Pomacea reevei, Ampuero & Ramírez, 2023

Ampuero, André & Ramírez, Rina, 2023, Description of two new species of apple snail (Ampullariidae: Pomacea) from Peruvian Amazonia, Zootaxa 5258 (1), pp. 76-98 : 85-94

Pomacea reevei sp. nov.

Figs. 4C, 4D , 5B , 6B, 6D , 7B, 7C, 7E , 10D, 10E, 10F, 10G , 12 , 13 , 14 , 15 , 16E

Synonymy: Pomacea sp. 1 — Ramírez et al. 2022, fig 2E.

Types: PERU. Holotype male MUSM 5723H . Paratypes: MUSM 5723P , MZSP 122666 (ex MUSM 5723P ), SMF 348817 (ex MUSM 5723P ), LORETO, Maynas prov., Kichwa Cocha, near Napo River , Rango Isla populated center, 2°21'42.55''S 73°52'11.27''W, leg. R. Chujutalli & & S. Perez, 18/viii/2022, 7 specimens; MUSM 5716P , LORETO, Maynas prov., Pucayacu, near Napo River , 2°12'13.26''S 74°5'11.55''W, leg. R. Chujutalli, 29/xi/2018, 5 specimens; MUSM 5715 P, LORETO, Maynas prov., Puerto Alegre near Lagartococha , Napo River , 2°37'20''S 73°31'40.1''W, leg. R. Chujutalli, 17/viii/2017, 5 specimens; MUSM 5720P , LORETO, Alto Amazonas prov., Cocha Naranjillo near Huallaga River , Naranjal community, 5°13'27,56''S 70°54'32.1''W, leg. J. Sucumbio et al. 06/iii/2020, 5 specimens; MUSM 5724P , LORETO, Ucayali prov., Hermanos Lake, near Cruz Muyuna Lake , Ucayali River . 6°44'31.8''S 75°01'40.1''W, leg. R. Chujutalli, 05/iii/2022, 1 specimen; MUSM 5719P , LORETO, Alto Amazonas prov., Shirui Cocha near Huallaga River , Naranjal community, 5°13'29.58''S 75°40'21.58''W, leg. J. Sucumbio, et al. 27/v/2019, 1 specimen; MUSM 5627P , MADRE DE DIOS, Tambopata prov., Chacra Gamitana station, near Madre de Dios River , 12°30'05.7''S 68°58'34.2''W, A. Ampuero et al., 17/vi/2011, 4 specimens; MUSM 5718P , LORETO, Maynas prov., Bandeja Isla in Monte Verde oxbow, near Napo River , 2°8'2.78''S 74°13'16.91''W, leg. R. Chujutalli & G. Monchoa, 21/xii/2019, 4 specimens .

Etymology: The specific epithet of the type species is in honor of the English malacologist Lovell Augustus Reeve, who contributed with several illustrated works in malacology.

Additional material examined: PERU. MUSM 5634 , UCAYALI, Purus prov., Oxbow Lake near Cocha San Marcos , 9°53'47.9''S 70°51'69.5''W, 28/vii/2010, 4 shells; MUSM 5633 , UCAYALI, Purus prov., Alto Purús River: Esperanza Surveillance Post , Cocha San Marcos , 9°53'48''S 70°51'69.5''W, leg. F. Chang, 09/vii/1994, 1 shell; MUSM 5635 , UCAYALI, Purus prov., Cocha Livia , 9°56'58.2''S 70°54'32.1''W, 25/vii/2010, 8 shells; MUSM 5632 , UCAYALI, Purus prov., Miguel Grau, Cocha Grau near Curanja River , 09°57'S 70°59''W, leg. F. Chang, 08/ix/1994, 1 shell; MUSM 5629 , MADRE DE DIOS, Tambopata prov., Cocha Camp in Cuzco Amazonico-Biotrop (Inkaterra), Madre de Dios River , 12°35'S 69°05'W, R. Ramírez, 30/iv/1991, 3 shells ; MUSM 5722 , MADRE DE DIOS, Tambopata prov., ITA Inkaterra, Madre de Dios River , 12°32'04.9''S 69°02'50.8''W, leg. W. Ruiz, 23/xii/2017, 10 shells ; MUSM 5631 , MADRE DE DIOS, Tambopata prov., Miraya temporary lake, Palma Real River , ca. Palma Real Control Post , Palma Real Community , 12°30'59.1''S 68°48'44.3''W, leg. H. Ortega, 28/vii/1995, 2 shells ; MUSM 5628 , MADRE DE DIOS, Tambopata prov., Oxbow Lake near Valencia Lake , 12°28'11.9''S 68°47'32.8''W, A. Ampuero et al., 17/vi/2011, 1 shell.

