INTRODUCTION
⌅The family Pharidae currently includes 5 subfamilies and 14 genera. These are Pharinae H. and A. Adams, 1856 (9 species in 3 genera), Cultellinae Davies, 1935 (more than 25 species in 6 genera), Siliquinae Bronn, 1862 (15 species, 1 genus), Pharellinae Stoliczka, 1870 (7 species in 2 genera) and Novaculininae Ghosh, 1920 (5 species in 2 genera) (Cosel 2009Cosel R.v. 2009. The razor shells of the eastern Atlantic, part 2. Pharidae II: the genus Ensis Schumacher, 1817 (Bivalvia, Solenoidea). Basteria 73: 9-56., Coan and Valentich-Scott 2012Coan E.V., Valentich-Scott P. 2012. Bivalve seashells of tropical West America. Marine Bivalve Mollusks from Baja California to Perú. Santa Barbara Museum of Natural History monographs, Number 6, Studies in biodiversity, Number 4, 2 vols, Santa Barbara Museum of Natural History, Santa Barbara, 1258 pp., Cosel and Gofas 2019Cosel R.v., Gofas S. 2019. Marine bivalves of tropical west Africa: from Rio de Oro to southern Angola. Mus. Nat. Hist. nat., Paris, IRD, Marseille, 1104 pp. https://doi.org/10.5852/fft48 ). Usually, the members of this group of bivalves have medium-to-large shells that are cylindrical in cross section and quadrate to ovate in outline. Some species show laterally compressed shells with terminal (Ensis) to subterminal (Siliqua, Cultellus) umbos. The exterior surface of the shell is characterized by commarginal ribs or irregular growth striae. The ligament is external and opisthodetic, and the hinge shows one vertical cardinal and one horizontal cardinal in the right valve and two vertical cardinals and two horizontal cardinals in the left valve. No lateral teeth are present in this family. Finally, the anterior adductor muscle scar is clearly larger than the posterior one. The mantle cavity organs are characterized by a siphon with variable length, short to long, separate or fused at the base, and a large foot, laterally compressed and truncate.
Taxonomic studies related to the family Pharidae have been carried out in several regions (Bloomer 1906Bloomer H.H. 1906. On the anatomy of Ensis macha, Solen fonesii, and S. viridis. J. Moll. Stud. 7: 18-19. https://doi.org/10.1093/oxfordjournals.mollus.a066117 , Urk 1964Urk R.M.v. 1964. The genus Ensis in Europe. Basteria 28: 13-44., 1966Urk R.M.v. 1966. Interrelationship in European species of Ensis. Basteria 30: 11-14., 1971Urk R.M.v. 1971. Fossil Ensis species in the Netherlands. Basteria 35: 1-37., 1972Urk R.M.v. 1972. Notes on American fossil Ensis species. Basteria 36: 131-142., 1980Urk R.M.v. 1980. Probleme in der Systematik am Beispiel der Gattung Ensis (Mollusca, Bivalvia). Soosiana 8: 91-85., 1986Urk R.M.v. 1986. Eine systematisch-nomenklatorische Frage am Beispiel der Gattung Ensis Schumacher (Mollusca: Bivalvia). Soosiana. 14: 25-29., Cosel 2009Cosel R.v. 2009. The razor shells of the eastern Atlantic, part 2. Pharidae II: the genus Ensis Schumacher, 1817 (Bivalvia, Solenoidea). Basteria 73: 9-56.), and the latitudinal species richness was recently tested by Saeedi et al. (2017)Saeedi H., Dennis T.E., Costello M. 2017. Bimodal latitudinal species richness and high endemicity of razor clams (Mollusca). J. Biogeog. 44: 592-604. https://doi.org/10.1111/jbi.12903 . For the southern tip of South America, only Ensis macha (Molina, 1782Molina G.I. 1782. Saggio Sulla Storia Naturalia Del Chili. Bologna, Italy, 367 pp. https://doi.org/10.5962/bhl.title.62689 ) has been historically mentioned in the literature (Carcelles 1944Carcelles A. 1944. Catálogo de los moluscos marinos de Puerto Quequén. Rev. Mus. La Plata. 3 sección Zool: 233-309., Carcelles and Williamson 1951Carcelles A., Williamson S. 1951. Catálogo de los moluscos marinos de la provincia magallánica. Rev. Inst. Nac. Invest. Cient. Nat. 2 Cienc. Zool. (5): 225-383., Castellanos 1970Castellanos Z.J.A.D. 1970. Catálogo de los moluscos marinos bonaerenses. An. Com. Invest. Cient. Prov. Buenos Aires. 