Astyanax armandoi, a Junior Synonym of Astyanax aeneus - BioOne

Copeia 2008, No. 2, 409–413

Astyanax armandoi, a Junior Synonym of Astyanax aeneus (Teleostei: Characidae) J. J. Schmitter-Soto1, M. E. Valdez-Moreno1, R. Rodiles-Hernańdez2, and A. A. Gonza´lez-Dıáz2 Astyanax armandoi Lozano-Vilano and Contreras-Balderas, 1990, a characid described as endemic to a small stream in southern Mexico, is hereby synonymized with A. aeneus (Gu ¨ nther, 1860), a species widespread in northern Central America. Astyanax armandoi was diagnosed by its expanded lower lip, in combination with a suite of osteological characters. The labial expansion has been shown in other Astyanax populations (in Campeche and Chiapas, Mexico) to be an ecophenotype, an adaptation to hypoxia. The osteological, meristic, and morphometric characters of A. armandoi are compatible with the remarkable intra- and interpopulational variation of A. aeneus. The type locality has been repeatedly visited in the last decade; no further specimens identifiable as A. armandoi have been found, only typical A. aeneus. This conclusion implies that A. armandoi should be taken off the Mexican list of endangered species (NOM-059-SEMARNAT-2001) and similar lists. Astyanax armandoi Lozano-Vilano and Contreras-Balderas, 1990, un caraćido descrito como ende´mico de un pequen ˜ o arroyo en el sur de Me´xico, se considera en este trabajo como sino ´ nimo de A. aeneus (Gu ¨ nther, 1860), especie de amplia distribucio ´ n en el norte de Centroame´rica. La diagnosis de A. armandoi se basa en su labio inferior expandido, junto con un conjunto de caracteres osteolo ´ gicos. La expansio ´ n labial se ha observado tambień en otras poblaciones de Astyanax (en Campeche y en Chiapas, Me´xico) y se trata de un ecofenotipo, una adaptacio ´ n a condiciones de hipoxia. Los caracteres osteolo ´ gicos, merı´sticos, y morfome´tricos de A. armandoi son compatibles con la notable variacio ´ n intra- e interpoblacional de A. aeneus. La localidad tipo ha sido visitada repetidamente durante la u ´ ltima dećada sin que se hayan encontrado ma´s especı´menes identificables como A. armandoi, so ´ lo el tı´pico A. aeneus. Esta conclusio ´ n implica que A. armandoi debe borrarse de la Norma Oficial Mexicana (NOM-059-SEMARNAT-2001) y de listas similares de especies en peligro.

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STYANAX armandoi Lozano-Vilano and ContrerasBalderas, 1990, was described from an unnamed stream at Peńjamo (a Mexican village now called Coronel Gregorio Meńdez Magan ˜ a), near Palenque, Chiapas (although actually in the State of Tabasco, contrary to the statement in the original description), its type locality and only known site of occurrence (17u289N, 91u369W), in the Usumacinta basin. Currently, the species is listed as endangered in Mexico (Norma Oficial Mexicana or NOM059-SEMARNAT-2001). The species was distinguished from A. aeneus (Gu ¨ nther, 1860), widespread in the same basin (and elsewhere in southern Mexico and northern Central America; Miller et al., 2005) mainly because of its expanded lower lip, but also on the basis of several osteological characters. In addition, following Lozano-Vilano and Contreras-Balderas (1990, hereafter LV&CB), A. armandoi has a flatter head profile, nostrils elongate rather than rounded, and lips meeting at an acute angle. The hallmarks of A. armandoi are the papillae and flaps in the extended lower lip. However, these traits are usual in the Characidae and other freshwater fishes when populations face hypoxic conditions; they are thought to provide a means for surface breathing (Winemiller, 1989). The type locality, an unnamed stream, is 2.5–4.0 m wide and 0.3–0.4 m deep. Water temperature was 27uC at the time the types of A. armandoi were captured, although air 1

