Acuariidae ( Nematoda ) in Procellariiformes ( Aves ) on the southern coast of Rio Grande do Sul , Brazil Acuariidae ( Nematoda ) em Procellariiformes ( Aves ) no litoral sul do Rio Grande do Sul , Brasil

Acuariidae nematodes are normally found in the digestive tract of aquatic birds, including Procellariiformes. Were examined Calonectris borealis (n = 4), Diomedea exulans (n = 1), Macronectes giganteus (n = 8), Thalassarche chlororhynchos (n = 5), Thalassarche melanophrys (n = 15), Procellaria aequinoctialis (n = 4), Puffinus gravis (n = 2) and Puffinus puffinus (n = 6), collected on the southern coast of RS, Brazil. A total of 16 birds (35.5%) were parasitized by two species of Acuariidae. Stegophorus diomedeae and Seuratia shipleyi were identified, with prevalences of 26.1% and 21.7%, respectively. Few studies on nematodes in Procellariiformes have been conducted. Here, the acuariids Seuratia shipleyi in Calonectris borealis and Procellaria aequinoctialis and Stegophorus diomedeae in Diomedea exulans, Procellaria aequinoctialis and Thalassarche chlororhynchos were reported for the first time.


Introduction
Acuariidae include midsized nematodes that inhabit the upper digestive tract of aquatic birds (Procellariiformes, Pelecaniformes, Ciconiiformes, Anseriformes, Charadriiformes and Coraciiformes), although a few are associated with terrestrial birds such as Falconiformes, Galliformes and Passeriformes (ANDERSON, 2000).
The species of this subfamily are characterized by the presence of cephalic cords as fixation structures (CHABAUD, 2009).
Over the life cycle of acuariids, it has been observed that larvae in the infective stage are encapsulated in the intestine or mesentery of paratenic hosts (frog or fish) to reach the final host.However, some nematodes undergo all their developmental stages within the gizzard of the definitive host, where the adults are found, while others first develop to the subadult stage in the proventriculus before migrating to the gizzard.Some esophageal parasites develop entirely in the esophagus, while others reach
the subadult stage in the proventriculus before parasitizing the esophagus.Proventricular nematodes probably undergo their entire development in this organ, and some of these species occur in seabirds.On the migration routes used by these birds, ingestion of shellfish that are intermediate hosts can contribute towards the diversity of acuariids that infect birds (ANDERSON, 2000).Acuariidae comprises Acuariinae, Schistorophinae and Seuratiinae.The subfamily Seuratiinae comprises seven genera, among which are Stegophorus and Seuratia, commonly found parasitizing seabirds in different regions (Table 1).
Procellariiformes are widely distributed seabirds, but with greater diversity of species in the southern hemisphere.This order consists of 99 species divided into four families: Procellariidae, Hydrobatidae, Pelecanoididae and Diomedeidae (SICK, 1997;IBAMA, 2006).These are predatory birds at the top of the food chain and they generally require productive waters to ensure their survival and reproduction (CURY et al., 2011).Their diet consists of squid, krill, fish, carcasses and chicks of other birds.These birds also often follow fishing boats in search of debris that has been in the sea for a long time (BARBIERI, 2008;CUBAS et al., 2014.).Presence of seabirds of the order Procellariiformes is indicative of the presence of fish shoals and hence of ecosystem health.Presence/absence of prey is reflected in changes to these birds' diet (CUBAS et al., 2014).
The coast of Rio Grande do Sul, in southern Brazil, is an important feeding site for several species of seabirds.One factor responsible for this large concentration of birds is high biological productivity, especially in winter, when a coastal branch of the Falkland current enters, bearing cold water rich in organic matter from the south (PEREZ, 2012).
Considering the ecological importance of these birds, the conservation condition of these species and the lack of information about their biology and helminth fauna, the aim of the present study was to report on occurrences of the acuariid nematodes Stegophorus diomedeae and Seuratia shipleyi as parasites of Procellariiformes on the southern coast of Rio Grande do Sul, and the infection rates in these birds.
Seuratia shipleyi had greatest mean intensity of infection and mean abundance in P. gravis (MII = 39 helminths/host and MA = 19.5),while Stegophorus diomedeae showed highest rates in D. exulans (MII = 28 helminths/host and MA = 28).However, only a few hosts belonging to this species were examined.In contrast, in T. melanophrys (n = 15), the MII and MA for both acuariid species showed low values (Table 2).Coinfection between the two acuariids was observed in four individuals (8.9% of the hosts): three specimens of Puffinus puffinus and one of P. aequinoctialis.In P. puffinus, it was observed that in the birds coinfected with these two species, S. shipleyi had higher mean intensity than S. diomedeae.