8: 9-365.). More recently, this species has been included in several lists of taxa and compendiums (Zelaya 2016Zelaya D.G. 2016. Marine bivalves from the Argentine coast and continental shelf: Species diversity and assessment of the historical knowledge. Am. Malacol. Bull. 33: 245-262. https://doi.org/10.4003/006.033.0204 , Valentich-Scott et al. 2020Valentich-Scott P., Coan E.V., Zelaya D.G. 2020. Bivalve Seashells of Western South America Marine Bivalve Mollusks from Punta Aguja, Perú to Isla Chiloé, Chile. Santa Barbara Museum of Natural History Monographs - 8. Studies in Biodiversity: Number 6, 593 pp., Giacomino and Signorelli 2021Giacomino S., Signorelli J.H. 2021. Systematic re-description of Solen (Ensisolen) tehuelchus and Ensis macha (Bivalvia: Solenoidea) from Argentina, southwestern Atlantic Ocean. Zootaxa 4964: 541-558. https://doi.org/10.11646/zootaxa.4964.3.6 ). The reported distribution range of Ensis macha goes from the San Matías Gulf (40°S) in the Atlantic Ocean to the northern coast of Peru (8°S) in the Pacific (Zaixso et al. 2015Zaixso H.E., Ré M.E., Morsán E. 2015. Moluscos costeros de interés económico, actual o potencial. In: Zaixso H.E., Boraso A.L. (eds) La zona costera patagónica argentina. Vol. 1. Editorial Universitaria de la Patagonia, pp. 119-299., Paredes et al. 2016Paredes C., Cardoso F., Santamaría J., et al. 2016. Lista anotada de los bivalvos marinos del Perú. Rev. Peruana Biol. 23(2): 127-150. https://doi.org/10.15381/rpb.v23i2.12397 , Márquez et al. 2017Márquez F., Trivellini M.M., Van der Molen S. 2017. Use of shell shape variation as an assessment tool in the southernmost razor clam fishery. Fish. Res. 186: 216-222. https://doi.org/10.1016/j.fishres.2016.08.027 ). However, a recent study based on genetic data (COI mitochondrial and 856 nuclear genes) revealed the presence of two clades along the Pacific coast of South America (Márquez et al. 2020). They were designated as northern and southern clades. The northern clade is mainly distributed in the Peruvian biogeographic province (a warm-temperate region), from Peru (8°S) to the Chilean coast at around 37°S, while the southern clade is distributed along the Magellan province (a cold-temperate region) from Chiloé (40°S) on the Pacific coast to northern Patagonia on the Atlantic coast (40°S) (Fig. 1, Table 1).
Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 analysed the variation in external shell shape (outlines) using an elliptic Fourier analysis. They found that the two clades showed an overlapping morphospace, although there was a slight separation trend. The genetic distances reported by Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 , plus new results based on landmark-based geometric morphometrics (GM), allowed the formal descriptions of a new species of Pharidae from the Pacific coast of South America. In order to maximize the separation between clades, 2D landmark-based GM was performed to analyse inner shell shape variation. Biogeographical implications related to the presence of two valid species of Ensis in the eastern Pacific coast of South America are discussed.
| Species | Locations | Lat/long | n |
|---|---|---|---|
| Ensis macha (Molina, 1782Molina G.I. 1782. Saggio Sulla Storia Naturalia Del Chili. Bologna, Italy, 367 pp. https://doi.org/10.5962/bhl.title.62689 ) | Puerto Lobos, Argentina | 42°00’S 65°04’W | 57 |
| Caleta Carolina, Argentina | 44°54’S 65°36’W | 56 | |
| El Porvenir, Chile | 53°17’S 70°21’W | 51 | |
| Ancud, Chile | 41°52’S 73°48’W | 46 | |
| Niebla, Chile | 39°52’S 73°23’W | 64 | |
| Ensis loboi n. sp. | Trujillo, Peru | 08°06’S 79°01’W | 2 |
| Dichato, Chile | 36°37’S 72°57’W | 49 | |
| Tubul, Chile | 37°13’S 73°26’W | 45 | |
| Total | 370 |
MATERIALS AND METHODS
⌅Sample collection
⌅The specimens were collected throughout the entire geographic distribution range of the South American razor clam, Ensis, from San Matías Gulf (41°34’S) in the Atlantic Ocean to Trujillo in the Pacific Ocean (08°06’S; Table 1). This study is compliant with the CBD and Nagoya protocols. All material was examined and compared with the specimens assigned to the new species. An updated distribution range for each valid species is illustrated (Fig. 1). The examined specimens were deposited in the Invertebrate Collection of IBIOMAR (CNP-Inv).