Mitochondrial COI sequences are deposited into GenBank under the accession numbers MZ351319–MZ351332, as well as 16S rRNA MZ354652–MZ354656.

Type locality ( Fig. 2D ): PERU. LORETO, Maynas prov., Kichwa Cocha, near Napo River , Rango Isla populated center (2°21'42.55''S 73°52'11.27''W) .

Diagnosis: Grey penis sheath wide with bulged tip. Penis sheath gland in the apical region, occupying the entire bulged tip and with a small notch.

Shell ( Fig. 12 ): Shell large (81–137 mm), globose, thin, some specimens with thick shells, with 5.3 to 5.6 whorls. Periostracum yellowish to chestnut; Sculpture similar to previous species. Spire slightly elevated to depressed, with a deeply sutural channel. Aperture wide and ovate. Interior cream to white; specimens from Madre de Dios and Purus basins with notorious dark spiral bands. Outer lip light brown to white, and as in the previous character, southern specimens different due to the presence of dark spots in outer lip. Umbilicus narrow and deep. Measurements in mm. Holotype, height: 114.10, width: 93.28, aperture height: 90.22, aperture width: 60.18. N=181, (average±standard deviation, minimum–maximum) height: 102.7±21.6, 72.6–207.7; width: 85.8±19.5, 59.7–185.4; aperture height: 81.8±16.2, 60.1–164.2; aperture width: 54.4±12.9, 37.1–120.7.

Operculum ( Figs. 4C, 4D ): Features similar to P. penai with the following remarks. Operculum ovate semicircular, covering ~2/3 of aperture. Concentric grooves in outer surface, with mesomarginal nucleus. Smooth inner surface. Elliptical insertion mark occupying ~2/3 of internal area.

External anatomy ( Figs. 5B , 13B ): Characters similar to P. penai with the following differences. Dark grey to black foot. Sole grey. Long cephalic tentacles. Short and broad ommatophores with dark eyes. Snout broad and elongated, with lateral labial palps, with ~2/3 of length of cephalic tentacles. Elongated siphon. Glandular furrow, occupying ~2/3 of anterior pedal margin. Broad and short columellar muscle, covering ~1/5 of the body whorl.

Mantle cavity ( Figs. 6B , 13A, 13C ): Similar characters of mantle to those of P. penai sp. nov. with following characters. Cavity ( Figs. 6B , 13A ) occupying almost half of body whorl. Osphradium ( Fig. 13C ) in left side of cavity, posterior to border, comprised laterally, with curved posterior region. Base of osphradium, wide and slightly elevated at anterior region. Lung sac elongated and trapezoidal, occupying ~3/5 of mantle cavity, with thick muscular walls. Ctenidial vein between gill and lung sac, thickening near pericardium region. Ctenidial filaments slender and long with tip slightly curved to left.

Circulatory and excretory systems ( Figs. 6B , 13A, 13D ): Similar to those described for previous species, with following remarkable attributes. Pericardium cavity ( Fig. 13A ) wide. Auricle broad. Ventricle pyramidal. Posterior kidney ( Fig. 13D ) slightly concave and vascularized, broad, with anterior region slightly curved with blunt tip. Anterior kidney elongated and triangular.

Digestive system ( Figs. 6D , 7B, 7C, 7E , 13A, 13E, 13F ): Structures similar to those of P. penai sp. nov. Buccal bulb spherical and broad ( Figs 6D , 13E ). Radula (N=3) with same configuration as previous species with the following differences: with ~26–41 rows ( Figs 7B, 7C, 7E ). Rachidian tooth rectangular with slightly concave base and lateral margins; central cusp broad and rounded; lateral cusps rounded and of ~2/11 length of central peak. Lateral teeth, with triangular central cusp, and minuscule outer lateral cusps around it. Inner marginal teeth with two tiny triangular cusps, internal cusp of ~2/11 length of outer cusp. Pair of salivary glands compact ( Figs 6D , 13E ), lateral to digestive tract. Esophageal pouches adjacent to esophagus slender and short. Gastric muscle broad and long ( Fig. 13F ). Septum lingulate and elevated. Proximal region of major typhlosole with elongated fold. Minor typhlosole origin with developed fold at margin of stomach pouch. Sorting area of same proportion as P. penai sp. nov. Elongated and wide intestinal caeca.

