Abstract
Two new species of apple snails are described, Pomacea penai sp. nov. and Pomacea reevei sp. nov. that are used as food resources in Peruvian Amazonia. We used anatomical and conchological features to diagnose these two species. Pomacea penai sp. nov. is characterized by a highly variable shell morphology, spire that is prominent to immersed, apical penis sheath gland covering 1/3 penis sheath and elongated basal gland, prostate broad proximally, reduced stomach septum, green eggs, and commonly inhabits temporary flooded areas, creeks, and oxbow lakes. Pomacea reevei sp. nov. possesses a large shell, ranging from 81–137 mm, grey broad penis sheath, small apical penis sheath gland and the basal gland covering 1/3 penis sheath, tall stomach septum, white eggs, and found in deep lentic water bodies.
References
Adams, D., Collyer, M. & Kaliontzopoulou, A. (2020) Geomorph: Software for geometric morphometric analyses. R package version 3.2.1. [program]
Alderson, E.G. (1925) Studies in Ampullaria. W. Heffer & Sons, Cambridge, xx, 102 pp. 19 pls.
Alyakrinskaya, I.O. (2004) Tissue hemoglobins of Gastropoda (Mollusca). Biology Bulletin of the Russian Academy of Sciences, 31 (5), 519–531.https://doi.org/10.1023/B:BIBU.0000043780.06599.c9
Ampuero, A. & Ramírez , R. (2017) Anatomy of a commercial apple snail from the Peruvian Amazon. In: Sant’Anna, B.S. & Hattori, G.Y. (Eds.), Amazonian Apple Snails. Nova Publishers, New York, pp. 21–38.
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 (1), 19–36.https://doi.org/10.1111/j.1469-7998.1965.tb01998.x
Berthold, T. (1991) Vergleichende Anatomie, Phylogenie und Historische Biogeographie der Ampullariidae (Mollusca, Gastropoda). Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg, 29, 1–256.
Burch, J.B. (1989) North American Freshwater Snails. Malacological Publications, Hamburg, 365 pp.
Cazzaniga, N.J. (2002) Old species and new concepts in the taxonomy of Pomacea (Gastropoda: Ampullariidae). Biocell, 26 (1), 71–81.
Cheesman, D.F. (1958) Ovorubin, a chromoprotein from the eggs of the gastropod mollusc Pomacea canaliculata. Proceedings of the Royal Society B: Biological Sciences, 149 (937), 571–87.https://doi.org/10.1098/rspb.1958.0093
Covich, A.P. (2010) Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance. Hydrobiologia, 653 (1), 191–215.https://doi.org/10.1007/s10750-010-0354-0
Cowie, R.H. (2002) Apple Snails (Ampullariidae) as Agricultural Pests: their Biology, Impacts and Management. In: Barker, G.M. (Ed.) Molluscs as crop pests. CABI, Wallingford, pp. 145–192.https://doi.org/10.1079/9780851993201.0145
Cowie, R.H. & Hayes, K.A. (2019) Ampullariidae. In: Lydeard, C. & Cummings, K.S. (Eds.), Freshwater Mollusks of the World: A Distribution Atlas. John Hopkins University Press, Baltimore, Maryland, pp. 37–42.
Cowie, R.H., Hayes, K.A., Strong, E.E. & Thiengo, S.C. (2017) Non-native apple snails: systematics, distribution, invasion history and reasons for introduction. In: Joshi, R.C., Cowie, R.H. & Sebastian, L.S. (Eds.), Biology and management of invasive apple snails. Philippine Rice Research Institute, Maligaya, pp. 3–32.
Cowie, R.H., Hayes, K.A. & Thiengo, S.C. (2006) What are apple snails? Confused taxonomy and some preliminary resolution. In: Joshi, R.C. & Sebastian, L.S. (Eds.), Global advances in ecology and management of golden apple snails. Philippine Rice Research Institute, Nueva Ecija, pp. 3–23.
Cowie, R.H. & 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 (1), 41–100.