Geometric morphometrics
⌅A total of 370 specimens, 274 from the southern clade and 96 from the northern clade were photographed with the inner side upwards. Following Márquez et al. (2017)Márquez F., Trivellini M.M., Van der Molen S. 2017. Use of shell shape variation as an assessment tool in the southernmost razor clam fishery. Fish. Res. 186: 216-222. https://doi.org/10.1016/j.fishres.2016.08.027 , the inner shell shape variation was studied using landmark-based GM and multivariate statistics. Twelve landmarks (2D configuration) were captured to examine shape variation of the internal muscle scars and pallial lines (Fig. 2). Procrustes analysis (Rohlf and Slice 1990Rohlf F.J., Slice D. 1990 Extensions of the Procrustes method for the optimal superimposition of landmarks. System. Zool. 39: 40-59. https://doi.org/10.2307/2992207 ) was used to remove rotation, translation and scale effects of the raw landmark coordinates. Centroid size (CS) was calculated as the square root of the sum of the square distances from the landmarks to the CS which they defined (Zelditch et al. 2004Zelditch M.L., Swiderski D.L., Sheets H.D., Fink W.L. 2004. Geometric morphometrics for biologists: a primer. Elsevier Academic Press, New York, Elsevier: New York, 456 pp.) and was used as a proxy for shell size. Multivariate regression (pooled within-site) between shape variables and CS values was calculated to evaluate and correct the positive allometry. To capture the shape components that maximized the separation between species, a discriminant function was calculated. Finally, the differences in mean shell shape between species were analysed by a T2 Hotelling test with 1000 permutations, and a re-sampling procedure (leave-one-out-cross-validation) was performed to estimate the percentage of misclassification to each species (Johnson and Wichern 2007Johnson R.A., Wichern D.W. 2007. Applied multivariate statistical analysis. Prentice hall Upper Saddle River, 6th edition, NJ, New York, 773 pp.). All GM analyses were conducted in MorphoJ, version 1.07a (Klingenberg 2011Klingenberg C.P. 2011. Morphoj: an integrated software package for geometric morphometrics. Mol. Ecol. Res. 11:353-357. https://doi.org/10.1111/j.1755-0998.2010.02924.x ).
RESULTS
⌅Geometric morphometrics
⌅The independence between the Procrustes coordinates and the CS values was rejected (P<0.0001). Allometry explained 2.62% of the variation, so the residuals were used as the new allometric-free shell shape variables for subsequent analyses. Discriminant analysis showed that the shell shape range was different between the southern and northern clades. The mean inner shell shapes of the clades were significantly different (T2=761.07, p<0.0001, Mahalanobis distances= 3.27) (Fig. 3). The mean shell shape of the southern clade shows an anterior retraction and an expansion of the posterior part with a reduction of the anterior adductor muscle scar and the anterior and posterior retractor muscle scar of the foot in comparison with the mean shell shape of the northern clade (Fig. 3). The cross-validation function, based on the Mahalanobis distance of each individual from group means, indicated a low number of allocation errors in the species assignation (3.1% of northern individuals were placed in the southern group and 5.5% of the southern individuals were placed within the northern group; Table 2).
| Species | E. loboi n. sp. | E. macha | Total | Correct percentage |
|---|---|---|---|---|
| E. loboi n. sp. | 93 | 3 | 96 | 96.9 |
| E. macha | 15 | 259 | 274 | 94.5 |
Taxonomy
⌅After the molecular data published by Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 and the GM results presented in this study, two species of Ensis distributed along the Pacific coast of South America are now recognized. They are Ensis loboi n. sp., distributed from Tubul, Chile (37°S) to Trujillo, Peru (8°S); and the Magellan E. macha, with a distribution range from San Matías Gulf (41°S) in the Atlantic Ocean to Niebla (40°S) in the Pacific Ocean. All records of E. macha mentioned northward of Tubul, Chile, must be considered synonyms of E. loboi (Soot-Ryen 1959Soot-Ryen T. 1959. Reports of the Lund University Chile Expedition 1948-49. Pelecypoda. Lund Univ Arssk. 55: 1-86., Peña 1971Peña G.M.J. 1971. Zonas de distribución de los bivalvos marinos del Perú. An. Cient. Univ. Nac Agraria 9: 127-138., Basly-Santa Maria 1983Basly-Santa Maria J. 1983. Moluscos marinos del norte de Chile. Catálogo Ilustrativo. Impreso en Offset por W. Morales: Viña del Mar, Chile, 49 pp., Guzmán et al. 1998Guzmán N., Saá S., Ortlieb L. 1998. Catálogo descriptivo de los moluscos litorales (Gastrópoda y Pelecypoda) de la zona de Antofagasta, 23° S (Chile). Est Oceanol. 17: 17-86., Ramírez et al. 2003Ramírez R., Paredes C., Arenas J. 2003. Moluscos del Perú. Rev. Biol. Trop. 51: 225-284., Uribe et al. 2013Uribe Alzamora R., Rubio Rodríguez J., Carbajal Enzian P., Berrú Paz P. 2013. Invertebrados marinos bentónicos del litoral de la Región Áncash, Perú. Bol. Inst. Mar. Perú 28: 136-293., Paredes et al. 2016Paredes C., Cardoso F., Santamaría J., et al. 2016. Lista anotada de los bivalvos marinos del Perú. Rev. Peruana Biol. 23(2): 127-150. https://doi.org/10.15381/rpb.v23i2.12397 ).