Discussion and Conclusion
Most of the studies that have reported Acuariidae in Procellariiformes have dealt with records of these helminths in different hosts and have generally only presented the prevalence index (HOBERG & RYAN, 1989;FOSTER et al., 1996).Similarly, there have been few studies on occurrences of coinfection between acuariid helminths (MENDONÇA & RODRIGUES, 1968;RODRIGUES & MENDONÇA, 1967).Mendonça and Rodrigues (1968) and Rodrigues and Mendonça (1967) observed S. shipleyi and S. diomedeae in the proventriculus of a specimen of T. melanophrys, thus indicating that coinfection with these acuariids was present.Hoberg & Ryan (1989) examined the gastrointestinal tract of P. gravis and identified S. shipleyi in the proventriculus of five birds (25%).(FOSTER et al. 1996) examined 15 specimens of P. gravis, from Florida, and reported S. shipleyi in the proventriculus and Stegophorus stellaepolaris and S. diomedeae in the ventricle, with prevalences of 60%, 20% and 93%, respectively.However, they did not report any data on coinfection.Spotorno et al. (2005) examined 51 specimens of Procellariiformes that were found dead on Cassino beach (32° 22' S; 52° 18' W), in Rio Grande do Sul.They reported that 47% were infected with nematodes, and observed injuries in the proventriculus caused by Seuratia spp. in Macronectes giganteus, they reported ulcers, epithelial and gastric gland injuries and cell necrosis in the proventriculus.In Macronectes halli, presence of Seuratia spp. was associated with granuloma in the mucosa of the proventriculus.These authors commented that the damage caused by these nematodes might, in some cases, cause infection by bacteria, thus indirectly leading these birds' death.Barbosa & Palacios (2009)

Table 1 .
Species of Seuratiinae (Nematoda: Acuariidae) recorded in birds, according to host collection site, with the respective bibliographical references.
Sala et al. (2012)es from seabirds and cited Seuratia and Stegophorus parasitizing various Charadriiformes, Procellariiformes and Sphenisciformes, but did not report the infection rates.LaSala et al. (2012)examined 103 specimens of Larus atlanticus (Charadriiformes) in Argentina between 2005 and 2006.They found the acuariids Pectinospirura argentata, Sciadiocara sp. and Skrjabinoclava andersoni parasitizing the proventriculus of these hosts, with prevalence and mean intensity of 80.3% and 23.7 helminths/infected host, and 89.2% and 50.8 helminths/infected host, in 2005 and 2006, respectively.Mild inflammation in the proventriculus was caused by these nematodes because of their mucosal adherence and associated ulcerations.This is the first record of parasitological indexes for both of these species of Acuariidae, Seuratia shipleyi and Stegophorus diomedeae, in Procellariiformes in Rio Grande do Sul, southern Brazil.It was observed that these helminths have low host specificity, since they occur not only in various species of Procellariiformes but also in Charadriiformes and Sphenisciformes.Regarding knowledge of helminth diversity in Procellariiformes, S. shipleyi is reported for the first time in Calonectris borealis, Procellaria aequinoctialis, Puffinus gravis and likewise, Stegophorus diomedeae in Diomedea exulans, P. aequinoctialis, Thalassarche chlororhynchos, Macronectes giganteus and Puffinus puffinus.