Delessert, M.B. (1841) Recueil de coquilles décrites par Lamarck dans son histoire naturelle des animaux sans vertèbres et non encore figurées. Chez Fortin, Masson et Cie, Paris, 40 pls.
Emery, K.F. (2007) Aprovechamiento de la fauna en Piedras Negras: dieta, ritual y artesanía del periodo Clásico maya. Mayab, 19, 51–69.
Estebenet, A.L. & Martin, P.R. (2003) Shell interpopulation variation and its origin in Pomacea canaliculata (Gastropoda: Ampullariidae) from Southern Pampas, Argentina. Journal of Molluscan Studies, 69 (4), 301–310.https://doi.org/10.1093/mollus/69.4.301
García-Sánchez, J. & Bernex de Falen, N. (1994) El río que se aleja: cambio del curso del Amazonas, estudio histórico-técnico. CETA-IIAP, Iquitos, Perú, 51 pp.
Ghiretti, F. & Ghiretti-Magaldi, A. (1972) Chapter 7 - Respiratory Proteins in Mollusks. In: Florkin, M. & Scheer, B.T. (Eds.), Chemical Zoology. Vol. 7 Mollusca. Academic Press, New York, pp. 201–217.https://doi.org/10.1016/B978-0-12-395535-7.50011-5
Guo, J., Zhang, C., Zhang, J. & Zhao, B. (2019) Sex differences in the morphological defenses of an invasive snail: dimorphism and predator-induced plasticity. Freshwater Science, 38 (3), 582–590.https://doi.org/10.1086/704997
Gustafson, K., Kensinger, B., Bolek, M. & Luttbeg, B. (2014) Distinct snail (Physa) morphotypes from different habitats converge in shell shape and size under common garden conditions. Evolutionary Ecology Research, 16 (1), 77–89.
Haas, F. (1947) Malacological Notes—V. Fieldiana Zoology, 31 (22), 171–188.https://doi.org/10.5962/bhl.title.3005
Hanning, G. (1979) Aspects of reproduction in Pomacea paludosa (Mesogastropoda: Pilidae). Department of Biological Science. Florida State University, Tallahassee, Florida, x + 138 pp.
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, M.Y., Rodriguez, C., Saveanu, L., Seuffert, M.E., Strong, E.E., Sun, J., Tamburi, N.E., Tiecher, M.J., Turner, R.L., Valentine-Darby, P.L. & Cowie, R.H. (2015) Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae). Malacologia, 58 (1–2), 245–302.https://doi.org/10.4002/040.058.0209
Hayes, K.A., Cowie, R.H. & Thiengo, S.C. (2009) A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biological Journal of the Linnean Society, 98 (1), 61–76.https://doi.org/10.1111/j.1095-8312.2009.01246.x
Hayes, K.A., Cowie, R.H., Thiengo, S.C. & 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 (4), 723–753.https://doi.org/10.1111/j.1096-3642.2012.00867.x
Heras, H., Dreon, M.S., Ituarte, S. & Pollero, R.J. (2007) Egg carotenoproteins in neotropical Ampullariidae (Gastropoda: Arquitaenioglossa). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146 (1–2), 158–67.https://doi.org/10.1016/j.cbpc.2006.10.013
Hylton-Scott, M.I. (1957) Estudio morfológico y taxonómico de los Ampuláridos de la República Argentina. Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ e Instituto Nacional de Investigacion de las Ciencias Naturales. Ciencias Zoologicas, 3 (5), 231–333.
Ituarte, S., Dreon, M.S., Ceolín, M. & Heras, H. (2008) Isolation and characterization of a novel perivitellin from the eggs of Pomacea scalaris (Mollusca, Ampullariidae). Molecular Reproduction and Development, 75 (9), 1441–1448. https://doi.org/10.1002/mrd.20880
Lopes, H.S. (1955) Sobre duas especies do gênero Pomacea (Perry, 1810) com um estudo da genitália em ambos os sexos (Mesogastropoda, Architaenioglossa, Mollusca). Revista Brasileira de Biologia, 15 (2), 203–210.