temperature varied between 25 and 37uC. The bottom is gravelly, with sand and mud (LV&CB, 1990). The seasonally interrupted flow and pollution observed at the site are known to cause periodic episodes of low dissolved-oxygen concentration (Mallin et al., 2006). Reservations about the validity of A. armandoi have been expressed before by other ichthyologists (R. R. Miller, in litt., 1993), albeit never in print. Moreover, a preliminary study by Valdez-Moreno (1997) provided data on the variability of A. aeneus that call into question the osteological distinctiveness of A. armandoi. Because of the prevailing opinion that A. armandoi is an endangered species, and the possibility that the main diagnostic character might be induced by the environment, we undertook a study to examine the validity of the species, by attempting to gather additional samples, reexamine the types, and compare them to a broad sample of populations of A. aeneus. MATERIALS AND METHODS Most meristic, morphometric, and osteological data on Astyanax armandoi are taken from LV&CB’s (1990) original description, since no further specimens have ever been collected. Comparative data on A. aeneus are taken from that same source, as well as from Schmitter-Soto (1998, meristics

El Colegio de la Frontera Sur, Unidad Chetumal, A.P. 424, C.P. 77000, Chetumal, Quintana Roo, Mexico; E-mail: (JJSS) jschmit@ ecosur-qroo.mx. Send reprint requests to JJSS. 2 El Colegio de la Frontera Sur, Unidad San Cristo´bal de Las Casas, A.P. 63, C.P. 29290, San Cristo´bal de Las Casas, Chiapas, Mexico. Submitted: 19 January 2007. Accepted: 24 September 2007. Associate Editor: C. J. Ferraris. DOI: 10.1643/CI-07-012 F 2008 by the American Society of Ichthyologists and Herpetologists

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and morphometrics) and Valdez-Moreno (1997, osteology), and directly from specimens at ECOSC, ECOCH, and UANL. Measurements and counts follow the methods used in the original description, except that proportional distances are consistently given as thousandths of standard length. Selected meristic and morphometric characters were compared between A. armandoi and A. aeneus. The holotype and a cleared-and-stained paratype of A. armandoi were examined (by MEVM) at Universidad Autońoma de Nuevo Leoń. Additional paratypes at Universidad Nacional Autońoma de Me´xico and Instituto Politećnico Nacional were also examined. (See LV&CB, 1990 for the complete list of 57 paratypes.) The syntypes of Tetragonopterus aeneus were examined (by JJSS) at the Natural Museum Museum, London. RESULTS Despite several visits to the type locality of A. armandoi over the last decade (by RRH and AAGD, and also by LV&CB), only normal Astyanax aeneus have been found (specimens at ECOSC, see Material Examined). The stream is highly degraded, with water flow interruptions during the dry season, garbage dumps nearby, and pollution from sewage and detergents. Diagnosis of Astyanax armandoi.—The five characters used to diagnose A. armandoi are evaluated as follows: ‘‘Lower lip expanded’’. As already mentioned, the trait is not unique to A. armandoi. Astyanax aeneus exhibits this character under low oxygen conditions (Calakmul, Campeche, 0.8 mg?l21, Fig. 1; also in Catazaja´ [pers. obs.] and La Encrucijada [E. Vela´zquez, pers. comm., 2007], Chiapas, Pacific versant). LV&CB (1990) argued that all of the A. armandoi specimens show the trait, whereas in other populations the expanded lips do not show up in all or even most specimens. However, most of the Campeche specimens (seven out of eight) display the expanded lips. ‘‘Snout flat in profile, forming an acute angle with the upper lip and gape’’. Astyanax aeneus is contrasted as having its lips meeting in a ‘‘straight’’ fashion and its profile being ‘‘convex’’ (LV&CB, 1990:fig. 3A). The character is, however, extremely variable, some specimens having a convex profile and others a profile straight or even somewhat concave dorsad to the eyes. The lips can also meet in acute angle in many specimens of A. aeneus (Schmitter-Soto, 1998:fig. 3, ECOCH 3089), including the expanded-lip population from Campeche (Fig. 1). ‘‘Orbitosphenoid ventral process clubshaped, with its anterior profile concave, gently curved’’ (LV&CB, 1990:fig. 7A). The description also fits other Astyanax populations, for example, A. aeneus from the Nautla River, Veracruz (UANL 10167, Fig. 2A). On the other hand, this bone is not particularly useful in the taxonomy of the genus Astyanax because of its intrapopulational variability. In several cases, Valdez-Moreno (1997) found as many different shapes as examined individuals from one population. ‘‘Proximal third of the posterior profile of the orbitosphenoid with two discrete angles, flat on its distal two third[s]’’. In LV&CB (1990:table 3), the wording is ‘‘posterior profile [of orbitosphenoid] base 2 step, stairlike; distal[ly] flat’’, and the bone is shown in their figure 7A. Again, similarly shaped orbitosphenoids are found in other Astyanax populations (e.g., UANL 3169, Fig. 2B). In any case, as stated in the preceding paragraph, the orbitosphenoid shows a large

