Gastropod species found in birds ’ nests from Argentina

Bird’s nests are specialized habitats that are inhabited by a diverse suite of invertebrates, such as insects, spiders, pseudoscorpions, and ticks. This study presents a list of gastropods found in birds’ nests from Argentina for the first time. A total of 138 specimens of gastropods, belonging to 11 species, 10 genera and 8 families of snails were present in the nests of 42 birds from 6 families in 6 provinces in Argentina. Fifty eight specimens of the snail Pupisoma latens of different sizes were found alive in a nest, representing a new habitat for this species, which has been previously described from the aerial parts of trees. The remaining species were represented by dead specimens (fragments or empty shells), which can be tentatively attributed to bird diets. Among these, the most abundant species were Bulimulus bonariensis bonariensis and Succinea meridionalis, both as pre-adults. The nests Anumbius annumbi and Furnarius rufus from the province of Buenos Aires had the highest number of specimens. Freshwater snails (Heleobia parchappii, Biomphalaria sp., and Drepanotrema sp.) comprised 13% of the snail species found.


INTRODUCTION
The nests of birds constitute a microenvironment that provides organic material and shelter for a diverse suite of invertebrates (insects, spiders, pseudoscorpions, and ticks), which inhabit these nests in varying abundance (Di Iorio & Turienzo, 2009Turienzo, , 2011;;Turienzo & Di Iorio, 2008, 2010, 2011, 2014a).Nevertheless, data about the occurrence of American gastropods in birds' nests are scarcely found in literature (Appendix 1).
The probable causes of the presence of snails in bird's nests were in part suggested by Judd (1963) and Nolan (1959).Judd (1963) reported, "most of the snails were in nests constructed in flood debris or in trees and shrubs at the river's edge."One species found in the nests is "among the commonest snail in flood debris, another is found among damp under leaves in densely shaded places, a third is found on low ground near streams, and a fourth, "the snail found most commonly in the nests, as well as being in nests along the river, is also found climbing trees".Thus, in these cases, birds' nests also serve as an extension of the natural habitat of the species already present on the branches and foliage.
According to Nolan (1959), Roscoe (1955) tells of the discovery of aquatic snails on birds' plumage.Ramsden (1914), McAtee (1914), andPaton &Williamson (1943) refer to similar episodes involving terrestrial snails, i.e. that the snails are involuntarily transported by the birds.Vagvolgyi (1975) postulated that a species of petrel could be responsible for the introduction of the micromolusk Nesopupa galapagensis Vagvolgyi, 1974 to the Galápagos Islands (Miquel & Herrera, 2014).The physiological and/or behavioral features of each species must be considered, e.g., the characteristics of the pedal mucus of species of Succinea, which is particularly adhesive, could help the passive transport of this gastropod (Vagvolgyi, 1975).In recent years, it was observed that operculate gastropods can survive the passage through the digestive tract of birds (Kawakami et al., 2008;van Leeuwen et al.,2012;Wada et al.,2012;Rusiecki & Rusiecka, 2013).
This study presents the first records of ter- restrial gastropods found in avian nests from Argentina, alive or dead, in Argentina.The purpose of this work is to present new information about the existence of a relationship between birds and continental mollusks, which could provide information about the spreading of gastropods by avian species.

MATERIALS AND METHODS
Extensive research on invertebrate communities in birds' nests from Argentina was undertaken between 2005 and 2010, encompassing a total of 695 nests belonging to 13 bird families from 14 provinces (Turienzo & Di Iorio, 2014b).Nest identifications were made following the nest descriptions of De la Peña (1987, 2005) and Narosky et al. (1983), and by the observation of the birds following Narosky & Yzurieta (2003).Each nest was entirely removed from the tree branches, placed in a bag, and taken to the laboratory where it was dissected.All invertebrates were manually collected and preserved by P.  (Reichenbach, 1853) [Furnariidae], the nests of this last species remodeled and occupied by Myiopsitta monachus catita (Olrog, 1976) [Psittacidae]; Passer domesticus (L., 1758) [Passeridae], outside and inside the nests of F. rufus; Myiopsitta monachus catita Olrog, 1976 [Psittacidae]; Sicalis flaveola pelzelni Sclater, 1872 [Aves: Thraupidae], inside the nests of F. rufus; Turdus amaurochalinus Cabanis, 1850 [Aves: Turdidae], and in one undetermined nest of an inquiline bird inside a nest of F. rufus (Table 1).
A total of 138 gastropods were found in 42 nests, representing 6.04 % of the whole sampled nests (Turienzo & Di Iorio, 2014b), belonging to 14 species in seven families of birds from six Argentine provinces (Table 1).About 69 % of the positive nests were of birds in the family Furnariidae (n = 29), especially in 13 nests of A. annumbi.The nests of F. rufus are closed domed nests build with mud, which eventually serves as nidification sites for other birds, such as S. f. pelzelni, P. domesticus and P. chalybea, where also snails were found, as well as in nests of F. rufus without inquiline birds (Table 1).
The snails were distributed across 11 species, 10 genera and 8 families.Out of this total, 7 species were soil-related, and 4 taxa were limnic species (Table 2).The average number of snails by bird species was 6.66.However, Pupisoma latens accounted for 58 live specimens in a single nest.All the remaining gastropods were collected as empty shells, with a low abundance (1.86 shells by nest).Thirty percent of the specimens were fragmented shells.
Remark.The analyzed specimens were adults, ranging between 4 to 5 mm in length with seven to eight whorls.Planorbidae Biomphalaria sp.

