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Inicio Revista Mexicana de Biodiversidad Review of the geographic distribution of Hoffmannola hansi (Gastropoda: Pulmonat...
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Vol. 85. Núm. 2.
Páginas 463-471 (junio 2014)
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Vol. 85. Núm. 2.
Páginas 463-471 (junio 2014)
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Review of the geographic distribution of Hoffmannola hansi (Gastropoda: Pulmonata) in the Mexican Pacific
Revisión del ámbito de distribución geográfica de Hoffmannola hansi (Gastropoda: Pulmonata) en el Pacífico mexicano
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Omar Hernando Avila-Poveda1, Quetzalli Yasú Abadia-Chanona2, Raúl Herrera-Fragoso3, Benoît Dayrat4
1 División de Estudios de Posgrado, Universidad del Mar, 70902 Puerto Ángel, Oaxaca, Mexico.
2 Licenciatura en Biología Marina, Universidad del Mar, 70902 Puerto Ángel, Oaxaca, Mexico. Present address: Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, 23096 La Paz, Baja California Sur, Mexico.
3 Universidad La Salle-Nezahualcoyotl. Av. Bordo de Xochiaca, 57300 Nezahualcóyotl, Estado de México, Mexico.
4 Department of Biology, Pennsylvania State University. University Park, 16802 PA, USA.
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Table 1. Records ol Hoffmannola hansi along the Tropical Eastern Pacilic. Coordinates were taken Irom each original source. Dashed lines indicate unavailable data. Data was organized according to geographical coordinates and area according to country, state, region, and locality. R, is the progressive record for each locality. The gray shadow helping to distinguish each group by state
Abstract

Hoffmannola hansi (Mexican intertidal leather slug) is traditionally reported as an endemic species to the Gulf of California, Mexico. However, its presence in the southern Mexican Pacific has been mentioned in regional checklists and reports. Here we provide new records of H. hansi populations from at least 3 locations from Oaxaca, Mexico. The anatomical characteristics useful for H. hansi identification are described for both, living and preserved specimens. Specimen's reports from the Gulf of California to Oaxaca, Mexico, are mentioned, yielding a revised distribution throughout the Mexican Pacific. A map with the wider geographic distribution of H. hansi is also updated. Therefore, this species is not “endemic” to the Gulf of California, but is distributed throughout the Mexican Pacific. However its distribution is discontinuous with the possible existence of 2 cryptic species geographically separated by the Sinaloan gap: l in the North (Gulf of California) and l in the South. Additional work is needed to explore in more detail the complete geographical range of H. hansi populations on the entire Mexican Pacific Coast.

Key words:
Mollusca
Onchidiidae
non-endemic
Oaxaca
Gulf of California
Tropical Eastern Pacific (TEP)
geographical range
cryptic species
Resumen

Hoffmannola hansi (babosa de cuero intermareal mexicana) es tradicionalmente registrada como una especie endémica del golfo de California, México. Sin embargo, su presencia en el sur del Pacífico mexicano ha sido mencionada en listas de control y en informes regionales. Ofrecemos nuevos registros de poblaciones de H. hansi de al menos 3 localidades de Oaxaca, México. Las características anatómicas que ayudan a identificar a H. Hansi se describen para ejemplares vivos y conservados. Se mencionan los ejemplares desde el golfo de California hasta Oaxaca, México, proporcionando una distribución ampliada a lo largo del Pacífico mexicano. Un mapa con la distribución geográfica de H. Hansi también se actualiza. Por lo tanto, esta especie no es endémica del golfo de California, sino que está bien distribuida en el Pacífico mexicano. Sin embargo, su distribución es discontinua, con la posible existencia de 2 especies crípticas geográficamente separadas por la brecha sinaloense: una en el Norte (golfo de California) y otra en el Sur. Sigue siendo necesario realizar trabajo adicional para explorar en mayor detalle la distribución geográfica completa de las poblaciones de H. hansi en toda la costa del Pacífico mexicano.

