Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Predation on eggs of the apple snail Pomacea dolioides (Reeve, 1856) in rural and urban areas of the Amazon

Aldeiza M. Fonseca A and Bruno S. Sant’Anna A B
+ Author Affiliations
- Author Affiliations

A Universidade Federal do Amazonas, Instituto de Ciências Exatas e Tecnologia, Rua Nossa Senhora do Rosário, N 3863, São Jorge, Itacoatiara, 69103-128, AM, Brasil.

B Corresponding author. Email: brunusant@hotmail.com

Marine and Freshwater Research 71(6) 662-669 https://doi.org/10.1071/MF19095
Submitted: 19 March 2019  Accepted: 17 July 2019   Published: 1 October 2019

Abstract

This study investigated the predation of eggs of the apple snail Pomacea dolioides in Itacoatiara, Amazonas, Brazil. Predation was compared between rural and urban areas, period of day, shaded and unshaded clutches. In addition, we evaluated clutch height and the behaviour of predators. Between April 2017 and July 2018, 962 egg clutches were observed at different times of the day: 492 in rural areas with predation of 68 egg clutches and 470 in urban areas with predation of only 9 egg clutches. Significant differences were recorded for predation rate and differences were recorded for egg clutch height in the areas. In the rural areas, the most frequent predators during the day were ants Solenopsis invicta, Crematogaster cf. carinata and the most abundant were S. invicta, Wasmannia aff. iheringi and C. cf. carinata. During the night, S. invicta was the most frequent and abundant predator. In urban areas, the frequency of predation and abundance of S. invicta were higher during the day and night than those of other predators. Populations of P. dolioides in rural areas are more affected by egg predation, mostly by S. invicta and C. cf. carinata, and predatory behaviour depended on the species of the predator.

Additional keywords: Ampullariidae, behaviour, natural enemy, reproduction.


References

Albrecht, E. A., Carreno, N. B., and Castro-Vaszquez, A. (1996). A quantitative study of copulation and spawning in the South American apple-snail, Pomacea canaliculata (Prosobranchia: Ampullariidae). The Veliger 39, 142–147.

Alcantara-Bocanegra, F., Valverde, N. N., and Perea, E. Z. (1996). Características del desova de churo, Pomacea maculata em ambiente controlado. Folia Amazónica 8, 7–11.
Características del desova de churo, Pomacea maculata em ambiente controlado.Crossref | GoogleScholarGoogle Scholar |

Azevedo, F. R., Moura, E. S., Azevedo, R., Santos, C. M., and Nere, D. R. (2015). Inventário da entomofauna de ecossistemas da área de proteção ambiental do Araripe com bandejas d’água amarelas. Holos 31, 121–134.
Inventário da entomofauna de ecossistemas da área de proteção ambiental do Araripe com bandejas d’água amarelas.Crossref | GoogleScholarGoogle Scholar |

Baccaro, F. B., Feitosa, R. M., Fernandez, F., Fernandes, I. O., Izzo, T. J., Souza, J. D., and Solar, R. (2015). ‘Guia para os gêneros de formigas do Brasil.’ (Editora Instituto Nacional de Pesquisas da Amazôna: Manaus, Brazil.)

Beissinger, S. R. (1983). Hunting behavior, prey selection, and energetics of snail kites in Guyana: consumer choice by a specialist. Auk 100, 84–92.

Burks, R. L., Kyle, C. H., and Trawick, M. K. (2010). Pink eggs and snails: field oviposition patterns of an invasive snail, Pomacea insularum, indicate a preference for an invasive macrophyte. Hydrobiologia 646, 243–251.
Pink eggs and snails: field oviposition patterns of an invasive snail, Pomacea insularum, indicate a preference for an invasive macrophyte.Crossref | GoogleScholarGoogle Scholar |

