Abstract

Waterbird-mediated zoochory is one of the main ecological mechanisms by which non-flying freshwater invertebrates can disperse between isolated wetlands. Passive dispersal through gut passage inside waterbirds (endozoochory) may explain how many organisms spread in the landscape. Here, we evaluate the potential for dispersal of aquatic snails by three waterbird species in neotropical wetlands. A total of 77 faecal samples from Coscoroba coscoroba (n = 28), Dendrocygna viduata (n = 36) and Anas flavirostris (n = 13) were collected in the field and taken to the laboratory. There, the samples were examined under a stereomicroscope to check for the presence of gastropod shells. We found 496 intact gastropod shells, and Heleobia piscium was the most abundant species (n= 485). We also found two shells of Drepanotrema sp. and nine others distributed between two different morphotypes of Planorbidae. Snails were present in 20.8 % of all samples, and were more frequent in faeces of coscoroba swan (50%) than the other two bird species. Our data suggest that aquatic snails may disperse by avian endozoochory between neotropical wetlands, with vectors including migratory bird species.

Keywords:
Gastropods; waterfowl; wetlands; neotropics

Resumo

A zoocoria mediada por aves aquáticas é um dos principais processos ecológicos que explicam como invertebrados não-voadores habitantes de água doce se dispersam entre áreas úmidas isoladas. A dispersão passiva que ocorre através no interior dos intestinos de aves aquáticas (endozoocoria) pode explicar como estes invertebrados se distribuem na paisagem. Neste trabalho, avaliamos o potencial de dispersão de caramujos aquáticos por endozoocoria promovida por três espécies de aves aquáticas em áreas úmidas neotropicais. No total, 77 amostras fecais de capororoca (Coscoroba coscoroba, n = 28), irerê (Dendrocygna viduata, n = 36) e marreca-pardinha (Anas flavirostris, n = 13) foram coletadas em campo e levadas ao laboratório. As amostras foram examinadas em estereomicroscópio para verificar a presença de conchas de gastrópodes. Encontramos 496 conchas intactas, sendo Heleobia piscium a espécie mais abundante (n = 485). Também encontramos duas conchas de Drepanotrema sp. e nove de outros dois morfotipos de Planorbidae. Os caramujos estiveram presentes em 20,8% de todas as amostras, sendo mais frequentes nas fezes do capororoca (50%). Nossos dados sugerem que caramujos aquáticos podem se dispersar por endozoocoria de aves entre áreas úmidas neotropicais, com vetores incluindo espécies de aves migratórias e residentes.