Family Pharidae H. Adams and A. Adams, 1856
Genus Ensis Schumacher, 1817
[= Ensatella Swainson, 1840: 365. Type species Ensatella europaea Swainson, 1840 (=Ensis ensis (Linnaeus, 1758), OD); Hypogaea Poli, 1791 (in Poli, 1791-1795): 29 (in part), name given for soft parts of species included in Solenoidea, Tellinidae and Pholadidae ].
Type species: Ensis magnus Schumacher, 1817 by monotypy.
Distribution. Widely distributed along the Pacific coast of South America (Osorio and Reid 2002Osorio C., Reid D. 2002. Índice bibliográfico sobre biodiversidad acuática de Chile: Bivalvia (Mollusca). Rev. Cienc. Tecnol. Mar. 25: 167-175.), southwestern USA to western Central America (Coan and Valentich-Scott 2012Coan E.V., Valentich-Scott P. 2012. Bivalve seashells of tropical West America. Marine Bivalve Mollusks from Baja California to Perú. Santa Barbara Museum of Natural History monographs, Number 6, Studies in biodiversity, Number 4, 2 vols, Santa Barbara Museum of Natural History, Santa Barbara, 1258 pp., Valentich-Scott et al. 2020Valentich-Scott P., Coan E.V., Zelaya D.G. 2020. Bivalve Seashells of Western South America Marine Bivalve Mollusks from Punta Aguja, Perú to Isla Chiloé, Chile. Santa Barbara Museum of Natural History Monographs - 8. Studies in Biodiversity: Number 6, 593 pp.), western Atlantic coast of South America (Rios 2009Rios E.C. 2009. Compendium of Brazilian sea shells. Rio Grande, RS, 676 pp., Scarabino et al. 2016Scarabino F., Zelaya D.G., Orensanz J.M., et al. 2016. Cold, warm, temperate and brackish: Bivalve biodiversity in a complex oceanographic scenario (Uruguay, southwestern Atlantic). Am. Malacol. Bull. 33: 284-301. https://doi.org/10.4003/006.033.0219 , Giacomino and Signorelli 2021Giacomino S., Signorelli J.H. 2021. Systematic re-description of Solen (Ensisolen) tehuelchus and Ensis macha (Bivalvia: Solenoidea) from Argentina, southwestern Atlantic Ocean. Zootaxa 4964: 541-558. https://doi.org/10.11646/zootaxa.4964.3.6 ), east coast of North America (Mikkelsen and Bieler 2007Mikkelsen P.M., Bieler R. 2007. Seashells of Southern Florida - Living Marine Mollusks of the Florida Keys and Adjacent Regions: Bivalves. Princeton University Press, Princeton, New Jersey, 503 pp. https://doi.org/10.1515/9780691239453 ), Europe (Costello et al. 2001Costello M.J., Emblow C., White R.J. 2001. European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collection Patrimoines Naturels, 50. Mus. Nat. Hist. nat., Paris, 463 pp., Cosel 2009Cosel R.v. 2009. The razor shells of the eastern Atlantic, part 2. Pharidae II: the genus Ensis Schumacher, 1817 (Bivalvia, Solenoidea). Basteria 73: 9-56.) and tropical west Africa (Cosel 2009Cosel R.v. 2009. The razor shells of the eastern Atlantic, part 2. Pharidae II: the genus Ensis Schumacher, 1817 (Bivalvia, Solenoidea). Basteria 73: 9-56.).