Palabras clave:
Mollusca
Onchidiidae
no endémico
Oaxaca
golfo de California
Pacífico Oriental Tropical (POT)
ámbito geográfico
especies crípticas
Texto completo
Introduction

Currently, the Onchidiidae (Mollusca: Gastropoda: Pulmonata) is classified within the pulmonate gastropods (Holznagel et al., 2010; Wu et al., 2010; Dayrat et al., 2011a). However, its phylogenetic position has been heavily debated during the last 8 decades. Authors have considered them as opisthobranchs (Fretter, 1943; Boettger, 1954; Marcus, 1965; Marcus and Marcus, 1967; 1970), pulmonates (Bretnall, 1919; Baker, 1938; Baker, 1955; Ghiselin, 1965; Solem, 1978; Britton, 1984; Barker, 2001; Grande et al., 2004; Dayrat, 2009; Dayrat et al., 2011a,b), euthyneurans (Marcus and Burch, 1965; Selmi et al., 1988; Winnepenninckx et al., 1998; Dayrat and Tillier, 2000; 2002; 2003), or even as a separate Order Onchidiida (Starobogatov, 1976) and Silicodermatae (Labbé, 1934). Regardless, Onchidiidae remains a poorly-known taxon in many regards, especially in species diversity and distribution.

The most interesting aspect of the geographic range for Onchidiidae is that almost all the genera are exclusively found in tropical and subtropical areas from the Indo-West Pacific (Bretnall, 1919; Stringer, 1969; Wu et al., 2010) and the Mediterranean Sea (Barletta and Ghisotti, 1978), excepting 4 nominal Onchidella species and 2 nominal Hoffmannola species (i.e., H. hansi and H. lesliei) that are restricted to the tropical Eastern Pacific (Dayrat, 2009; Dayrat et al., 2011b). Onchidella has an extensive geographical range in all the tropical Eastern Pacific; while Hoffmannola hansi is restricted to the Northern Gulf of California and Hoffmannola lesliei to the Galapagos (e.g., Marcus and Marcus, 1967, 1970; Keen, 1971; Hendrickx et al., 2005; Dayrat, 2009; Dayrat et al., 2011a).

Hoffmannola hansiMarcus and Marcus, 1967 (for nomenclatural information, see, Dayrat et al., 2011b) has been known by its description as “endemic” commonly found in the rocky, intertidal communities of the Gulf of California, Mexico, across shores from Baja California Norte, Sonora, and Sinaloa (Marcus and Marcus, 1967, 1970; Keen, 1971; Hendrickx et al., 2005; Zamora-Silva and Naranjo-García, 2008; Dayrat, 2009; ASDM, 2011; Dayrat et al., 2011a). Nevertheless, various publications, reports, and regional checklists (none of which citing any deposited material) have mentioned H. hansi in other Mexican states and localities outside the Gulf of California and further south into the Mexican Pacific, such as, Jalisco (Esqueda-González, 1995; Esqueda et al., 2000), Jalisco, Colima and Michoacán (Holguín-Quiñones and González-Pedraza, 1994), Michoacán (Villaseñor-Gómez, 2005), Guerrero (Flores-Garza et al., 2005; 2007; Flores-Rodríguez et al., 2001, 2003, 2007, 2012; Flores-Rodríguez, 2004; Valdés-González et al., 2004) and Oaxaca (Rodríguez-Palacios et al., 1988; León-Herrera, 2000; 2001; Ramírez-González, 2008). Although they did not cite any actual specimens, those publications suggest that H. hansi may not be endemic to the Gulf of California.

The present study provides a review of the geographic distribution of H. hansi from available original literature (e.g., reports, grey literature, and regional checklists), several online databases of museum collections and specimens collected by our group Oaxaca, Mexico.

Material and methods

Specimens of different sizes of H. hansi were found while sampling for Chiton (Chiton) articulatus at Oaxaca (Avila-Poveda, 2013; Avila-Poveda and Abadia-Chanona, 2013). They were living next to 2 other species of mollusks (Chiton (Chiton) articulatus and/or Plicopurpura pansa) within crevices at high tide, or by themselves on the surface of rocks during low tide (Fig. 1). Several specimens of H. hansi were collected (n=18, 14TL48mm, total length, Fig. 2), in March, April, August, and October 2011 from 3 localities in Oaxaca, Mexico: 1) Puerto Angel (15°39’ N, 96°29’ W); 2) El Faro, Puerto Angel (15°39’ N, 96°30’ W), and 3) Conejos Bay, Huatulco (15°46’ N, 96°04’ W).

Figure 1.

Hoffmannola hansi. Live animals (∼50 specimens in picture) observed in the rocky intertidal of El Faro, Puerto Angel, Oaxaca, Mexico (15°39'N-96°30'W), USNM 1155112. The arrow indicates a 2 pesos Mexican coin (23mm diameter).

(0.39MB).
Figure 2.

Preserved specimens of different sizes of Hoffmannola hansi. The viscous fluid secreted by the marginal gland (repugnatorial gland) is observed in the periphery of each specimen.

(0.08MB).