Palavras-chave:
gastrópodes; aves aquáticas; áreas úmidas; região neotropical

Introduction

How some aquatic invertebrates with low locomotion capacity became widely distributed is an issue that has long intrigued naturalists (Darwin 1859DARWIN, C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1. ed. John Murray, London, UK. p. 502., Bohonak & Jenkins 2003BOHONAK, A. J., & JENKINS, D. G. 2003. Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters, 6(8), 783_796. DOI: 10.1046/j.1461-0248.2003.00486.x
https://doi.org/10.1046/j.1461-0248.2003... , Van Leeuwen 2012 aVAN LEEUWEN, C. H. A., VAN DER VELDE, G., VAN LITH, B., & KLAASSEN, M. 2012a. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One, 7(3), e32292. DOI: 10.1371/journal.pone.0032292
https://doi.org/10.1371/journal.pone.003... , bVAN LEEUWEN, C. H. A; TOLLENAAR, M. L., & KLAASSEN, M. 2012b. Vector activity and propagule size affect dispersal potential by vertebrates. Oecologia, 170(1), 101-109. DOI: 10.1007/s00442-012-2293-0
https://doi.org/10.1007/s00442-012-2293-... ). Waterbird-mediated zoochory is one of the main ecological mechanisms by which non-flying freshwater invertebrates disperse between isolated waterbodies such as lakes and temporary ponds (Figuerola & Green 2002FIGUEROLA, J., & GREEN, A.J. 2002. Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biology, 47(3), 483_494. DOI: 10.1046/j.1365-2427.2002.00829.x
https://doi.org/10.1046/j.1365-2427.2002... ; Silva et al., in press). Global distribution, high abundance and flight capacity make waterbirds vital vectors for the dispersal of aquatic invertebrates in the landscape (Figuerola et al. 2003FIGUEROLA, J., GREEN, A. J., & SANTAMARÍA, L. 2003. Passive internal transport of aquatic organisms by waterfowl in Doñana, south-west Spain. Global Ecology and Biogeography, 12(5), 427_436. DOI: 10.1046/j.1466-822X.2003.00043.x
https://doi.org/10.1046/j.1466-822X.2003... , Brochet et al. 2010BROCHET, A. L., GUILLEMAIN, M., FRITZ, H., GAUTHIER-CLERC, M., & GREEN, A. J. 2010. Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshwater Biology, 55(6), 1262_1273. DOI: 10.1111/j.1365-2427.2009.02350.x
https://doi.org/10.1111/j.1365-2427.2009... ). Endozoochory, when whole invertebrates or their propagules are passively transported inside the animal vector, has been demonstrated for a wide spectrum of taxa, including organisms without any apparent adaptation to gut passage, such as rotifers, nematodes and dipteran larvae, and others with a resistant structure that may favour survival during stressful conditions, such as bryozoan statoblasts or whole snails (Brown 1933BROWN, C. J. D. 1933. A limnological study of certain fresh-water Polyzoa with special reference to their statoblasts. Transactions of the American Microscopical Society, 52(4), 271_316. DOI: 10.2307/3222415
https://doi.org/10.2307/3222415... , Proctor 1964PROCTOR, V. W. 1964. Viability of crustacean eggs recovered from ducks. Ecology, 45(3), 656_658. DOI: 10.2307/1936124
https://doi.org/10.2307/1936124... , Malone 1965aMALONE, C. R. 1965A. Dispersal of aquatic gastropods via the intestinal tract of water birds. Nautilus, 78(4), 135_139., 1965bMALONE, C. R. 1965B. Dispersal of plankton: rate of food passage in mallard ducks. The Journal of Wildlife Management, 29(3), 529_533. DOI: 10.2307/3798052
https://doi.org/10.2307/3798052... , Green & Figuerola 2005GREEN, A. J., & FIGUEROLA, J. 2005. Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Diversity and Distributions, 11(2), 149_156. DOI: 10.1111/j.1366-9516.2005.00147.x
https://doi.org/10.1111/j.1366-9516.2005... , Brochet et al. 2010BROCHET, A. L., GUILLEMAIN, M., FRITZ, H., GAUTHIER-CLERC, M., & GREEN, A. J. 2010. Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshwater Biology, 55(6), 1262_1273. DOI: 10.1111/j.1365-2427.2009.02350.x
https://doi.org/10.1111/j.1365-2427.2009... , Laux & Kolsch 2014LAUX, J. J., & KOELSCH, G. 2014. Potential for passive internal dispersal: Eggs of an aquatic leaf beetle survive passage through the digestive sysyem of mallards. Ecological Entomology, 39(3), 391_394. DOI: 10.1111/een.12097
https://doi.org/10.1111/een.12097... , Simonová et al. 2016SIMONOVÁ, J., SIMON, O. P., KAPIC, S., NEHASIL, L., & HORSÀK, M. 2016. Medium-sized forest snails survive passage through birds’ digestive tract and adhere strongly to birds’ legs: more evidence for passive dispersal mechanisms. Journal of Molluscan Studies, 82(3), 422_426. DOI: 10.1093/mollus/eyw005
https://doi.org/10.1093/mollus/eyw005... , Lovas-Kiss et al. 2018LOVAS-KISS, Á., SÁNCHEZ, M. I., MOLNÁR, V. A., VALLS, L., ARMENGOL, X., MESQUITA-JOANES, F., & GREEN, A. J. 2018. Crayfish invasion facilitates dispersal of plants and invertebrates by gulls. Freshwater Biology, 63(4), 392_404. DOI: 10.1111/fwb.13080
https://doi.org/10.1111/fwb.13080... , Moreno et al. 2019MORENO, E., PÉREZ-MARTÍNEZ, C., & CONDE-PORCUNA, J. M. 2019. Dispersal of rotifers and cladocerans by waterbirds: seasonal changes and hatching success. Hydrobiologia, 834(1), 145_162. DOI: 10.1007/s10750-019-3919-6
https://doi.org/10.1007/s10750-019-3919-... , Silva et al., in press). Even fish eggs and whole plants can be dispersed by waterfowl endozoochory (Silva et al. 2018, Silva et al. 2019SILVA, G. G., WEBER, V., GREEN, A. J., HOFFMANN, P., SILVA, V. S., VOLCAN, M. V., & MALTCHIK, L. 2019. Killifish eggs can disperse via gut passage through waterfowl. Ecology, 100(11), e02774. DOI: 10.1002/ecy.2774
https://doi.org/10.1002/ecy.2774... ).