Pain, T. (1960) Pomacea (Ampullariidae) of the Amazon river system. Journal of Conchology, 24, 421–432.
Pasquevich, M.Y., Dreon, M.S. & Heras, H. (2014) The major egg reserve protein from the invasive apple snail Pomacea maculata is a complex carotenoprotein related to those of Pomacea canaliculata and Pomacea scalaris. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 169, 63–71.https://doi.org/10.1016/j.cbpb.2013.11.008
Puhakka, M., Kalliola, R., Rajasilta, M. & Salo, J. (1992) River types, site evolution and successional vegetation patterns in Peruvian Amazonia. Journal of Biogeography, 19 (6), 651–665.https://doi.org/10.2307/2845707
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. [program]
Rama Rao, S., Liew, T.-S., Yow, Y.-Y. & Ratnayeke, S. (2018) Cryptic diversity: Two morphologically similar species of invasive apple snail in Peninsular Malaysia. PLoS One, 13 (5), e0196582.https://doi.org/10.1371/journal.pone.0196582
Ramírez, R., Paredes, C. & Arenas, J. (2003) Moluscos del Perú. Revista de Biología Tropical, 51 (Supplement 3), 225–284.
Ramírez, R., Ramírez , J.L., Rivera, F., Justino, S., Solís, M., Morín, J., Ampuero, A., Mendivil, A. & Congrains, C. (2022) Do not judge a snail by its shell: molecular identification of Pomacea species (Gastropoda: Ampullariidae), with particular reference to the Peruvian Amazonian giant apple snail, erroneously synonymized with Pomacea maculata. Archiv für Molluskenkunde, 151 (1), 1–11.https://doi.org/10.1127/arch.moll/151/007-017
Ramírez, R., Solis, M., Ampuero, A., Morín, J., Jiménez-Vásquez, V., Ramírez, J.L., Congrains, C., Temoche, H. & Shiga, B. (2020) Identificación molecular y relaciones evolutivas de Pomacea nobilis, base para la autenticación específica del churo negro de la Amazonia peruana. Revista Peruana de Biología, 27, 139–148.https://doi.org/10.15381/rpb.v27i2.17875
Rawlings, T.A., Hayes, K.A., Cowie, R.H. & Collins, T.M. (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology, 7, 97.https://doi.org/10.1186/1471-2148-7-97
Read, K.R.H. (1966) 6. Molluscan Hemoglobin and Myoglobin. In: Wilbur, K.M. & Yonge, C.M. (Eds.), Physiology of Mollusca. Vol. II. Academic Press, New York, New York, pp. 209–232.https://doi.org/10.1016/B978-1-4832-3242-3.50012-4
Reeve, L.A. (1856) Monograph of the genus Ampullaria. In: Conchologia Iconica: or, illustrations of the shells of molluscous animals. Vol. X. Lovell Reeve & Co., London, pls. 1–28.https://doi.org/10.5962/bhl.title.8129
Rohlf, F.J. (2019) tpsDig, version 2.16. Stony Brook University, Stony Brook, NY.
Sachwatkin, V. (1920) Das urogonital-system von Ampullaria gigas Spix. Acta Zoologica, 1920, 67–130.https://doi.org/10.5962/bhl.title.47046
Sánchez, F., Agapito, W., De la Cruz, W., Julio, S., Monge, M., Robert, W., Chira Fernández, J., Herrera, I., Valencia, M. & Romero, D. (1999) Geología de los cuadrángulos de Puerto Arturo, Flor de Agosto, San Antonio del Estrecho, Nuevo Perú, San Felipe, Río Algodón, Quebrada Airambo, Mazán, Francisco de Orellana, Huanta, Iquitos, Río Maniti, Yanashi, Tamshiyacu, río Tamshiyacu, Buenjardín, Ramón Castilla, Río Yavarí-Mirín y Buenavista. Boletín Instituto Geológico, Minero y Metalúrgico (INGEMMET), Carta Geológica Nacional, Sector Energía y Minas, Serie A, 132 1–372.