Fig. 1. Head of Astyanax aeneus from Manuel Castilla Brito, Calakmul Biosphere Reserve, Campeche, Mexico (ECOCH 2317), a locality with nearly zero (,1 mg?l21) dissolved-oxygen concentration at the time of capture. Note expanded lower lip, snout flat in profile, and lips meeting at acute angle, as in A. armandoi. (Photograph, H. Bahena.)

degree of intra- and interpopulational variability in Mexican Astyanax (see also Valdez-Moreno and Contreras-Balderas, 2003:fig. 18). This variation was overlooked in the original description of A. armandoi, where composite drawings were presented. ‘‘Anal base ending under a vertical from the adipose fin posterior border’’. The trait is not evident in LV&CB’s (1990) figure 2; in the text (p. 100) the wording is less stringent: ‘‘ . . . to a vertical from the end or behind adipose fin’’. This character is also quite variable. Schmitter-Soto (1998:fig. 3) shows a specimen of A. aeneus from Yucatan whose anal-fin base clearly corresponds to the description of A. armandoi. Additional characters.—In addition to the five diagnostic characters, LV&CB (1990:table 3) provided a comparison of selected characters, most of which were accepted by LV&CB to be the same for A. armandoi and A. aeneus, except for the following: Nostril shape, elongate vs. round. The distinction is not evident in LV&CB (1990:fig. 3). However, the character shows extreme intra- and interpopulational variability. The syntypes of A. aeneus have a nostril that could rightly be described as ‘‘elongate’’ rather than ‘‘round’’ (pers. obs.). Lower lip, prognathous vs. included. Again, the trait is quite variable in A. aeneus. Individuals with the lower lip somewhat protruded (e.g., a syntype of A. aeneus, pers. obs.) are at least as common as those that have the lower lip included or even with upper lip (LV&CB, 1990:fig. 3B). Gape profile ‘‘flat horizontal’’ vs. ‘‘nearly horizontal’’. We find the character to be too subtle to interpret; even in LV&CB (1990:fig. 2), the gape of A. armandoi does not look completely horizontal.

Schmitter-Soto et al.—Astyanax armandoi, junior synonym of A. aeneus

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Fig. 2. Osteological characters of Astyanax aeneus that overlap with those listed as diagnostic for A. armandoi (see text). (A) Orbitosphenoid ventral process; (B) orbitosphenoid posterior profile; (C) premaxillary posterior process; (D) maxillary anterior arm; (E) retroarticular; (F) anguloarticular; (G) dentary mental process; (H) first anterior dentary foramen. (Figures from Valdez-Moreno, 1997.) Bars are 5 mm, except (E), 1 mm.

