Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Carrion consumption and its importance in a freshwater trophic generalist: the invasive apple snail Pomacea canaliculata

Lucía Saveanu A , Enzo Manara A and Pablo R. Martín A B
+ Author Affiliations
- Author Affiliations

A INBIOSUR (Universidad Nacional del Sur – Consejo Nacional de Investigaciones Científicas y Técnicas), Laboratorio de Ecología, Departamento de Biología, Bioquímica y Farmacia – Universidad Nacional del Sur, San Juan 670, 8000, Bahía Blanca, Argentina.

B Corresponding author. Email: pmartin@criba.edu.ar

Marine and Freshwater Research 68(4) 752-759 https://doi.org/10.1071/MF15304
Submitted: 8 August 2015  Accepted: 13 April 2016   Published: 1 July 2016

Abstract

Trophic flexibility is a relevant trait in the potential for organisms to establish widely, maintain high abundances and spread after invasion. Pomacea canaliculata is an apple snail that feeds primarily on aquatic macrophytes, although it also consumes other trophic resources that likely play an important role in its persistence and contribute to its effects in invaded wetlands. In the present study we determined the ingestion rates in P. canaliculata for carrion and subsequent effects on growth, and performed field and laboratory experiments to investigate the mechanism of carrion detection. We observed P. canaliculata snails of all sizes feeding on carrion. The specific ingestion rates of carrion decreased with snail size and were 20 times lower than when feeding on lettuce. The growth rates of snails feeding only on carrion were 15–30% higher than those of fasting snails and 30% of those snails feeding on lettuce or lettuce and carrion. We found no evidence of distant chemoreception of carrion. The importance of carrion for P. canaliculata is mostly as an alternative resource when its preferred food is absent, and not as a complementary resource that could enhance growth. Nevertheless, the ability of P. canaliculata to profit from carrion may help explain its potential to establish widely and to have effects on aquatic vegetation.

Additional keywords: Ampullariidae, gastropod, invasion, trophic ecology.


References

Aditya, G., and Raut, S. K. (2001). Food of the snail, Pomacea bridgesi, introduced in India. Current Science 80, 919–921.

Alonso, A. S., and Ageitos de Castellanos, Z. J. (1949). Algunos datos sobre alimentación de las ampularias. Notas del Museo de La Plata 14 – Zoologia 115, 31–34.

Andrews, E. B. (1965). The functional anatomy of the gut of the prosobranch gastropod Pomacea canaliculata and of some other pilids. Proceedings of the Zoological Society of London 145, 19–36.
The functional anatomy of the gut of the prosobranch gastropod Pomacea canaliculata and of some other pilids.Crossref | GoogleScholarGoogle Scholar |

Boland, B. B., Meerhoff, M., Fosalba, C., Mazzeo, N., Barnes, M. A., and Burks, R. L. (2007). Juvenile snails, adult appetites: contrasting resource consumption between two species of applesnails (Pomacea). The Journal of Molluscan Studies 74, 47–54.
Juvenile snails, adult appetites: contrasting resource consumption between two species of applesnails (Pomacea).Crossref | GoogleScholarGoogle Scholar |

Burela, S., and Martín, P. R. (2014). Nuptial gifts in Pomacea canaliculata (Ampullariidae, Caenogastropoda): experimental and field evidence about their function. Malacologia 57, 319–327.
Nuptial gifts in Pomacea canaliculata (Ampullariidae, Caenogastropoda): experimental and field evidence about their function.Crossref | GoogleScholarGoogle Scholar |

Carlsson, N. O. L., and Brönmark, C. (2006). Size-dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands. Freshwater Biology 51, 695–704.
Size-dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands.Crossref | GoogleScholarGoogle Scholar |

Carlsson, N. O. L., Brönmark, C., and Hansson, L. A. (2004). Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85, 1575–1580.
Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands.Crossref | GoogleScholarGoogle Scholar |

Cazzaniga, N. J., and Estebenet, A. L. (1984). Revisión y notas sobre los hábitos alimentarios de los Ampullariidae (Gastropoda). Histoire et Nature 4, 213–224.