Simone, L. (2004) Comparative morphology and phylogeny of representatives of the superfamilies of Architaenioglossans and the Annulariidae (Mollusca, Caenogastropoda). Arquivos do Museu Nacional, Rio de Janeiro, 62, 387–504.
Snyder, N.F.R. & Snyder, H.A. (1971) Defenses of the Florida apple snail Pomacea paludosa. Behaviour, 40 (3/4), 175–215.https://doi.org/10.1163/156853971X00384
Sowerby, G.B. (1909) Notes on the family Ampullariidae, with list of species, varieties, and synonyms, also descriptions of four new species. Proceedings of the Malacological Society of London, 8, 345–362.https://doi.org/10.1093/oxfordjournals.mollus.a066281
Strong, E., Gargominy, O., Ponder, W. & Bouchet, P. (2008) Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia, 595 (1), 149–166.https://doi.org/10.1007/s10750-007-9012-6
Sturm, C.F., Mayhew, R. & Bales, B.R. (2006) Field and laboratory methods in malacology. In: Sturm, C.F., Pearce, T.A. & Valdes, A. (Eds.), The mollusks: a guide to their study, collection, and preservation. American Malacological Society, Pittsburgh, pp. 9–31.
Tamburi, N.E., Seuffert, M.E. & Martín, P.R. (2018) Temperature-induced plasticity in morphology and relative shell weight in the invasive apple snail Pomacea canaliculata. Journal of Thermal Biology, 74, 331–336.https://doi.org/10.1016/j.jtherbio.2018.04.008
Thiengo, S.C. (1987) Observations on the morphology of Pomacea lineata (Spix, 1827)(Mollusca, Ampullariidae). Memorias do Instituto Oswaldo Cruz, 82, 563–570.https://doi.org/10.1590/S0074-02761987000400015
Tillier, S. (1980) Gastéropodes terrestres et fluviatiles de Guyane Française. Mémoires du Muséum National d’Histoire Naturelle, Nouvelle Série, Série A, Zoologie, 118, 1–189.
Trussell, G.C., Johnson, A.S., Rudolph, S.G. & Gilfillan, E.S. (1993) Resistance to dislodgement: habitat and size-specific differences in morphology and tenacity in an intertidal snail. Marine Ecology Progress Series, 100 (1/2), 135–144.https://doi.org/10.3354/meps100135
van Aardt, W.J. & de Kock, K.N. (1991) Oxygen consumption and haemocyanin function in the freshwater snail Marisa cornuarietis (L.). Comparative Biochemistry and Physiology Part A: Physiology, 100 (2), 413–418.https://doi.org/10.1016/0300-9629(91)90492-U
Villela, G.G. (1956) Carotenoids of some Brazilian freshwater gastropods of the genus Pomacea. Nature, 178 (4524), 93.https://doi.org/10.1038/178093a0
Wagner, J.A. (1827) Testacea fluviatilia quae in itinere per Brasilianum annis MDCCCXVII–MDC-CCXX jussu et auspicilis Maximiliani Josephi I. Bavariae regis augustissimi suscepto collegit et pingenda curavit Dr. J. B. de Spix, quondam ordinis regii coronae Bavaricae civilis eques, academiae scientarum Bavaricae socius ordinarius, musei regii zoologici, zootomici et ethno-graphici conservator rel. Herausgeber Dr. F. A Paul von Schrank und Dr. C. F. P. von Martius, C. Wolf, Monachii [Munich], iv + [ii] + 36 pp., 29 pls.
Wright, L.E. (2005) Identifying immigrants to Tikal, Guatemala: Defining local variability in strontium isotope ratios of human tooth enamel. Journal of Archaeological Science, 32 (4), 555–566.https://doi.org/10.1016/j.jas.2004.11.011