Remarks. The genus Ensis includes 14 extant species (Cosel 2009Cosel R.v. 2009. The razor shells of the eastern Atlantic, part 2. Pharidae II: the genus Ensis Schumacher, 1817 (Bivalvia, Solenoidea). Basteria 73: 9-56., Coan and Valentich-Scott 2012Coan E.V., Valentich-Scott P. 2012. Bivalve seashells of tropical West America. Marine Bivalve Mollusks from Baja California to Perú. Santa Barbara Museum of Natural History monographs, Number 6, Studies in biodiversity, Number 4, 2 vols, Santa Barbara Museum of Natural History, Santa Barbara, 1258 pp., Valentich-Scott et al. 2020Valentich-Scott P., Coan E.V., Zelaya D.G. 2020. Bivalve Seashells of Western South America Marine Bivalve Mollusks from Punta Aguja, Perú to Isla Chiloé, Chile. Santa Barbara Museum of Natural History Monographs - 8. Studies in Biodiversity: Number 6, 593 pp.) widely distributed along both coasts of America, Europe and Western Africa. Ensis loboi n. sp. constitutes the fifteenth species of the genus.
Ensis loboi n. sp.
Ensis californicus of authors (not Dall, 1899Dall W.H. 1899. Synopsis of the Solenidae of North America and the Antilles. Proc. US Nat. Mus. 22: 107-112. https://doi.org/10.5479/si.00963801.22-1185.107 ) Alamo-Vázquez and Valdivieso-Milla, 1997: 141-142, 144, fig. 378Alamo-Vázquez V., Valdivieso-Milla V. 1997. Lista sistemática de moluscos marinos del Perú (segunda edición, revisada y actualizada). Instituto del Mar del Peru: Callao, Peru, 183 pp..
Ensis macha of authors (not Molina, 1782Molina G.I. 1782. Saggio Sulla Storia Naturalia Del Chili. Bologna, Italy, 367 pp. https://doi.org/10.5962/bhl.title.62689 ) Stempell, 1899: 239-240Stempell W. 1899. Die Muscheln der Sammlung Plate. Fauna Chilensis. Abhand Kennt Zool. Chiles Samm. von L. Plate 2: 217-250. (in part); Soot-Ryen, 1959: 67Soot-Ryen T. 1959. Reports of the Lund University Chile Expedition 1948-49. Pelecypoda. Lund Univ Arssk. 55: 1-86.; Peña, 1971: 137Peña G.M.J. 1971. Zonas de distribución de los bivalvos marinos del Perú. An. Cient. Univ. Nac Agraria 9: 127-138.; Basly-Santa Maria, 1983: 26, pl. 10, fig. 83Basly-Santa Maria J. 1983. Moluscos marinos del norte de Chile. Catálogo Ilustrativo. Impreso en Offset por W. Morales: Viña del Mar, Chile, 49 pp.; Guzmán et al. 1998: 70-71Guzmán N., Saá S., Ortlieb L. 1998. Catálogo descriptivo de los moluscos litorales (Gastrópoda y Pelecypoda) de la zona de Antofagasta, 23° S (Chile). Est Oceanol. 17: 17-86.; Ramírez et al. 2003: 268Ramírez R., Paredes C., Arenas J. 2003. Moluscos del Perú. Rev. Biol. Trop. 51: 225-284.; Uribe et al. 2013: 230Uribe Alzamora R., Rubio Rodríguez J., Carbajal Enzian P., Berrú Paz P. 2013. Invertebrados marinos bentónicos del litoral de la Región Áncash, Perú. Bol. Inst. Mar. Perú 28: 136-293.; Paredes et al. 2016: 149Paredes C., Cardoso F., Santamaría J., et al. 2016. Lista anotada de los bivalvos marinos del Perú. Rev. Peruana Biol. 23(2): 127-150. https://doi.org/10.15381/rpb.v23i2.12397 .
Type material: CNP-Inv 875, holotype. Paratypes: CNP-Inv 844, 1 specimen, CNP-Inv 872, 1 left valve, CNP-Inv 874, 1 specimen, Tubul, Talcahuano, Concepción, Chile (36.726202°S 73.132905°W).
Type locality. Tubul, Talcahuano, Concepción, Chile (36.726202°S 73.132905°W).
Etymology. This species is dedicated to José María “Lobo” Orensanz in recognition of his significant contribution to the field of fisheries and his invaluable advice to the authors of this manuscript over several years.
Description. Shell (Fig. 4A-R): large, thick, length up to 230 mm, cylindrical in cross section, elongate; dorsal and ventral margins almost straight, posterior end truncate; anterior end rounded; yellowish to dark brown periostracum, thin to moderately thick, partially eroded along the dorsal slope in larger specimens; exterior surface smooth with three sculptured zones, usually observed within Ensis; external ligament long and brown, over the dorsal edge, anteriorly placed behind the beaks; interior surface white to purple; hinge plate with two cardinal teeth in the right valve, one anterior and vertically oriented and one posterior and horizontally oriented; four cardinal teeth in the left valve, two vertically placed and two horizontally oriented, parallel to dorsal margin (Fig. 4), the horizontally oriented teeth are four times longer than the vertically oriented ones; ligament dark, opisthodetic (Fig. 4).