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Premaxillary posterior process convex vs. concave [at tip]. Valdez-Moreno (1997) depicted specimens of A. aeneus (UANL 5879, Fig. 2C) with premaxillae about as convex as those in LV&CB (1990:fig. 4A). There are populations of A. aeneus where the convexity is even more intense, for example at Coatzacoalcos River (Valdez-Moreno, 1997). Maxillary anterior arm diamond- vs. rod-shaped. Rather than ‘‘diamond-shaped,’’ LV&CB (1990:fig. 5A) show a maxillary anterior arm with a distinct dorsal angle, contrasted to an evenly continuous or somewhat convex dorsal border in other Astyanax. While this angle could not be found in any population of Astyanax studied by ValdezMoreno (1997), the bone proved to be extremely variable: one can find within the same population individuals with a convex dorsal border and others with an almost concave dorsal border in the maxillary anterior arm (UANL 10026, Fig. 2D). Retroarticular heart-shaped vs. roughly quadrangular. Some specimens from the population of A. aeneus at La Nueva River, Chiapas, have a heart-shaped retroarticular (UANL 6319, Fig. 2E). On the other hand, Valdez-Moreno and Contreras-Balderas (2003:fig. 12) show intraspecific variations of this bone in A. mexicanus that are similar to the alleged interspecific variations shown by LV&CB (1990:fig. 6). Anguloarticular 2-pointed vs. 3-pointed. The presence of a third rostrad point in this bone depends on the degree of concavity in the anteroventral edge of the bone. LV&CB (1990:fig. 6A) show an articular with an anteroventral edge so slightly concave that there is no third point, just a curve; however, this trait can vary continuously within a single population, which thus can exhibit 2-pointed or 3-pointed articular bones (e.g., UANL uncat., Fig. 2F). Anguloarticular upper process 2-angled vs. single-angled. This character state could not be verified in the cleared-andstained paratype (UANL 6378); it seems to be an artifact of incomplete staining, as also happens with other features of this bone. Anguloarticular middle process straight vs. curved. The trait can be variable in Astyanax species (e.g., UANL uncat., Fig. 2F). Posterior socket of anguloarticular angled vs. round or ‘‘semilunar’’ (i.e., crescent-shaped). The difference is not obvious in LV&CB (1990:fig. 6), but this socket can be angled rather than rounded in some populations of Astyanax (Valdez-Moreno, 1997). Dentary mental process notched vs. single. The population of A. aeneus at Coatzacoalcos River, Veracruz, has dentary mental processes that can be notched (UANL 2580, Fig. 2G). First anterior dentary foramen under second tooth vs.under third tooth. In a population of A. aeneus from Tamazulapan River, Oaxaca, this foramen occurs under the second tooth (UANL uncat., Fig. 2H). Meristics and morphometrics.—According to LV&CB (1990), only two meristic traits do not overlap completely between A. armandoi and A. aeneus: anal-fin rays and lateral-line scales. The holotype of A. armandoi, as well as three paratypes, displays 28 anal-fin rays (range 24–28), while according to LV&CB (1990:table 2), A. aeneus shows a median of 25 (range 23–27). Using only LV&CB’s (1990) data, the difference between A. armandoi and A. aeneus is significant (t 5 2.9, P , 0.05). However, specimens of A.