Cadierno, M. P., Dreon, M. S., and Heras, H. (2017). Apple snail perivitellin precursor properties help explain predators’ feeding behavior. Physiological and Biochemical Zoology 90, 461–470.
Apple snail perivitellin precursor properties help explain predators’ feeding behavior.Crossref | GoogleScholarGoogle Scholar | 28402234PubMed |

Clark, D. B., Guayasamín, C., Pazmiño, O., Donoso, C., and de Villacís, V. P. (1982). The tramp ant Wasmannia auropunctata: autecology and effects on ant diversity and distribution on Santa Cruz Island, Galapagos. Biotropica 14, 196–207.
The tramp ant Wasmannia auropunctata: autecology and effects on ant diversity and distribution on Santa Cruz Island, Galapagos.Crossref | GoogleScholarGoogle Scholar |

Cowie, R. H., and Thiengo, S. C. (2003). The apple snails of the Americas (Mollusca: Gastropoda: Ampullariidae: Asolene, Felipponea, Marisa, Pomacea, Pomella): a nomenclatural and type catalog. Malacologia 45, 41–100.

Dáttilo, W., Sibinel, N., Falcão, J. C. F., and Nunes, R. V. (2011). Ant fauna in a urban remnant of Atlantic Forest in the Municipality of Marília, State of São Paulo, Brazil. Bioscience Journal 27, 494–504.

Delabie, J. H. C., Da Encarnaçao, A. M. V., and Cazorla, I. M. (1994). Relations between the little fire ant, Wasmannia auropunctata, and its associated mealybug, Planococcus citri in Brazilian cocoa farms. In ‘Exotic Ants: Biology, Impact, and Control of Introduced Species’. (Ed, D. F. Williams.) pp. 91–103. (Westview Press: Boulder, CO, USA.)

Denno, R. F., and Lewis, D. (2009). Predator–prey interactions. In ‘The Princeton Guide to Ecology’. (Ed. S. A. Levin.) pp. 202–212. (Princeton University Press: Princeton, NJ, USA.)

Dreon, M. S., Ituarte, S., and Heras, H. (2010). The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation. PLoS One 5, e15059.
The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation.Crossref | GoogleScholarGoogle Scholar | 21151935PubMed |

Dreon, M. S., Frassa, M. V., Ceolín, M., Ituarte, S., Qiu, J. W., Sun, J., Fernández, P. E., and Heras, H. (2013). Novel animal defenses against predation: a snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins. PLoS One 8, e63782.
Novel animal defenses against predation: a snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins.Crossref | GoogleScholarGoogle Scholar | 23737950PubMed |

Fonseca, A. M., Watanabe, T. T., Hattori, G. Y., and Sant’Anna, B. S. (2017a). Effects of the dry season on two apple snails of the Amazon. In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori.) pp. 155–176. (NOVA Science Publishes: New York, NY, USA.)

Fonseca, A. M., Hattori, G. Y., and Sant’Anna, B. S. (2017b). Imposex in two apple snails of the Amazon. In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori.) pp. 47–66. (NOVA Science Publishes: New York, NY, USA.)

Geffeney, S., Brodie, E. D., and Ruben, P. C. (2002). Mechanisms of adaptation in a predator–prey arms race: TTX-resistant sodium channels. Science 297, 1336–1339.
Mechanisms of adaptation in a predator–prey arms race: TTX-resistant sodium channels.Crossref | GoogleScholarGoogle Scholar | 12193784PubMed |

Giglio, M. L., Ituarte, S., Pasquevich, M. Y., and Heras, H. (2016). The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins. Canadian Journal of Zoology 94, 777–785.
The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins.Crossref | GoogleScholarGoogle Scholar |

Grisolia, B. B. (2014). Efeitos indiretos das aranhas Peucetia spp. (Oxyopidae) e Misumenops argenteus (Thomisidae) no sucesso reprodutivo de Trichogoniopsis adenantha (DC) (Asteraceae) e no comportamento das guildas associadas à planta. M.Sc. Thesis, Universidade Estadual Paulista, Rio Claro Brazil.