Gastropod shells are adapted to survive hard environmental conditions and mechanical stress (Chapuis & Ferdy 2012CHAPUIS, E., & FERDY, J.B. 2012. Life history traits variation in heterogeneous environment: The case of a freshwater snail resistance to pond drying. Ecology and Evolution, 2(1), 218_226. DOI: 10.1002/ece3.68
https://doi.org/10.1002/ece3.68... , Havel et al. 2012). Peculiarities of the shell provide physical and chemical resistance that may allow some gastropod species to survive inside the anoxic and high temperature environment of the bird alimentary tract after being ingested, although many shells are excreted empty (or with dead bodies in them) by birds (Cadeé 2011CADÉE, G. C. 2011. Hydrobia as “Jonah in the Whale”: shell repair after passing through the digestive tract of shelducks alive. Palaios, 26(4), 245_249. DOI: 10.2110/palo.2010.p10-095r
https://doi.org/10.2110/palo.2010.p10-09... , Wada et al. 2012WADA, S., KAWAKAMI, K., & CHIBA, S. 2012. Snails can survive passage through a bird’s digestive system. Journal of Biogeography, 39(1), 69_73. DOI: 10.1111/j.1365-2699.2011.02559.x
https://doi.org/10.1111/j.1365-2699.2011... , Van Leeuwen 2012aVAN LEEUWEN, C. H. A., VAN DER VELDE, G., VAN LITH, B., & KLAASSEN, M. 2012a. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One, 7(3), e32292. DOI: 10.1371/journal.pone.0032292
https://doi.org/10.1371/journal.pone.003... ). Avian endozoochory has been considered a plausible explanation for dispersal of some aquatic snails, such as Physella acuta (Physidae), Bithynia tentaculata (Bithyniidae) and Potamopyrgus antipodarum (Tateidae) (Alonso & Castro-Diez 2008ALONSO, A., & CASTRO-DIEZ, P. 2008. What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)?. Hydrobiologia, 614(1), 107_116. DOI: 10.1007/s10750-008-9529-3
https://doi.org/10.1007/s10750-008-9529-... , Kappes & Haase 2012KAPPES, H., & HAASE, P. 2012. Slow, but steady: dispersal of freshwater molluscs. Aquatic Sciences, 74(1), 1_14. DOI: 10.1007/s00027-011-0187-6
https://doi.org/10.1007/s00027-011-0187-... , Vinarski 2017VINARSKI, M. V. 2017. The history of an invasion: phases of the explosive spread of the physid snail Physella acuta through Europe, Transcaucasia and Central Asia. Biological Invasions, 19(4), 1299_1314. DOI: 10.1007/s10530-016-1339-3
https://doi.org/10.1007/s10530-016-1339-... ). Van Leeuwen et al. (2012 aVAN LEEUWEN, C. H. A., VAN DER VELDE, G., VAN LITH, B., & KLAASSEN, M. 2012a. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One, 7(3), e32292. DOI: 10.1371/journal.pone.0032292
https://doi.org/10.1371/journal.pone.003... , bVAN LEEUWEN, C. H. A; TOLLENAAR, M. L., & KLAASSEN, M. 2012b. Vector activity and propagule size affect dispersal potential by vertebrates. Oecologia, 170(1), 101-109. DOI: 10.1007/s00442-012-2293-0
https://doi.org/10.1007/s00442-012-2293-... ) demonstrated that whole Hydrobia ulvae (Hydrobiidae) may survive after gut passage of mallards (Anas platyrhynchos), even remaining five hours inside the bird. Considering a waterbird can fly at speeds of 50-78 km/h (Welhun 1994WELHUN, C. V. J. 1994. Flight speeds of migrating birds: a test of maximum range speed predictions from three aerodynamic equations. Behavioral Ecology, 5(1), 1_8. DOI: 10.1093/beheco/5.1.1
https://doi.org/10.1093/beheco/5.1.1... , García-Alvarez et al. 2015GARCÍA-ÁLVAREZ, A., VAN LEEUWEN, C. H. A., LUQUE, C. J., HUSSNER, A., VÉLEZ-MARTÍN, A., PÉREZ-VÁZQUEZ, A., GREEN, A. J., & CASTELLANOS, E. M. 2015. Internal transport of alien and native plants by geese and ducks: and experimental study. Freshwater Biology, 60(7), 1316_1329. DOI: 10.1111/fwb.12567
https://doi.org/10.1111/fwb.12567... , Lovas-Kiss et al. 2020LOVAS-KISS, Á., VINCZE, O., KLEYHEEG, E., SRAMKÓ, G., LACZKÓ, L., FEKETE, R., MOLNÁR V, A., & GREEN, A.J. 2020. Seed mass, hardness, and phylogeny explain the potential for endozoochory by granivorous waterbirds. Ecology and Evolution, 10(3), 1413_1424. DOI: 10.1002/ece3.5997
https://doi.org/10.1002/ece3.5997... ), we can assume that snails may be dispersed at different spatial scales, including long-distance dispersal during waterbird migration. Avian vectors have often been proposed as an explanation for the genetic structure of snail metapopulations, or the phylogeography of closely related species (Miller et al. 2006MILLER, M. P., D. E. WEIGEL, AND K. E. MOCK. 2006. Patterns of genetic structure in the endangered aquatic gastropod Valvata utahensis (Mollusca: Valvatidae) at small and large spatial scales. Freshwater Biology 51:2362-2375., Holland et al. 2007HOLLAND, B. S., AND R. H. COWIE. 2007. A geographic mosaic of passive dispersal: population structure in the endemic Hawaiian amber snail Succinea caduca (Mighels, 1845). Molecular Ecology 16:2422-2435., Zielske & Haase 2014ZIELSKE, S., AND M. HAASE. 2014. When snails inform about geology: Pliocene emergence of islands of Vanuatu indicated by a radiation of truncatelloidean freshwater gastropods (Caenogastropoda: Tateidae). Journal of Zoological Systematics and Evolutionary Research 52:217-236. DOI: 10.1111/jzs.12053
https://doi.org/10.1111/jzs.12053... ). Here, we report the occurrence of aquatic snails found in faeces of three waterfowl species, and address the potential for dispersal by waterfowl endozoochory in the neotropic region.

