFFMANN et al., 2009).The association between P. minor and P. infuscatus may be related to the bird's feeding habits and habitat.The low parasitological indexes in P. infuscatus and the biology of members of Deletrocephalidae (Table 4) suggest that infections may have been accidental.
Likewise, infection by a larva of Dioctophyme renale (Goeze, 1782) in an avian host may be considered accidental.This nematode is a parasite of wild and domestic mammals and has aquatic oligochaetes, anurans, and fish as intermediate and paratenic hosts, respectively (Table 4) (ANDERSON, 2000).
The diet of P. infuscatus is composed of annelids, molluscs, and insects (BELTON, 2003) which are the intermediate or paratenic hosts (or both) (Table 4) of many of the helminths reported in this survey.
The presence of helminth infections in males and females of endothermic hosts may indicate that the highest prevalence is due to morphological, physiological, and behavioral aspects such as territorialism and social interaction which may vary throughout the life of the host (POULIN, 1996).
The low prevalence of some helminth species may be related to low levels of natural infection and low availability of intermediate hosts in the environment (ROBINSON et al., 2008).
In the State of Rio Grande do Sul, studies carried out in Turdus rufiventris Vieillot, 1818, (Passeriformes: Turdidae) (n=151) (CALEGARO-MARQUES & AMATO, 2010) and in Phalacrocorax brasilianus (Gmelin, 1789) (Suliformes: Phalacrocoracidae) (n = 47) (MONTEIRO et al., 2011) assessed the correlation between the gender of hosts and the occurrence of helminth infections.There were no differences between males and females in terms of the composition and parasitological indexes of helminths.These results are similar to those found in P. infuscatus and is attributed to the similar diet and the habitat shared by males and females.

Conclusions
The infection rates allow us to conclude that helminths Hystrichis acanthocephalicus, Porrocaecum heteropterum, Echinostomatidae gen.sp., and Megalacanthus sp. are common in the assembly of P. infuscatus from southern Brazil.
With regard to male and female avian hosts, both have a similar helminth fauna, except for H. acanthocephalicus, which was more prevalent in females.

Table 1 .
Helminth fauna of the bare-faced ibis Phimosus infuscatus in South America.

Table 2 .
Helminths of Phimosus infuscatus (n=28) in southern Brazil and their respective infection sites and parasitological indexes.

Table 3 .
Parasitological indexes in male and female Phimosus infuscatus in southern Brazil.

Table 4 .
Helminth parasites of Phimosus infuscatus in southern Brazil and their respective intermediate and paratenic hosts, considering the information available for life cycles of congeners species or species of the same family.