Pupisoma latens
Remarks.The analyzed specimens ranged from 1.3 to 4.5 mm in size.This species was preliminarily considered to be conspecific with P. comicolense (Baker, 1928) by Hausdorf (2007), because there are apparently intermediate specimens between the extreme forms of the latter.This taxonomic statement requires further research.Northern and Southern Hemispheres shows several coincidences: Pupillidae and species of Pupoides were found in both regions, though Pupoides albilabris (C.B. Adams) from Canada was found alive, while P. paredesi was found dead; Vallonidae were also found in both regions, though the species found were from different genera (Cionella Jeffreys, 1829, Gastrocopta Wollaston, 1878, Vallonia Risso, 1826, Novisuccinea Pilsbry, 1948, and others) and were, notably, found alive in birds' nests (Appendix 1).
Here only one species was found living in a bird nest, a relatively large number of snails belonging to the native species Pupisoma latens.This species is a micromollusk that lives on trees in the native forests of Cabana (Córdoba province).It is small, corneous-colored and has a few whorls (~ 3.5) (Hylton Scott, 1960).The current record in Mina Clavero extends its natural distribution to the western area of Córdoba province and confirms its presence in aerial habitats, e.g., nests of the Furnariidae Pseudoseisura lophotes as an extension of its natural habitat in the branches and leaves of trees (Hylton Scott, 1960).Another species in this genus (P.galapagorum Pilsbry, 1934) was found living in Geospizzini (finch) nests made of bryophytes and liverworts in the Galapagos Islands.
As many of the specimens were found dead (empty shells and/or fragments), they may be part of the diet of the adult birds or nestlings.This is an accidental transport, the most likely form of transporting the aquatic and terrestrial micromollusks cited here.Succinea meridionalis and Bulimulus b. bonariensis, the two largest snails registered, may be actively selected and transported by the bird as a part of its diet, but also the remaining species of snails found dead in the birds' nests can be regarded here as prey items of the respective birds.Among the dead gastropods found in the nests, Bulimulus bonariensis bonariensis was the most abundant shell, with 32 specimens (40 % of the sample) in eight nests from Chaco and Córdoba.The second most frequent species, Paralaoma servilis, was found in four nests in Buenos Aires.The less represented species were Drepanotrema sp.(Entre Ríos), Lamellaxis gracilis (La Pampa) and Pupoides paredesi (Salta), with only one specimen each.Gastropod length was not uniform and there were fewer adults than juveniles.Only 15 % of the specimens of Bulimulus b. bonariensis were adults or pre-adults, while the average total length of Succinea meridionalis specimens was 6.8 mm (size of an adult usually is over 10 mm).By the other side, only 13 % of the species were freshwater snails (genera Heleobia Stimpson, 1865, Biomphalaria Preston, 1910, and Drepanotrema Crosse & Fischer, 1880), that agree with the predation of aquatic organisms by some of these terrestrial birds recorded in literature (Turienzo & Di Iorio 2014b).

CONCLUSIONS
The snail species recorded here from Argentine bird's nests can be grouped in two classes: 1) those found living inside a nest, that may be counted as inhabitants of this habitat, and comprise a single species: Pupisoma latens, and 2) those found dead inside bird's nests, which may be tentatively counted among the food items of each bird: Heleobia parchappii, Biomphalaria sp., Drepanotrema sp., Succinea meridionalis, Pupoides paredesii, Lamellaxis (Allopeas) gracilis, Bulimulus b. bonariensis, Naesiotus deletangi, Paralaoma servilis, and Zonitoides arboreus.
Two plausible possibilities can be considered regarding the presence of empty shells in the nests.The first one is that these species were passively transported by the birds to their nests, where the snails subsequently died because of inadequate environmental conditions.The second possibility is that bird's nests function as a trap, because their location inside the natural habitats of the snails allows the snails enter them as a natural extension of their natural habitat, but the snails die, as in the first case, due to the complex structure of the nests (as in the cases of Furnariidae oven nests and Psittacidae stick nests in Argentina).Further sampling might help answer these questions, deepening the comprehension of each species' habitat and providing more information about live specimens inside birds' nests.

Table 2 .
Number of gastropods specimens (mostly shells) found in bird's nests in Argentina, shown for each avian species.* The only species found alive in a nest is Pupisoma latens.