Material and Methods

We analysed data collected in the Coastal Plain of Rio Grande do Sul, southern Brazil, one of the most important regions for waterbird conservation in South America (Silva et al. 2021SILVA, G. G., GREEN, A. J., HOFFMAN, P., WEBER, V., STENERT, C., LOVAS‐KISS, Á., & MALTCHIK, L. (2021). Seed dispersal by neotropical waterfowl depends on bird species and seasonality. Freshwater Biology, 66(1), 78-88. DOI: 10.1111/fwb.13615
https://doi.org/10.1111/fwb.13615... ; Figure 1). We obtained faecal samples of coscoroba swan (Coscoroba coscoroba, n= 28); white-faced whistling-duck (Dendrocygna viduata, n= 36) and yellow-billed teal (Anas flavirostris, n=13) from August 2017 to December 2019 in wetlands located in Tavares and Santa Vitória do Palmar municipalities. Field sample collection and laboratory procedures followed Silva et al. (2021)SILVA, G. G., GREEN, A. J., STENERT, & MALTCHIK, L. (2021). Invertebrate dispersal by waterbird species in neotropical wetlands. Brazilian Journal of Biology, 84. DOI: https://doi.org/10.1590/1519-6984.250280 .
https://doi.org/10.1590/1519-6984.250280... . Briefly, we identified individuals or monospecific groups of three bird species resting or feeding around lake edges, and collected fresh droppings from the grass. We stored samples individually in plastic tubes and frozen (- 4 °C) to avoid fungal infestation. In the laboratory at UNISINOS University, the samples were defrosted, weighed and washed in tap water using a sieve (53 μm). The washed content was analyzed under a stereomicroscope (10x to 1.6x - 5 x of total magnification) to separate the visible snails from other material. We compared the frequency of occurrence of snails in waterfowl faeces through a Chi-square test.