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aeneus with 28 anal-fin rays are not uncommon. Comparing A. armandoi vs. a better representation of the species-level variability in A. aeneus (Valdez-Moreno, 1997:table 2; also ECOSC 2987, 3619, 3620, 3621, 3697, and 3849: eleven populations of A. aeneus, spanning from Veracruz to Guatemala, n 5 88, range 23–28 anal-fin rays, median 26), the difference between A. armandoi and A. aeneus turns out to be non-significant (t 5 1.7, P , 0.05). Lateral-line scale counts for A. armandoi range from 34 to 37, median 35; LV&CB (1990:table 2) reported a range of 35–38 for A. aeneus, median 36. The difference in their data is significant (t 5 7.4, P , 0.05). However, again, the range of lateral-line scale counts in a better geographical representation of A. aeneus is wider. Using Valdez-Moreno’s data (1997:table 2) and the above mentioned ECOSC material (same populations, same sample size, range 33–38 lateralline scales, median 35), the difference between A. armandoi and A. aeneus is non-significant (t 5 1.5, P , 0.05). LV&CB (1990:figs. 8, 9) singled out snout length and caudal-peduncle depth (their figure 9) in box-and-whisker graphs that showed at least a distinct tendency towards a longer snout and greater caudal-peduncle depth in A. armandoi. The differences in snout length in LV&CB’s (1990) data are significant (t 5 9.9, P , 0.05). However, we think that the modified mouth of A. armandoi affects the measurement of this character, so a more appropriate comparison would be between A. armandoi and expandedlip populations of A. aeneus. When we measured the specimens of A. aeneus with expanded lips from Campeche (seven specimens, ECOCH 2317), the difference in snout length between this population and the A. armandoi types turned out to be non-significant (t 5 1.3, P , 0.05). As for caudal-peduncle depth, the differences in LV&CB’s (1990) data are also significant between both species (t 5 6.6, P , 0.05), A. armandoi having a mean of 126 (thousandths SL; range 117–138) and A. aeneus a mean of 119 (113–128). However, we felt that the use of only three populations of A. aeneus for comparison did not represent adequately the variation in this species. Using again ValdezMoreno’s data (1997:table 2) and the above mentioned ECOSC material (same populations and sample size), A. aeneus has a mean of 125 (110–130) and the difference in caudal-peduncle depth between both species becomes nonsignificant (t 5 0.5, P , 0.05). As noted above, the ranges of all other meristic and morphometric characters provided by LV&CB (1990:tables 1, 2) overlap completely or almost completely between A. armandoi and A. aeneus. DISCUSSION We have shown that all the diagnostic characters of A. armandoi, whether meristic, morphometric or osteological, and also the external morphology, including the lip flaps, are within the variation range of A. aeneus. Therefore, in the absence of any character that distinguishes the types of A. armandoi from A. aeneus, we conclude that there is no reason to treat A. armandoi as a distinct species and instead place that name in the synonymy of A. aeneus. Lozano-Vilano and Contreras-Balderas (1990) mentioned that they knew ‘‘several cases of lower lip expansion hypothetically caused by hypoxia’’, some of which (three species of poeciliids) they collected simultaneously with A. armandoi. Miller et al. (2005) suggested culturing A. armandoi to check the heritability of the trait, or subjecting the fish to different conditions of dissolved oxygen in the

Schmitter-Soto et al.—Astyanax armandoi, junior synonym of A. aeneus

laboratory, but the idea is not feasible because specimens resembling the types of A. armandoi are no longer to be found at that stream or elsewhere. The conclusion that A. armandoi is not a valid species has implications for conservation. Most authors have recognized A. armandoi as valid (Espinosa Pe´rez et al., 1993:24; Lima et al., 2003:107; Nelson et al., 2004:80; Miller et al., 2005:155), perhaps invoking a precautionary principle, because of the conservation status of the species in Mexico. Now that there is clear evidence that the name does not represent a valid species, it should be removed from the Mexican list of endangered species (NOM-059-SEMARNAT2001) and similar lists. MATERIAL EXAMINED Institutional abbreviations are as listed at http://asih.org/ codons.pdf. Localities (all in Mexico, unless otherwise noted), catalog numbers, and number of specimens (in parentheses) are as follows (additional data can be obtained from the authors on request): Astyanax armandoi. Unnamed stream at Peńjamo (5Coronel Gregorio Meńdez Magan ˜ a), ‘‘Chiapas’’ (actually Tabasco), UANL 6380 (holotype), UANL 6378 (cleared-andstained paratype), IBUNAM 3240 (2 paratypes), IPN uncat. (2 paratypes). A. aeneus. Stream at Las Flores, Oaxaca, BMNH 1860.6.17.41–2, BMNH 1907.4.10.3 (3 syntypes); stream at Manuel Castilla Brito, Campeche, ECOCH 2317 (8); cenote 15 km E of Celestuń, Yucatan, ECOCH 3089 (1); Laguna Patricio at Catazaja´, Chiapas, ECOSC 2987 (30); unnamed stream at Peńjamo (5Coronel Gregorio Meńdez Magan ˜ a), Tabasco, ECOSC 3619 (1), ECOSC 3620 (32), ECOSC 3621 (1), ECOSC 3697 (12), ECOSC 3849 (7); Coatzacoalcos River, Veracruz, UANL 2580 (5); River Huixtla, Chiapas, UANL 3169 (5); Usumacinta River, Chiapas, UANL 5879 (5); River La Nueva, Chiapas, UANL 6319 (5); Santa Rosa, Guatemala, UANL 7382 (3); River Tecolutla, Veracruz, UANL 9861 (5); River Chachalacas, Veracruz, UANL 10026 (5); River Nautla, Veracruz, UANL 10167 (5); River Tamazulapan, Oaxaca, UANL uncat. (5). ´ lamo-Bravo, Tamaulipas, UANL 3932 A. mexicanus. River A (4); River San Juan, Nuevo Leoń, UANL 4924 (4). ACKNOWLEDGMENTS We thank L. Lozano-Vilano and S. Contreras-Balderas for discussing the status of A. armandoi with us, even though they do not agree with the conclusions reached herein. L. LozanoVilano, H. Espinosa-Pe´rez, E. Soto-Galera, O. Crimmen, and P. Campbell kindly allowed examination of type material under their care during visits to UANL, IBUNAM, IPN, and BMNH. E. Vela´zquez shared with us his unpublished finding of expanded lip A. aeneus in the Pacific versant of Chiapas. H. Bahena photographed the specimen at ECOCH.