Reproductive system: Female ( Figs. 6B , 13A ). Structures resembling previous species with the following differences. Ovary ivory, with several separated acini joining and forming the visceral oviduct. Seminal receptacle ( Fig. 13A ) elongated. Parenchymal tissue of albumen gland-capsule gland complex orange colored. Albumen gland lumen expanded. Vagina broad ( Figs. 6B , 13A ), with thick walls, adjacent to right side of mantle cavity, beneath a short urinary gutter. Female opening wide.

Male ( Fig. 14 ). Visceral structures similar to previous species. Testis cream, occupying approximately first 3 1/2 whorls. Slender spermiduct in the basal region of the testis, over pericardium region. Seminal vesicle globose and reniform ( Fig. 14C ). Prostate elongated with a strong curvature at the proximal region, running adjacent to rectum, and beneath urinary gutter in its distal portion. Prostate inserted below anal papilla. Penis pouch ( Figs. 14A, 14B ) massive, containing penis and penis bulb, this latter solid and occupying ~1/2 of penis pouch. Penis cylindrical and thick, abruptly decreasing diameter at distal portion. Penis sheath grey, wide, triangular, slightly curved to the right, and bulged tip. With two glands in right dorsal margin: one in distal region, occupying entire bulged tip and with a small notch; basal gland wrinkled, elongated and subtriangular to trapezoidal, near to sheath base and occupying ~1/3 or less of penis sheath. Basal outer gland embedded in the right region of the sheath, with a pore in the ventral surface.

Eggs ( Figs. 10D, 10E, 10F, 10G ): Clutch (N=3) with spherical eggs, slightly tight disposed; newly hatched white with a slime layer cover, turning with time to a cream color; number of eggs approximately of 300, average egg diameter near 6 mm.

Shell variability ( Fig. 15 ): Geometric morphometric analysis of the shells (N=142) showed most specimens from Madre de Dios basin had a lower spire and expanded aperture. First and second principal component explained 48.65% of the variation. Shape variation across the first principal component showed an expanded aperture relative to a depressed body whorl at the positive end of the axis; towards negative end of axis, shells have elevated body whorls. For the second principal component, shells displayed an elongated aperture and high spire at the end of the negative axis, and an expanded aperture and depressed spire at the positive end of the axis.

Procrustes ANOVA showed highly significant differences among localities (F: 7.2221, p<0.001). Pairwise comparisons also found significant differences among several localities. In particular, Madre de Dios specimens had highly significant differences compared to other localities, except Amazonas (Supplementary Table 1 provides the pairwise results). Other significant pairs were Amazonas / Huallaga , Amazonas / Napo and Napo / Huallaga (p<0.05). axes.

Distribution and habitat: Deep oxbow lakes near Napo, Huallaga, Ucayali, Madre de Dios and Purus Rivers. Fishers usually find them in their fish traps left overnight.