Figure 1
Study region of the Coastal Plain of Rio grande do Sul, southern brazil, where waterflow faecal samples were collected (black dots).

Results

We found 496 intact shells of four different gastropod taxa, Heleobia piscium (Hydrobiidae, n= 485; Figure 2), Drepanotrema sp. (Planorbidae, n= 2; Figure 3) and nine shells of two other unidentified genera of Planorbidae. Snails were present in 20.8 % of the total samples, and were more frequent in faecal samples of coscoroba swan (57.1%; n=16) than white-faced whistling-duck (2.8%; n=1) and yellow-billed teal (7.7%, n=1). Snails were also more abundant in coscoroba swan samples (X² = 1388,2; df = 3; P < 0,001) than the other two waterfowl species, and this result was influenced by the high abundance of Heleobia piscium shells (Table 1). We confirmed the presence of snail bodies inside 68 shells of Heleobia piscium (14%), by close inspection under the microscope. The dispersed shells of Heleobia piscium had 2.9 mm length (ranging from 2.4 to 3.5 mm) and 1.9 mm width (from 2.4 to 3.5 mm). Drepanotrema sp. shells had 4.9 mm length (4.7 mm to 5.5 mm) and 1.3 mm width (1.2 mm to 1.6 mm).

Figure 2
Helobia piscium shell with parts of animal body inside, found in a faecal sample from coscoroba swan.

Figure 3
Drepanotrema sp. shell found in a faecal sample from coscoroba swan.

Discussion

Dispersal by avian endozoochory is an accepted explanation for dispersal of some aquatic snails, and the survival by gastropods of passage through avian guts has been repeatedly demonstrated (Cadeé 2011CADÉE, G. C. 2011. Hydrobia as “Jonah in the Whale”: shell repair after passing through the digestive tract of shelducks alive. Palaios, 26(4), 245_249. DOI: 10.2110/palo.2010.p10-095r
https://doi.org/10.2110/palo.2010.p10-09... , Wada et al. 2012WADA, S., KAWAKAMI, K., & CHIBA, S. 2012. Snails can survive passage through a bird’s digestive system. Journal of Biogeography, 39(1), 69_73. DOI: 10.1111/j.1365-2699.2011.02559.x
https://doi.org/10.1111/j.1365-2699.2011... , Van Leeuwen et al. 2012 aVAN LEEUWEN, C. H. A., VAN DER VELDE, G., VAN LITH, B., & KLAASSEN, M. 2012a. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One, 7(3), e32292. DOI: 10.1371/journal.pone.0032292
https://doi.org/10.1371/journal.pone.003... , Simonova et al. 2016SIMONOVÁ, J., SIMON, O. P., KAPIC, S., NEHASIL, L., & HORSÀK, M. 2016. Medium-sized forest snails survive passage through birds’ digestive tract and adhere strongly to birds’ legs: more evidence for passive dispersal mechanisms. Journal of Molluscan Studies, 82(3), 422_426. DOI: 10.1093/mollus/eyw005
https://doi.org/10.1093/mollus/eyw005... ). Although our method necessarily involved freezing of the samples, making a survival test unfeasible, our study provides evidence that endozoochory may be a valid dispersal process for four different snail taxa in wetlands of southern Brazil. Further studies in which fresh samples are analysed immediately after collection in the field are needed to assess whether these snails were indeed viable.