Cowie, R. H. (2002). Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management. In ‘Molluscs as Crop Pests’. (Ed. G. M. Barker.) pp. 145–192. (CABI Publishing: Wallingford, UK.)

Daleo, P., Escapa, M., Isacch, J. P., Ribeiro, P., and Iribarne, O. (2005). Trophic facilitation by the oystercatcher Haematopus palliatus (Temminick) on the scavenger snail Buccinanops globulosum (Kiener) in a Patagonian bay. Journal of Experimental Marine Biology and Ecology 325, 27–34.
Trophic facilitation by the oystercatcher Haematopus palliatus (Temminick) on the scavenger snail Buccinanops globulosum (Kiener) in a Patagonian bay.Crossref | GoogleScholarGoogle Scholar |

Dillon, R. T. (2000). ‘The Ecology of Freshwater Mollusks.’ (Cambridge University Press: Cambridge.)

Dreon, M. S., Fernández, P. E., Gimeno, E. J., and Heras, H. (2014). Insights into embryo defenses of the invasive apple snail Pomacea canaliculata: egg mass ingestion affects rat intestine morphology and growth. PLoS Neglected Tropical Diseases 8, e2961.
Insights into embryo defenses of the invasive apple snail Pomacea canaliculata: egg mass ingestion affects rat intestine morphology and growth.Crossref | GoogleScholarGoogle Scholar | 24945629PubMed |

Estebenet, A. L. (1995). Food and feeding in Pomacea canaliculata (Gastropoda: Ampullariidae). The Veliger 38, 277–283.

Fenoglio, S., Merritt, R. W., and Cummins, K. W. (2014). Why do no specialized necrophagous species exist among aquatic insects? Freshwater Science 33, 711–715.
Why do no specialized necrophagous species exist among aquatic insects?Crossref | GoogleScholarGoogle Scholar |

Godoy, M. S., Castro-Vazquez, A., and Vega, I. A. (2013). Endosymbiotic and host proteases in the digestive tract of the invasive snail Pomacea canaliculata: diversity, origin and characterization. PLoS One 8, e66689.
Endosymbiotic and host proteases in the digestive tract of the invasive snail Pomacea canaliculata: diversity, origin and characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVOhsL7E&md5=36eb1306c8e58a8b99db28de74b688efCAS | 23818959PubMed |

Granval, N. I., and Gaviola, J. C. (1991). ‘Manual de producción de semillas hortícolas: Lechuga.’ (Instituto Nacional de Tecnología Agropecuaria.)

Hayden, B., Massa‐Gallucci, A., Harrod, C., O’Grady, M., Caffrey, J., and Kelly‐Quinn, M. (2014). Trophic flexibility by roach Rutilus rutilus in novel habitats facilitates rapid growth and invasion success. Journal of Fish Biology 84, 1099–1116.
Trophic flexibility by roach Rutilus rutilus in novel habitats facilitates rapid growth and invasion success.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2crjsl2htQ%3D%3D&md5=208ce40f9c38857ea50aa23b8ecfe47dCAS | 24628030PubMed |

Hayes, K. A., Joshi, R. C., Thiengo, S. C., and Cowie, R. H. (2008). Out of South America: multiple origins of non‐native apple snails in Asia. Diversity & Distributions 14, 701–712.
Out of South America: multiple origins of non‐native apple snails in Asia.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 |

Hayes, K. A., Burks, R. L., Castro-Vazquez, A., Darby, P. C., Heras, H., Martín, P. R., Qiu, J.-W., Thiengo, S. C., Vega, I. A., Wada, T., Yusa, Y., Burela, S., Cadierno, M. P., Cueto, J. A., Dellagnola, F. A., Dreon, M. S., Frassa, M. V., Giraud-Billoud, M., Godoy, M. S., Ituarte, S., Koch, E., Matsukura, K., Pasquevich, Y., Rodriguez, M. C., Saveanu, L., Seuffert, M. E., Strong, E. E., Sun, J., Tamburi, N. E., Tiecher, M. J., Turner, R. L., Valentine-Darby, P. L., and Cowie, R. H. (2015). Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae). Malacologia 58, 245–302.
Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae).Crossref | GoogleScholarGoogle Scholar |