Guimarães, C. T. (1981). Algumas observações de campo sobre biologia e ecologia de Pomacea haustrum (Reeve, 1856) (Mollusca, Pilidae). Memorias do Instituto Oswaldo Cruz 76, 343–351.
Algumas observações de campo sobre biologia e ecologia de Pomacea haustrum (Reeve, 1856) (Mollusca, Pilidae).Crossref | GoogleScholarGoogle Scholar |

Hayes, K. A., Cowie, R. H., Thiengo, S. C., and Strong, E. E. (2012). Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zoological Journal of the Linnean Society 166, 723–753.
Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda).Crossref | GoogleScholarGoogle Scholar |

Heard, T. A., and Klinken, R. D. V. (2004). Rapid preliminary characterisation of host specificity of leaf-beetles (Coleoptera: Chrysomelidae). Biocontrol Science and Technology 14, 499–511.
Rapid preliminary characterisation of host specificity of leaf-beetles (Coleoptera: Chrysomelidae).Crossref | GoogleScholarGoogle Scholar |

Heras, H., Dreon, M. S., Ituarte, S., and Pollero, R. J. (2007). Egg carotenoproteins in Neotropical Ampullariidae (Gastropoda: Arquitaenioglossa). Comparative Biochemistry and Physiology. Toxicology & Pharmacology 146, 158–167.
Egg carotenoproteins in Neotropical Ampullariidae (Gastropoda: Arquitaenioglossa).Crossref | GoogleScholarGoogle Scholar |

Hölldobler, B., and Wilson, E. O. (1990). ‘The Ants.’ (The Belknap Press of Harvard University Press: Cambridge, MA, USA.)

Horn, K. C., Johnson, S. D., Boles, K. M., Moore, A., Siemann, E., and Gabler, C. A. (2008). Factors affecting hatching success of golden apple snail eggs: effects of water immersion and cannibalism. Wetlands 28, 544–549.
Factors affecting hatching success of golden apple snail eggs: effects of water immersion and cannibalism.Crossref | GoogleScholarGoogle Scholar |

Horvitz, C. C., and Schemske, D. W. (1990). Spatiotemporal variation in insect mutualists of a neotropical herb. Ecology 71, 1085–1097.
Spatiotemporal variation in insect mutualists of a neotropical herb.Crossref | GoogleScholarGoogle Scholar |

Jolivet, P. H., and Verma, K. K. (2002). ‘Biology of Leaf Beetles.’ (Intercept Ltd: Andover, UK.)

Kushlan, J. A. (1978). Predation on apple snail eggs (Pomacea). The Nautilus 92, 57–58.

Lattke, J. E. (2003) Biogeografía de las hormigas neotropicales. In ‘Introducción a las Hormigas de la Region Neotropical’. (Ed. F. Fernández.) pp. 65–85. (Instituto de Investigación de Recursos Biológicos Alexander von Humboldt: Bogotá, Colombia.)

Lima, S. L. (1998). Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48, 25–34.
Nonlethal effects in the ecology of predator-prey interactions.Crossref | GoogleScholarGoogle Scholar |

Longino, J. T. (2003). The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica. Zootaxa 151, 1–150.
The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica.Crossref | GoogleScholarGoogle Scholar |

Lutinski, J. A., Lopes, B. C., and Morais, A. B. B. (2013). Diversidade de formigas urbanas (Hymenoptera: Formicidae) de dez cidades do Sul do Brasil. Biota Neotropica 13, 332–342.
Diversidade de formigas urbanas (Hymenoptera: Formicidae) de dez cidades do Sul do Brasil.Crossref | GoogleScholarGoogle Scholar |

Maestri, R., Leite, M. A. D. S., Schmitt, L. Z., and Restello, R. M. (2013). Efeito de mata nativa e bosque de eucalipto sobre a riqueza de artrópodos na serrapilheira. Perspectiva 37, 31–40.