Additional material examined. Peru: CNP-Inv 3903, three specimens collected at Trujillo by José M. Lobo Orensanz. Chile: Bahía Coliumo, Dichato, Concepción (36.720555°S 73.150833°W), CNP-Inv 292, 19 valves, Tubul, Talcahuano, Concepción (36.726202°S 73.132905°W), Cnp-Inv-281, 26 specimens.
Distribution. From Trujillo, Peru (8°8’S 79°3’W) to Tubul, Chile (37°13’S 73°26’W).
Habitat. E. macha and E. loboi inhabit superficial sandy bottoms, from the shallow subtidal to about 30 m depth, forming fishing grounds or banks (Osorio and Bahamonde 1970Osorio C., Bahamonde N. 1970. Lista preliminar de Lamelibranquios de Chile. Bol. Mus. Nac. Hist. Nat. 31: 185-256., Márquez and Van der Molen 2011Márquez F., Van der Molen S. 2011. Intraspecific shell-shape variation in the razor clam Ensis macha along the Patagonian coast. J. Moll. Stud. 77: 1-6. https://doi.org/10.1093/mollus/eyq044 ). Razor clams can be found in a substrate characterized by a mixture of grain sizes, where fine and very fine sand with a low level of organic matter generally predominate (Aracena et al. 1998Aracena O., Carmona M.G., Medina L.E. 1998. FONDEF D96I1095. La navaja en la VIII Región. Documento Nº1, 14 pp., Jaramillo 1998Jaramillo E. 1998. Estudio biológico pesquero de los recursos almeja, navajuela y huepo en la VIII y X regiones. Informe Final Proyecto F.I.P. 96-46. Universidad Austral de Chile, 106 pp., Márquez and Van der Molen 2011Márquez F., Van der Molen S. 2011. Intraspecific shell-shape variation in the razor clam Ensis macha along the Patagonian coast. J. Moll. Stud. 77: 1-6. https://doi.org/10.1093/mollus/eyq044 ).
Remarks. None of the synonyms of E. macha mentioned by Giacomino and Signorelli (2021)Giacomino S., Signorelli J.H. 2021. Systematic re-description of Solen (Ensisolen) tehuelchus and Ensis macha (Bivalvia: Solenoidea) from Argentina, southwestern Atlantic Ocean. Zootaxa 4964: 541-558. https://doi.org/10.11646/zootaxa.4964.3.6 apply to the northern clade. Solen poirieri Mabille and Rochebrune, 1889 and Solen scalprum P. P. King, 1832 were described from the Magellan region. The registered type locality of Ensis luzonicus Dunker, 1862 (Luzon Island, Philippines) was erroneous. And the type of Solen gladiolus, described from “S. America”, has not been found in the NHMUK. The synonymy with E. macha is currently open awaiting further analysis (Giacomino and Signorelli 2021Giacomino S., Signorelli J.H. 2021. Systematic re-description of Solen (Ensisolen) tehuelchus and Ensis macha (Bivalvia: Solenoidea) from Argentina, southwestern Atlantic Ocean. Zootaxa 4964: 541-558. https://doi.org/10.11646/zootaxa.4964.3.6 ). For these reasons, a new name is proposed for the northern clade. The shell morphology of E. loboi n. sp. and E. macha (Fig. 5) is similar. Slight differences are illustrated in Figure 6 and listed in Table 3. Ensis loboi n. sp. was found to possess a stronger and thicker shell than E. macha. In addition, the GM revealed slight differences between the two species. The main shape differences were the distance between the posterior adductor muscle and the postero-ventral mantle projection (landmarks 5-6, Fig. 3); the distance between ventral and dorsal mantle projections (landmarks 1-5, Fig. 3); and the length of the anterior adductor muscle (landmarks 10-8, Fig. 3). Ensis californicus was reported from southern Peru (Alamo-Vázquez and Valdivieso-Milla 1997: 141-142, 144, fig. 378Alamo-Vázquez V., Valdivieso-Milla V. 1997. Lista sistemática de moluscos marinos del Perú (segunda edición, revisada y actualizada). Instituto del Mar del Peru: Callao, Peru, 183 pp.). However, the illustrated specimen clearly differs from the type material of Dall (USNM 158891), which has a well-defined concave dorsal margin. This was also noticed by Valentich-Scott et al. (2020)Valentich-Scott P., Coan E.V., Zelaya D.G. 2020. Bivalve Seashells of Western South America Marine Bivalve Mollusks from Punta Aguja, Perú to Isla Chiloé, Chile. Santa Barbara Museum of Natural History Monographs - 8. Studies in Biodiversity: Number 6, 593 pp.. In addition, the distribution of E. californicus is well documented from Sonora to Jalisco, Mexico (Coan and Valentich-Scott 2012Coan E.V., Valentich-Scott P. 2012. Bivalve seashells of tropical West America. Marine Bivalve Mollusks from Baja California to Perú. Santa Barbara Museum of Natural History monographs, Number 6, Studies in biodiversity, Number 4, 2 vols, Santa Barbara Museum of Natural History, Santa Barbara, 1258 pp.). After the analysis of new material from Trujillo, Peru, the specimens illustrated by Alamo-Vázquez and Valdivieso-Milla (1997)Alamo-Vázquez V., Valdivieso-Milla V. 1997. Lista sistemática de moluscos marinos del Perú (segunda edición, revisada y actualizada). Instituto del Mar del Peru: Callao, Peru, 183 pp. must be considered E. loboi n. sp.