Hill, J. M., Jones, R. W., Hill, M. P., and Weyl, O. L. (2015). Comparisons of isotopic niche widths of some invasive and indigenous fauna in a South African river. Freshwater Biology 60, 893–902.
Comparisons of isotopic niche widths of some invasive and indigenous fauna in a South African river.Crossref | GoogleScholarGoogle Scholar |

Himmelman, J. H. (1988). Movement of whelks (Buccinum undatum) towards a baited trap. Marine Biology 97, 521–531.
Movement of whelks (Buccinum undatum) towards a baited trap.Crossref | GoogleScholarGoogle Scholar |

Horgan, F. G., Stuart, A. M., and Kudavidanage, E. P. (2014). Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecologica 54, 90–100.
Impact of invasive apple snails on the functioning and services of natural and managed wetlands.Crossref | GoogleScholarGoogle Scholar |

Izquierdo Córser, P., Torres Ferrari, G., Barbosa De Martínez, Y., Márquez Salas, E., and Allara Cagnasso, M. (2000). Análisis proximal, perfil de ácidos grasos, aminoácidos esenciales y contenido de minerales en doce especies de pescado de importancia comercial en Venezuela. Archivos Latinoamericanos de Nutricion 50, 187–194.
| 11048593PubMed |

Karraker, N. E., and Dudgeon, D. (2014). Invasive apple snails (Pomacea canaliculata) are predators of amphibians in South China. Biological Invasions 16, 1785–1789.
Invasive apple snails (Pomacea canaliculata) are predators of amphibians in South China.Crossref | GoogleScholarGoogle Scholar |

Kwong, K. L., Chan, R. K. Y., and Qiu, J. W. (2009). The potential of the invasive snail Pomacea canaliculata as a predator of various life-stages of five species of freshwater snails. Malacologia 51, 343–356.
The potential of the invasive snail Pomacea canaliculata as a predator of various life-stages of five species of freshwater snails.Crossref | GoogleScholarGoogle Scholar |

Kwong, K. L., Dudgeon, D., Wong, P. K., and Qiu, J. W. (2010). Secondary production and diet of an invasive snail in freshwater wetlands: implications for resource utilization and competition. Biological Invasions 12, 1153–1164.
Secondary production and diet of an invasive snail in freshwater wetlands: implications for resource utilization and competition.Crossref | GoogleScholarGoogle Scholar |

Lv, S., Zhang, Y. I., Steinmann, P., Yang, G. J., Yang, K. U. N., Zhou, X. N., and Utzinger, J. (2011). The emergence of angiostrongyliasis in the People’s Republic of China: the interplay between invasive snails, climate change and transmission dynamics. Freshwater Biology 56, 717–734.
The emergence of angiostrongyliasis in the People’s Republic of China: the interplay between invasive snails, climate change and transmission dynamics.Crossref | GoogleScholarGoogle Scholar |

Lyabzina, S. N. (2013). Invertebrate necrobionts in the littoral zone in freshwater lakes of Karelia. Inland Water Biology 6, 131–138.
Invertebrate necrobionts in the littoral zone in freshwater lakes of Karelia.Crossref | GoogleScholarGoogle Scholar |

Martín, P. R., Estebenet, A. L., and Cazzaniga, N. J. (2001). Factors affecting the distribution of Pomacea canaliculata (Gastropoda: Ampullariidae) along its southernmost natural limit. Malacologia 43, 13–23.

Mendoza, R., Aguilera, C., Montemayor, J., and Rodríguez, G. (1999). Utilization of artificial diets and effect of protein/energy relationship on growth performance of the apple snail Pomacea bridgesi (Prosobranchia: Ampullariidae). The Veliger 42, 109–119.

Mendoza, R., Aguilera, C., Hernández, M., Montemayor, J., and Cruz, E. (2002). Elaboración de dietas artificiales para el cultivo del caracol manzana (Pomacea bridgesi). Revista AquaTIC 16, 1–12.