Marinho, C. G., Zanetti, R. O. N. A. L. D., Delabie, J. H., Schlindwein, M. N., and Ramos, L. D. S. (2002). Ant (Hymenoptera: Formicidae) diversity in Eucalyptus (Myrtaceae) plantations and cerrado litter in Minas Gerais, Brazil. Neotropical Entomology 31, 187–195.
Ant (Hymenoptera: Formicidae) diversity in Eucalyptus (Myrtaceae) plantations and cerrado litter in Minas Gerais, Brazil.Crossref | GoogleScholarGoogle Scholar |

Medina, C., Lapointe, S., and Chacon, P. (1993). Fauna de hormigas associadas com forrages tropicales y su implicación com depredadoras de huevos y ninfas del salivazo de ospastos, Aeneolamia ssp. Revista Colombiana de Entomologia 19, 143–150.

Meier, R. E. (1994). Coexisting patterns and foraging behavior of introduced and native ants (Hymenoptera Formicidae) in the Galapagos Islands (Ecuador). In ‘Exotic Ants: Biology, Impact, and Control of Introduced Species’. (Ed. D. F. Williams.) pp. 45–66. (Westview Press: Boulder, CO, USA.)

Melo, I. B., Hattori, G. Y., and Sant’Anna, B. S. (2017). Reproduction and substrate selection for oviposition of the gastropod Pomacea dolioides (Reeve, 1856). In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori.) pp. 89–103. (NOVA Science Publishes: New York, NY, USA.)

Milward-de-Andrade, R., Carvalho, O. S., and Guimarães, C. T. (1978). Alguns dados bioecológicos de Pomacea haustrum (Reeve, 1856), predador-competidor de hospedeirosintermediários de Schistosoma mansoni Sambon, 1907. Revista de Saude Publica 12, 78–89.
Alguns dados bioecológicos de Pomacea haustrum (Reeve, 1856), predador-competidor de hospedeirosintermediários de Schistosoma mansoni Sambon, 1907.Crossref | GoogleScholarGoogle Scholar | 580972PubMed |

Naumann, K. (1994). An occurrence of two exotic ant (Formicidae) species in British Columbia. Journal of the Entomological Society of British Columbia 91, 69–70.

Ng, T. H., and Tan, S. K. (2011). Observations of land snails feeding on the eggs of Pomacea canaliculata (Lamarck, 1822) (Mollusca: Gastropoda). Nature in Singapore 4, 79–83.

Pacheco, R., Silva, R. R., Morini, M. S. C., and Brandão, C. R. F. (2009). A comparison of the leaf-litter ant fauna in a secondary Atlantic Forest with an adjacent pine plantation in southeastern Brazil. Neotropical Entomology 38, 55–65.
A comparison of the leaf-litter ant fauna in a secondary Atlantic Forest with an adjacent pine plantation in southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., and Oliveira, L. J. F. (2017). Histology and histochemistry of the testes in two Amazonian apple snails. In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori) pp. 127–144. (NOVA Science Publishes: New York, NY, USA.)

Pires-Júnior, A. N., Hattori, G. Y., and Sant’Anna, B. S. (2017). Effects of diet and feeding frequency on culture of juveniles of Apple Snail Pomacea dolioides. In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori.) pp. 67–88. (NOVA Science Publishes: New York, NY, USA.)

Pires-Júnior, A. N., Hattori, G. Y., and Sant’Anna, B. S. (2019). Effect of stock density of cultured Amazon Apple Snail Pomacea dolioides (Gastropoda: Ampullariidae) in Brazil. Brazilian Journal of Animal Science 48, e20180053.
Effect of stock density of cultured Amazon Apple Snail Pomacea dolioides (Gastropoda: Ampullariidae) in Brazil.Crossref | GoogleScholarGoogle Scholar |

Pitts, J. P., McHugh, J. V., and Ross, K. G. (2005). Cladistic analysis of the fire ants of the Solenopsis saevissima species-group (Hymenoptera: Formicidae). Zoologica Scripta 34, 493–505.
Cladistic analysis of the fire ants of the Solenopsis saevissima species-group (Hymenoptera: Formicidae).Crossref | GoogleScholarGoogle Scholar |