Remarks ( Fig. 16 ): Pomacea reevei sp. nov. matches with the illustration of Delessert (1841:pl. 31, figs. 3a, 3b) as Ampullaria canaliculata (Lamarck, 1822) . This author described the specimen ( Fig. 16A , coded MHNG-MOLL-33489) as a large-shelled individual claiming that it once belonged to Lamarck’s collection. Our concept of P. reevei sp. nov. includes Ampullaria gigas (non Spix in Wagner, 1827) as presented by Reeve (1856:pl. 1, fig. 3) in his Conchologia Iconica. Reeve described it in detail based on shell material (NHMUK 20110205), with type locality of Solomon’s River (possibly referring to Solimıes River, the upper section of Amazon River located in Brazil) ( Fig 16B ). Sowerby (1909) and Alderson (1925) disregarded Delessert specimen as A. canaliculata based on its size, and considered it was Ampullaria gigas (Spix in Wagner, 1827), synonymizing also with A. gigas ( Reeve, 1856) . Later, Pain (1960) proposed A. gigas of Spix and Reeve to be synonyms of P. maculata ( Cowie & Thiengo 2003) . This could be demonstrated by P. reevei sp. nov. specimens in Pain collection housed in Wales Museum (NMW.Z.1981.118.00486; NMW.Z.1981.118.00201) determined as P. maculata ( Figs. 16C, 16D ). We should add that previous authors such as Pain or Alderson described the shell of their P. gigas as thin, a trait present in our material, and did not mention Spix’s holotype, probably as much of his material was lost or destroyed ( Alderson 1925). Hayes et al. (2012) assigned a neotype for P. gigas , and rejected the possible type status of Delessert’s shell arguing that there are still doubts regarding the labelling process of this specimen. Based on observations of collected material for the present research, we propose that the material used by Delessert and Reeve could be P. reevei sp. nov. Likewise, we compared P. reevei sp. nov. with Pomacea maculata described by Hayes et al. (2012). Shells of P. reevei sp. nov. are frequently thin and fragile even in most larger specimens, compared to the thickness of P. maculata . Deeply narrow umbilicus and angled channeled suture are shared with Pomacea crosseana (Hidalgo, 1871) (syntypes examined, MNCN 15.05.1047 and 15.05.11485), where P. reevei had a more prominent and expanded body whorl.

Male reproductive system of P. reevei sp. nov. resembles Pomacea paludosa (Say, 1829) ( Hanning 1979) , but with following exceptions: apical penis sheath gland covers entire sheath tip including the notch, and basal internal gland does not cover most of penis sheath gland. It is noteworthy that in COI phylogeny, P. reevei and P. paludosa were closely related (genetic distance ranged from 13.6–14.3%), although with low support, within P. canaliculata clade; one species of this clade, P. maculata , had a distance of 12.1–12.8% to P. reevei ( Ramírez et al. 2022) . Pomacea reevei sp. nov. could be distinguished from P. maculata and P. canaliculata by possession of its apical penis sheath gland located in the bulged tip, as opposed to enlarged apical gland that occupies more than 1/3 of the penis sheath ( Sachwatkin 1920; Hayes et al. 2012); this character is shared also by Pomacea lineata (Spix, 1827) ( Thiengo 1987) . Penis pouch proportion in P. reevei sp. nov. is similar to Pomacea dolioides ( Reeve, 1856) and differs from this species by its smaller internal penis sheath glands, compared to the developed basal internal gland in P. dolioides ( Tillier 1980) . Kidney of P. reevei sp. nov. has characters similar to those of P. maculata , differing by its anterior broad set of lamellae in anterior kidney, as is present in P. canaliculata ( Hayes et al. 2012) . Ampulla vessels have the same pattern of P. canaliculata ( Hayes et al. 2012) . Regarding eggs, P. reevei shares spherical eggs shape and mucus matrix with P. paludosa ( Snyder & Snyder 1971; Rawlings et al. 2007). Spherical shape also appeared in species from this clade like P. canaliculata , P. maculata and P. lineata ( Thiengo 1987; Cowie et al. 2006; Hayes et al. 2012). Also, P. reevei sp. nov. eggs are characterized by their highest individual average diameter among all described Pomacea species.

Figures

FIGURE 2. Type localities of Pomacea penai sp. nov. and Pomacea reevei sp. nov. Flooding area of Nanay River, Nueva Bellavista—Nanay in Loreto department, during (A) wet and (B) dry season. (C) Map showing collection sites in Iquitos city, that includes type locality (asterisk), Bellavista Market (circle), Moronillo (triangle), and Isla Iquitos (square); collection sites included areas near and within populated areas, surrounded by flood zones and wetlands. (D) Kichwa Cocha, near Rango Isla populated center, Maynas province, Loreto department.

FIGURE 4. Outer and inner views of Pomacea spp. nov. opercula: Pomacea penai: (A) holotype MUSM 5692H and (B) paratype MUSM 5692P; Pomacea reevei: (C) holotype MUSM 5723H and (D) paratype MUSM 5723P. Scale bars = 10 mm.

FIGURE 5. Living specimens of (A) Pomacea penai MUSM 5713P and (B) Pomacea reevei MUSM 5723P.Scale bars = 20 mm.