Some reports indicate that Heleobia piscium, the most abundant species observed in our study, is distributed in the Coastal Plain of Rio Grande do Sul and in the region of La Plata River estuary (Darrigran et al. 1998DARRIGRAN, G., MARTIN, S. M., GULLO, B., & ARMENDARIZ, L. 1998. Macroinvertebrates associated with Limnoperna fortune (Dunker, 1857) (Bivalvia, Mytillidae) in Río de La Plata, Argentina. Hydrobiologia, 367(1), 223_230. DOI: 10.1023/A:1003244603854
https://doi.org/10.1023/A:1003244603854... , Pfeifer & Pitoni 2003PFEIFER, N. T. S., & PITONI, V. L. L. 2003. Análise qualitativa estacional da fauna de moluscos límnicos no Delta do Jacuí, Rio Grande do Sul, Brasil. Biociências, 11(2), 145_158., Coimbra et al. 2013COIMBRA, H. S., SCHUCH, L. F. D., MULLER, G., GONÇALVES, C. L., ZAMBRANO, C., OYARZABAL, M. E. B., PRESTES, L. S., & MEIRELES, M. C. A. 2013. Pesquisa de trematódeos digenéticos em Heleobia spp. (Mollusca: Hydrobiidae) em área de ocorrência da Ehrlichiose monocítica equina, no Rio Grande do Sul, Brasil. Arquivos do Instituto Biológico, 80(3), 266_272., Martin & Díaz 2016MARTIN, S. M., & DIAZ, A. C. 2016. Histology and gametogenesis in Heleobia piscium (Cochliopidae) from the Multiple Use Reserve “Isla Martín García”, Buenos Aires, Argentina. PeerJ 4:e2548. DOI: 10.7717/peerj.2548
https://doi.org/10.7717/peerj.2548... ). Drepanotrema species are mostly endemic to the Neotropical region, occurring in Southern Brazil, Uruguay and Argentina (Rumi et al. 2006RUMI, A., GREGORIC, D. E. G., NÚÑEZ, V., CÉSAR, I. I., ROCHE, M. A., TASSARA, M. P., MARTÍN, S. M., & ARMENGOL, M. F. L. 2006. Freshwater gastropoda from Argentina: Species richness, distribution patterns, and an evaluation of endangered species, Malacologia, 49(1), 189_208. DOI: 10.4002/1543-8120-49.1.189
https://doi.org/10.4002/1543-8120-49.1.1... , Núñez et al. 2010NÚÑEZ, V., GREGORIC, D. E. G., & RUMI, A. 2010. Freshwater gastropod provinces from Argentina. Malacologia, 53(1), 47_60. DOI: 10.4002/040.053.0103
https://doi.org/10.4002/040.053.0103... , Martin et al. 2013MARTÍN, S. M., DÍAZ, A. C., & RUMI, A. 2013. Crescimento individual de Drepanotrema cimex (Moricand, 1839)(Pulmonata, Planorbidae) de Arenalcito, Reserva Natural de Usos Múltiples “Isla Martín García”, Argentina. Brazilian Journal of Biology, 73(4), 833_835. DOI: 10.1590/S1519-69842013000400020
https://doi.org/10.1590/S1519-6984201300... , Palasio et al. 2019PALASIO, R. G. S., XAVIER, I. G., CHIARAVALOTTI-NETO, F., & TUAN, R. 2019. Diversity of Biomphalaria spp. freshwater snails and associated molluscs in areas with schistosomiasis risk, using molecular and spatial analysis tools. Biota Neotropica, 19(4), e20190746. DOI: 10.1590/1676-0611-bn-2019-0746
https://doi.org/10.1590/1676-0611-bn-201... ). Shells of Heleobia piscium were found in faeces of coscoroba swan and white-faced whistling-duck, and Drepanotrema sp in coscoroba swan. Coscoroba swan is a migratory species and can move up to a thousand kilometres in their seasonal displacement between Argentina and Brazil (Silva et al. 2020). Similarly, white-faced whistling-duck covers hundreds of kilometres in their regular movements through the region, according to resource availability. The distributions of Heleobia piscium and Drepanotrema sp. overlap with those of coscoroba swan and white-faced whistling-duck, this being consistent with a role for these birds as vectors of snail dispersal.

Two unidentified Planorbidae morphotypes (Morphotypes I and II) showed morphology characteristic of young individuals, and for that reason the identification to a lower taxonomic level was not possible. Morphotypes I and II were found in coscoroba swan samples, and Morphotype I was also found in faeces of yellow-billed teal, a resident waterfowl that remains in the region all year-round, making local movements between wetlands separated by several km.