Nghiem, L. T. P., Soliman, T., Yeo, D. C. J., Tan, H. T. W., Evans, T. A., Mumford, J. D., Keller, R. P., Baker, R. H. A., Corlett, R. T., and Carrasco, L. R. (2013). Economic and environmental impacts of harmful non-indigenous species in Southeast Asia. PLoS One 8, e71255.
Economic and environmental impacts of harmful non-indigenous species in Southeast Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlams7jN&md5=186b38f85f4e501dbf785b94f6f046cfCAS |

Ocon, C., Lopez-Van Oosterom, M. V., Muñoz, M. I., and Rodrigues-Capítulo, A. (2013). Macroinvertebrate trophic responses to nutrient addition in a temperate stream in South America. Fundamental and Applied Limnology 182, 17–30.
Macroinvertebrate trophic responses to nutrient addition in a temperate stream in South America.Crossref | GoogleScholarGoogle Scholar |

Ramnarine, I. W. (2004). Quantitave protein requirements of the edible snail Pomacea urceus (Muller). Journal of the World Aquaculture Society 35, 253–256.
Quantitave protein requirements of the edible snail Pomacea urceus (Muller).Crossref | GoogleScholarGoogle Scholar |

Saveanu, L., and Martín, P. R. (2013). Pedal surface collecting as an alternative feeding mechanism of the invasive apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae). The Journal of Molluscan Studies 79, 11–18.
Pedal surface collecting as an alternative feeding mechanism of the invasive apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae).Crossref | GoogleScholarGoogle Scholar |

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

Saveanu, L., and Martín, P. R. (2015). Neuston: a relevant trophic resource for apple snails? Limnologica 52, 75–82.
Neuston: a relevant trophic resource for apple snails?Crossref | GoogleScholarGoogle Scholar |

Seuffert, M. E., and Martín, P. R. (2010). Dependence on aerial respiration and its influence on microdistribution in the invasive freshwater snail Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biological Invasions 12, 1695–1708.
Dependence on aerial respiration and its influence on microdistribution in the invasive freshwater snail Pomacea canaliculata (Caenogastropoda, Ampullariidae).Crossref | GoogleScholarGoogle Scholar |

Seuffert, M. E., and Martín, P. R. (2012). A lentic dweller in lotic habitats: the behavior of the invasive South American apple snail Pomacea canaliculata in flowing water. Aquatic Ecology 46, 129–142.
A lentic dweller in lotic habitats: the behavior of the invasive South American apple snail Pomacea canaliculata in flowing water.Crossref | GoogleScholarGoogle Scholar |

Seuffert, M. E., Burela, S., and Martín, P. R. (2010). Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) at its southernmost limit (Southern Pampas, Argentina). Journal of Thermal Biology 35, 77–84.
Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) at its southernmost limit (Southern Pampas, Argentina).Crossref | GoogleScholarGoogle Scholar |

Takeichi, M., Hirai, Y., and Yusa, Y. (2007). A water-borne sex pheromone and trail following in the apple snail, Pomacea canaliculata. The Journal of Molluscan Studies 73, 275–278.
A water-borne sex pheromone and trail following in the apple snail, Pomacea canaliculata.Crossref | GoogleScholarGoogle Scholar |

Tamburi, N. E., and Martín, P. R. (2009). Feeding rates and food conversion efficiencies of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae). Malacologia 51, 221–232.
Feeding rates and food conversion efficiencies of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae).Crossref | GoogleScholarGoogle Scholar |

Tamburi, N. E., and Martín, P. R. (2016). Effects of absolute fasting on reproduction and survival of the invasive apple snail Pomacea canaliculata. Current Zoology 62, 1–7.

Weis, J. S. (2010). The role of behavior in the success of invasive crustaceans. Marine and Freshwater Behaviour and Physiology 43, 83–98.
The role of behavior in the success of invasive crustaceans.Crossref | GoogleScholarGoogle Scholar |

Wood, T. S., Anurakpongsatorn, P., Chaichana, R., Mahujchariyawong, J., and Satapanajaru, T. (2006). Heavy predation on freshwater bryozoans by the golden apple snail, Pomacea canaliculata Lamarck, 1822 (Ampullariidae). The Natural History Journal of Chulalongkorn University 6, 31–36.

Zischke, J. A., Watabe, N., and Wilbur, K. M. (1970). Studies on shell formation: measurement of growth in the gastropod Ampullarius glaucus. Malacologia 10, 423–439.