FIGURE 6. Visceral mass showing pallial cavity roof, and foregut in lateral view of (A, C) Pomacea penai and (B, D) Pomacea reevei. Abbreviations: am, ampulla; ct, ctenidium; dg, digestive gland; ed, esophageal diverticulum; es, esophagus; in, intestine; ls, lung sac; mb, mantle border; os, osphradium; po, pallial oviduct; pk, posterior kidney; rct, rectum; rs, radular sac; sg, salivary gland; st, septum; ve, ventricle; v, vagina. Scale bars = 10 mm.

FIGURE 7. Radulae of (A) Pomacea penai MUSM 5692P, and Pomacea reevei (B) MUSM 5715P, (C) MUSM 5627P in SEM. Drawings of the radular row of P. penai (D) and P. reevei (E). Abbreviations: R: rachidian tooth; L, lateral tooth; M1, inner marginal tooth; M2, outer marginal tooth. Scale bars = 500 μm.

FIGURE 10. Oviposition and eggs in Pomacea spp. (A) Female Pomacea penai and (D) Pomacea reevei laying eggs; egg clutches of (B) P. penai and (E) P. reevei; habitats where egg clutches of (C) P. penai and (F, G) P. reevei were found. Scale bar = 20 mm.

FIGURE 12. Frontal and dorsal views of Pomacea reevei shells. (A) Holotype MUSM 5723H (h=114.10 mm); (B) paratype MUSM 5723P (h=131.16 mm); (C) MUSM 5716P (h=131.90 mm); (D) MUSM 5627P (h=116.26 mm); (E) MUSM 5720P (h=128.26 mm); (F) MUSM 5715P (h=122.46 mm).

FIGURE 13.Anatomy of female Pomacea reevei: (A) ventral view of female pallial cavity roof, pericardic cavity opened, pallial oviduct turned aside and schematic view showing internal structures; (B) frontal view of head–foot; (C) osphradium morphology detailed; (D) outline of kidney morphology; (E) lateral right view of foregut; (F) stomach dorsally opened. Abbreviations: agl, albumen gland; ak, anterior kidney; am, ampulla; an, anus; au, auricle; bc, copulatory bursa; ce, cephalic tentacle; cgl, capsule gland; ct, ctenidium; cv, ctenidial vein; dd, digestive gland ducts; ed, esophageal diverticulum; es, esophagus; ey, eye; fo, female opening; gv, wall of gastric ventral chamber; gm, gastric muscle; ic, intestinal caecum; ig, intestinal groove; in, intestine; la, labial palp; lnl, left nuchal lobe; mb, mantle border; ls, lung sac; mo, mouth; om, ommatophore; op, operculum; os, osphradium; pa, parenchymal tissue of albumen gland-capsule gland complex; pc, pericardic cavity; pgf, pedal glandular furrow; pk, posterior kidney; pn, pneumostome; rcs, seminal receptacle; rct, rectum; rnl, right nuchal lobe; rs, radular sac; sa, sorting area; sg, salivary gland; sn, snout; so, sole; sp, stomach pouch; st, septum; t1, major typhlosole; t2, minor typhlosole; t1f, major typhlosole fold; t2f, minor typhlosole fold; ve, ventricle; v, vagina. Scale bars = 5 mm.

FIGURE 14. Male reproductive system of Pomacea reevei: penis sheath deflected externally of (A) fresh MUSM 5720P and (B) fixed specimen MUSM 5723H, and (C) mantle deflected showing prostate and seminal vesicle (marked with dashed lines). Abbreviations: asg, apical sheath gland; bsg, basal sheath gland; ct, ctenidium; os, osphradium; pb, penis bulb; pe, penis; pp, penis pouch; prs, prostate; rct, rectum; ug, urinary gutter; vs, seminal vesicle. Scale bars = 10 mm.

FIGURE 15. Shell shape variation of Pomacea reevei across localities based on principal component analysis (PCA) of 19 landmarks. Most extreme individuals and shape deformation associated with components are illustrated near the respective axes. Amazonas specimens correspond to Pain collection from Wales Museum.

FIGURE 16. Museum shell specimens compared to Pomacea reevei sp. nov. (A) Ampullaria canaliculata of Delessert MHNG- MOLL-33489; (B) Ampullaria gigas NHMUK 20110205; (C) Pomacea maculata NMW.Z.1981.118.00486; (D) Pomacea maculata NMW.Z.1981.118.00201; (E) Pomacea reevei MUSM 5722M (h=137.02 mm). Scale bar = 50 mm.