Rawlings, T. A., Hayes, K. A., Cowie, R. H., and Collins, T. M. (2007). The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology 7, 97.
The identity, distribution, and impacts of non-native apple snails in the continental United States.Crossref | GoogleScholarGoogle Scholar | 17594487PubMed |

Richard, F. J., Fabre, A., and Dejean, A. (2001). Predatory behavior in dominant arboreal ant species: the case of Crematogaster sp. (Hymenoptera: Formicidae). Journal of Insect Behavior 14, 271–282.
Predatory behavior in dominant arboreal ant species: the case of Crematogaster sp. (Hymenoptera: Formicidae).Crossref | GoogleScholarGoogle Scholar |

Santos-Neto, C. R. (2017). Record of egg predation of the gastropods of genus Pomacea. In ‘Amazonian Apple Snails’. (Eds B. S. Sant’Anna and G. Y. Hattori.) pp. 145–159. (NOVA Science Publishes: New York, NY, USA.)

Saveanu, L., and Martín, P. R. (2014). Egg cannibalism in Pomacea canaliculata (Caenogastropoda: Ampullariidae) from the southern Pampas: an alternative trophic strategy? Malacologia 57, 341–351.
Egg cannibalism in Pomacea canaliculata (Caenogastropoda: Ampullariidae) from the southern Pampas: an alternative trophic strategy?Crossref | GoogleScholarGoogle Scholar |

Schnorbach, H. J. (1995). The golden apple snail (Pomacea canaliculata Lamarck), an increasingly important pest in rice, and methods of control with Bayluscid. Pflanzenschutz-Nachrichten Bayer 48, 313–346.

Simone, L. R. L. (2006). ‘Land and Freshwater Mollusks of Brazil.’ (Editora Gráfica Bernardi, EGB; Fundação de Amparo a Pesquisa do Estado de São Paulo, FAPESP: São Paulo, Brazil.)

Smith, M. R. (1942). The relationship of ants and other organisms to certain scale insects on coffee in Puerto Rico. The Journal of Agriculture of the University of Puerto Rico 26, 21–27.

Snyder, N. F. R., and Snyder, H. A. (1971). Defenses of the Florida apple snail Pomacea paludosa. Behaviour 40, 175–214.
Defenses of the Florida apple snail Pomacea paludosa.Crossref | GoogleScholarGoogle Scholar |

Stevens, A. J., Stevens, N. M., Darby, P. C., and Percival, H. F. (1999). Observations of fire ants (Solenopsisinvicta Buren) attacking apple snails (Pomaceapaludosa Say) exposed during dry down conditions. The Journal of Molluscan Studies 65, 507–510.
Observations of fire ants (Solenopsisinvicta Buren) attacking apple snails (Pomaceapaludosa Say) exposed during dry down conditions.Crossref | GoogleScholarGoogle Scholar |

Tanaka, M. O., Souza, A. L., and Módena, É. S. (2006). Habitat structure effects on size selection of snail kites (Rostrhamus sociabilis) and limpkins (Aramus guarauna) when feeding on apple snails (Pomacea spp.). Acta Oecologica 30, 88–96.
Habitat structure effects on size selection of snail kites (Rostrhamus sociabilis) and limpkins (Aramus guarauna) when feeding on apple snails (Pomacea spp.).Crossref | GoogleScholarGoogle Scholar |

Yusa, Y. (2001). Predation on eggs of the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) by the fire ant Solenopsis geminata. The Journal of Molluscan Studies 67, 275–279.
Predation on eggs of the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) by the fire ant Solenopsis geminata.Crossref | GoogleScholarGoogle Scholar |

Zar, J. H. (1999). ‘Biostatistical Analysis.’ (Prentice-Hall: Upper Saddle River, NJ, USA.)