Waterfowl body size may lead to variation in the access to different depths for feeding, and consequently to habitat segregation between species (Pöysä, 1983; Green, 1998; Guillemain et al., 2002; Ntiamoa-Baidu et al., 1998). Despite some overlapping, this general pattern was observed for waterfowl in our study, where extremes of body size (large and small) may affect the species composition of seeds dispersed by endozoochory (Silva et al. 2021SILVA, G. G., GREEN, A. J., STENERT, & MALTCHIK, L. (2021). Invertebrate dispersal by waterbird species in neotropical wetlands. Brazilian Journal of Biology, 84. DOI: https://doi.org/10.1590/1519-6984.250280 .
https://doi.org/10.1590/1519-6984.250280... ). Coscoroba swan was the largest bird species (c.3.500 g), and had access to deepest water for feeding (c.1-1.5 m), where they often fed with the head or neck partially submerged (Silva et al., 2021SILVA, G. G., GREEN, A. J., STENERT, & MALTCHIK, L. (2021). Invertebrate dispersal by waterbird species in neotropical wetlands. Brazilian Journal of Biology, 84. DOI: https://doi.org/10.1590/1519-6984.250280 .
https://doi.org/10.1590/1519-6984.250280... ). In contrast, yellow-billed teal (c. 500 g) fed by dabbling at the surface of shallower water (c. 0.5 cm) while white-faced whistling-duck (c. 800 g) fed by submerging their head in the same deep water (Silva et al., 2021SILVA, G. G., GREEN, A. J., STENERT, & MALTCHIK, L. (2021). Invertebrate dispersal by waterbird species in neotropical wetlands. Brazilian Journal of Biology, 84. DOI: https://doi.org/10.1590/1519-6984.250280 .
https://doi.org/10.1590/1519-6984.250280... ). These differences in access to the bottom of the waterbody, combined with possible unknown differences in the preferred diet, may explain the variation in the abundance of shells among waterfowl species.

With the exception of killifish eggs that were found to be retained for at least 30 h inside the digestive tract of coscoroba swan (Silva et al., 2019SILVA, G. G., WEBER, V., GREEN, A. J., HOFFMANN, P., SILVA, V. S., VOLCAN, M. V., & MALTCHIK, L. 2019. Killifish eggs can disperse via gut passage through waterfowl. Ecology, 100(11), e02774. DOI: 10.1002/ecy.2774
https://doi.org/10.1002/ecy.2774... ), there is no information about gut retention times of any other taxa in the waterfowl species studied here. Furthermore, information about flight patterns of South American waterfowl is limited compared with North American or European species. However, considering flight speeds of 50-78 km/h (Welhun 1994WELHUN, C. V. J. 1994. Flight speeds of migrating birds: a test of maximum range speed predictions from three aerodynamic equations. Behavioral Ecology, 5(1), 1_8. DOI: 10.1093/beheco/5.1.1
https://doi.org/10.1093/beheco/5.1.1... ) and that a snail may survive at least five hours inside a waterbird (Van Leeuwen et al. 2012 aVAN LEEUWEN, C. H. A., VAN DER VELDE, G., VAN LITH, B., & KLAASSEN, M. 2012a. Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One, 7(3), e32292. DOI: 10.1371/journal.pone.0032292
https://doi.org/10.1371/journal.pone.003... ), it is possible that dispersal of snails recorded in our study may occur over long distances, especially for taxa dispersed by coscoroba swan and white-faced whistling-duck. For example, satellite tracking data from white-faced whistling-duck in Argentina found birds moving up to >600 km away from the capture site, with individuals having daily average movements of 0.1 - 23 km, and a mean of 4 km (Don Pablo Research Team 2012DON PABLO RESEARCH TEAM. 2012. Movements and resource utilization of four species of ducks captured in the mid-Paraná River Basin, Corrientes Province, Argentina. Technical Report. Cambridge, Maryland, USA. p. 115). In this case, stopover sites used during bird displacement can also be important for snail dispersal in the region. Further studies should investigate the survival during gut passage of the snails identified in our study and the success of their dispersal by waterbird endozoochory in neotropical wetlands, as previously demonstrated in other regions.

Acknowledgements

L.C.B thanks CAPES for the undergraduate scholarship. G.G.S. thanks CAPES for a doctoral scholarship. L.M. and C.S. hold Research Productivity Grants from CNPq. This research was supported by funds from UNISINOS (grant no. 02.00.023/00-0) and CNPq (grant no. 52370695-2). A.J.G. was supported by Spanish National Plan project CGL2016-76067-P (AEI/FEDER, EU), and PID2020-112774GB-I00 (AEI).

Ethics

This work was authorized by the Brazilian agency SISBIO (n° 59225-1)

Data Availability

The information necessary to replicate this study is present in the manuscript.

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