| Ensis loboi n. sp. | Ensis macha | |
|---|---|---|
| Shell | Stronger and thicker | Thinner |
| Dorsal margin | Straight | Slightly concave |
| Distance between the posterior adductor muscle and the postero-ventral mantle projection (landmarks 5-6) | Shorter | Longer |
| Distance between ventral and dorsal mantle projections (landmarks 1-5) | More closed | More opened |
| Length of anterior adductor muscle (landmarks 10-8) | Longer | Shorter |
| External ligament | Longer | Slightly Shorter |
DISCUSSION
⌅Morphological studies and GM were used to distinguish Ensis loboi n. sp. (the northern clade) from E. macha (the southern clade). Specimens collected from Chiloé Island, Chile (42°35’S) were described by Molina (1782)Molina G.I. 1782. Saggio Sulla Storia Naturalia Del Chili. Bologna, Italy, 367 pp. https://doi.org/10.5962/bhl.title.62689 as Solen macha. Thus, the southern clade must retain the name E. macha and the northern clade must be considered as E. loboi n. sp. Additionally, slight shell shape components allowed both species of Ensis to be delineated with high resolution using GM based on 2D landmark configuration. These two clades were recently revealed by Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 on the basis of mitochondrial and nuclear loci. The genetic distance of COI sequence data between the two clades was similar to the magnitude of divergence between other recognized species of Ensis (Vierna et al. 2012Vierna J, Jensen K.T., González-Tizón A.M., Martinez-Lage A. 2012. Population genetic analysis of Ensis directus unveils high genetic variation in the introduced range and reveals a new species from the NW Atlantic. Mar. Biol. 159: 2209-2227. https://doi.org/10.1007/s00227-012-2006-6 , Vierna 2014Vierna J. 2014. Genetic analyses in various razor shell species of family Pharidae, with a focus on Atlantic Ensis. Universidad de La Coruña, La Coruña, 233 pp.) and was greater than the sequence divergence expected for more than 98% of 13320 species pairs across the animal kingdom (2%, Hebert et al. 2003Hebert P.D., Ratnasingham S., De Waard J.R. 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. Roy Soc. London. Ser. B: Biol. Sci. 270 (suppl 1): S96-S99. https://doi.org/10.1098/rsbl.2003.0025 ). In addition, the nuclear genetic divergences were similar to those found for different species by previous studies using multiple markers (e.g. Klimov et al. 2019Klimov P.B., Skoracki M., Bochkov A. 2019. Cox 1 barcoding versus multilocus species delimitation: validation of two mite species with contrasting effective population sizes. Par. Vect. 12: 8. https://doi.org/10.1186/s13071-018-3242-5 ). Morphological and GM analysis reached the same conclusion as that obtained from genetic data reported by Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 . Many authors have reported genetic differentiation for species distributed along the southeastern Pacific coast. In the case of E. macha and E. loboi n. sp., the biogeographic break was observed at 36-39°S (Márquez et al. 2020Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 ). This result coincides with those reported for other taxa (Fraser et al. 2009Fraser C.I., Hay C.H., Spencer H.G., Waters J.M. 2009. Genetic and morphological analyses of the southern bull kelp Durvillaea antarctica (Phaeophyceae: Durvillaeales) in New Zealand reveal cryptic species. J. Phycol. 45: 436-443. https://doi.org/10.1111/j.1529-8817.2009.00658.x , Montecinos et al. 2012Montecinos A., Broitman B.R., Faugeron S., et al. 2012. Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the south east pacific. BMC Evol. Biol. 12: 97.https://doi.org/10.1186/1471-2148-12-97 ; Trovant et al. 2015Trovant B., Orensanz J.M., Ruzzante D.E., et al. 2015. Scorched mussels (Bivalvia: Mytilidae: Brachidontinae) from the temperate coasts of South America: phylogenetic relationships, trans-Pacific connections and the footprints of Quaternary glaciations. Mol. Phylog. Evol. 82: 60-74. https://doi.org/10.1016/j.ympev.2014.10.002 ). The presence of genetic structure was found to characterize several taxa across central and northern Chile and Peru (Hewitt 1996Hewitt G. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247-276. https://doi.org/10.1006/bijl.1996.0035 ). The opposite pattern was observed in several species distributed along the Magellan province (de Aranzamendi et al. 2011de Aranzamendi M.C., Bastida R., Gardenal C.N. 2011. Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Mar. Biol. 158: 2405-2418. https://doi.org/10.1007/s00227-011-1742-3 , Ceballos et al. 2012Ceballos S.G., Lessa E.P., Victorio M.F., Fernández D.A. 2012. Phylogeography of the sub-Antarctic notothenioid fish Eleginops maclovinus: evidence of population expansion. Mar. Biol. 159: 99-505. https://doi.org/10.1007/s00227-011-1830-4 , Trovant et al. 2015Trovant B., Orensanz J.M., Ruzzante D.E., et al. 2015. Scorched mussels (Bivalvia: Mytilidae: Brachidontinae) from the temperate coasts of South America: phylogenetic relationships, trans-Pacific connections and the footprints of Quaternary glaciations. Mol. Phylog. Evol. 82: 60-74. https://doi.org/10.1016/j.ympev.2014.10.002 ). However, no signs of genetic structure were found in the northern clade (E. loboi n. sp.) by Márquez et al. (2020)Márquez F., Trovant B., Van der Molen S., et al. 2020. Two evolutionary units on the South American razor clam Ensis macha (Bivalvia: Pharidae): genetic and morphometric evidence. Org. Div. Evol. 20: 331-344. https://doi.org/10.1007/s13127-020-00441-4 . This result could be related to the fact that only two populations were sampled. Additional localities in northern Chile and Peru will help to highlight the evolutionary history of E. loboi n. sp. A potential scenario to explain the observed findings is that the differentiation between the northern and southern clades may have been initiated during the late Pleistocene. Glacial activity affects the Pacific Ocean south of 39°S, reaching the Atlantic Ocean in southernmost Patagonia and Tierra del Fuego (Clapperton 1993Clapperton C.M. 1993. Nature of environmental changes in South America at the Last Glacial Maximum. Palaeogeograph. Palaeoclim. Palaeoecol. 101: 189-208. https://doi.org/10.1016/0031-0182(93)90012-8 , Sugden et al. 2005Sugden D.E., Bentley M.J., Fogwill C.J., et al. 2005. Late‐glacial glacier events in southernmost South America: a blend of ‘northern’ and ‘southern’ hemispheric climatic signals? Geog. Ann: Ser. A, Phys. Geog. 87: 273-288. https://doi.org/10.1111/j.0435-3676.2005.00259.x ), and could have separated the populations of northern Central Chile and Peru from those of southern Argentina. The isolation of populations could have interrupted gene flow and over time, resulted in the concomitant genetic differentiation observed between these two populations.
Several studies have demonstrated overexploitation of populations of E. macha along the coasts of Peru and southeastern Chile (Espinoza et al. 2010Espinoza R., Tarazona J., Laudien J. 2010 Características de una población sobreexplotada de concha navaja, Ensis macha, en Bahía Independencia, Perú, durante el 2004. Rev. Peruana Biol. 17: 285-292. https://doi.org/10.15381/rpb.v17i3.3 , Hernández et al. 2011Hernández A.F., Cubillos L.A., Quiñones R.A.J. 2011. Evaluación talla estructurada de los stocks de Ensis macha y Tagelus dombeii en el Golfo de Arauco, Chile. Rev. Biol. Mar. Oceanog. 46: 157-176. https://doi.org/10.4067/S0718-19572011000200006 ). The management of a species depends on a solid, well-founded science-based taxonomy and systematics (Mace 2004Mace G.M. 2004. The role of taxonomy in species conservation. Phil. Trans. Roy. Soc. Lond. Series B: Biol. Sci. 359: 711-719. https://doi.org/10.1098/rstb.2003.1454 ). The South American Ensis fishery is managed as one species throughout its distribution. However, this study suggests cryptic diversity in Ensis macha. Overlooking a second Ensis species may have contributed to the overestimation of the population size, resulting in overfishing. The finding of a new species of Ensis is highly relevant for managing and conserving this important fishing resource in South America.