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LITERATURE CITED Espinosa Pe´rez, H., M. T. Gaspar Dillanes, and P. Fuentes Mata. 1993. Listados faunı´sticos de Me´xico. III. Los peces dulceacuıćolas mexicanos. Instituto de Biologıá, Universidad Nacional Autońoma de Me´xico, Mexico City. Gu ¨ nther, A. 1860. On new reptiles and fishes from Mexico. Proceedings of the Zoological Society of London 1860:316–319. Lima, F. C. T., L. R. Malabarba, P. A. Buckup, J. F. P. da Silva, R. P. Vari, A. Harold, R. Benine, O. T. Oyakawa, C. S. Pavanelli, N. A. Menezes, C. A. S. Lucena, M. C. S. L. Malabarba, Z. M. S. Lucena, R. E. Reis, F. Langeani, L. Cassati, V. A. Bertaco, C. Moreira, and P. H. F. Lucinda. 2003. Genera incertae sedis in Characidae, p. 106–169. In: Check List of the Freshwater Fishes of South and Central America. R. E. Reis, S. O. Kullander, and C. J. Ferraris, , Jr. (eds.). EdiPUCRS, Porto Alegre. Lozano-Vilano, M. L., and S. Contreras-Balderas. 1990. Astyanax armandoi, n. sp. from Chiapas, Mexico (Pisces, Ostariophysi: Characidae) with a comparison to the nominal species A. aeneus and A. mexicanus. Universidad y Ciencia 7:95–107. Mallin, M. A., V. L. Johnson, S. H. Ensign, and T. A. MacPherson. 2006. Factors contributing to hypoxia in rivers, lakes and streams. Limnology and Oceanography 51:690–701. Miller, R. R., W. L. Minckley, and S. M. Norris. 2005. Freshwater Fishes of Me´xico. University of Michigan and University of Chicago Press, Chicago. Nelson, J. S., E. J. Crossman, H. Espinosa-Pe´rez, L. T. Findley, C. R. Gilbert, R. N. Lea, and J. D. Williams. 2004. Common and Scientific Names of Fishes from the United States, Canada, and Mexico, Sixth Edition. American Fisheries Society, Bethesda, Maryland. Norma Oficial Mexicana (NOM-059-SEMARNAT-2001). 2001. Secretarıá de Medio Ambiente y Recursos Naturales, Mexico City (consulted online, April 17, 2006). Schmitter-Soto, J. J. 1998. Diagnosis of Astyanax altior (Characidae), with a morphometric analysis of Astyanax in the Yucatan Peninsula. Ichthyological Exploration of Freshwaters 8:349–358. Valdez-Moreno, M. E. 1997. Estudio comparativo osteolo´gico del geńero Astyanax en diversas cuencas de Me´xico. Unpubl. M.Sc. thesis, Universidad Nacional Autońoma de Me´xico, Mexico City. Valdez-Moreno, M. E., and S. Contreras-Balderas. 2003. Skull osteology of the characid fish Astyanax mexicanus (Teleostei: Characidae). Proceedings of the Biological Society of Washington 116:341–355. Winemiller, K. O. 1989. Development of dermal lip protuberances for aquatic surface respiration in South American characid fishes. Copeia 1989:382–390.