Three specimens (45±3mm TL, Fig. 3) were relaxed and allowed to extend for 1h, with gradual additions of tap water to the seawater, until the salinity reached half the salinity of the seawater of the sampling site (i.e., 50:50 in volume: Avila-Poveda, 2013) and accelerating the relaxation process by adding few milliliters of 10% ethanol (after Lincoln and Sheals, 1979). Later, specimens were fixed in 10% neutral formalin-saline solution in seawater for 2 weeks and subsequently preserved in 70% ethanol (Avila-Poveda and Baqueiro-Cárdenas, 2009). Other specimens were preserved in 95% ethanol for future molecular work (Dayrat lab). The external and internal morphologies were studied under a dissecting microscope.

Figure 3.

Hoffmannola hansi. Live animals (A); and fixed and preserved individuals used for dissection (B). Collected at El Faro, Puerto Angel, Oaxaca, Mexico (15°39'N-96°30'W). Same number of asterisks indicates the same specimen.

(0.14MB).

Specimens were (or shortly will be) deposited in museums in the region: 1) Laboratorio de Sistemática de Invertebrados Marinos (LABSIM), Universidad del Mar, Puerto Angel, Oaxaca, Mexico; 2) California Academy of Sciences (CAS), San Francisco, California, USA; 3) Santa Barbara Museum of Natural History (SBMNH), Santa Barbara County, California, USA; 4) Scripps Institution of Oceanography (SIO), San Diego, California, USA; 5) Arizona-Sonora Desert Museum (ASDM), Tucson, Arizona, USA; 6) Smithsonian National Museum of Natural History (NMNH), NW Washington, D.C., USA.

A checklist and a map of the geographic distribution of H. hansi were developed, based on records found for this species in scientific databases and web sites (e.g., BHL, BioStor, JSTOR, among many others), available original literature (e.g., reports and checklists), online databases of museum collections (e.g., ASDM, CAS, LABSIM, NMNH, SBMNH, SIO) and with the samples collected by our group Oaxaca, Mexico.

Results

The most important anatomical characters observed that help to identify the species are (for additional information, see: Dayrat et al., 2011b): 1) the total length of live specimens ranges from 14mm to 48mm (Fig. 3A) while preserved material is on average 25% shorter (e.g., the largest live specimen of 48mm long measures only 33mm once preserved; see, Fig. 3B); exceptionally, we observed specimens in the field that were longer than 48mm, but in areas with difficult access; 2) the total width of the hyponotum (left and right side, H) relative to the width of the pedal sole (S) is around the third or fourth part (i.e., H<<<S) with H-S-H of 5-16/22-5mm for live organisms, while these are 4–13/18–4mm for the same preserved organisms; 3) there are generally about 14 marginal glands on the left and about 15 on the right; 4) the visceral cavity is divided in 2 by a septum (which actually is a characteristic of Hoffmannola).

During the sampling months (i.e., March, April, August, and October), early life stages of various species of intertidal mollusks such as Chiton (Chiton) albolineatus, Chiton (Chiton) articulatus, Echinolittorina aspera, Echinolittorina modesta, Plicopurpura pansa, Nerita scabricosta, and Hoffmannola hansi, among many others mollusks, were observed in large stocks that resembled a nursery.

A geographic distribution of H. hansi specimens was found available broadly over the Mexican pacific, and not just restricted to the Gulf of California (Table 1; Fig. 4).

Table 1.

Records ol Hoffmannola hansi along the Tropical Eastern Pacilic. Coordinates were taken Irom each original source. Dashed lines indicate unavailable data. Data was organized according to geographical coordinates and area according to country, state, region, and locality. R, is the progressive record for each locality. The gray shadow helping to distinguish each group by state

R  Catalog number  Coordinates  Geographical area and locality  Year of collection  Sources 
USNM 771808  45°N-125°W  USA, Washington, Fort Canby State Park***  1970  NMNH 2011 
USNM 710013  41°N-71°W  USA, New Hampshire, Pittsfield***  1974  NMNH 2011 
USNM 678419  29°N-113°W  Mexico, Baja California, Gulf of California, San Agustín  1967*  NMNH 2011, Marcus and Marcus 1967 
—  29°N-113°W  Mexico, Baja California, Gulf of California, Angel de la Guarda Island  —  ASDM 2011, Hendrickx et al. 2005 
—  29°N-113°W  Mexico, Baja California, Gulf of California, Angel de la Guarda Island  —  Keen 1971 
—  29°N-113°W  Mexico, Baja California, Gulf of California, San Agustín  1966  Marcus and Marcus 1970 
—  28°N-111°W  Mexico, Sonora, Gulf of California, Kino Bay  —  Keen 1971 
USNM-753651  27°N-110°W  Mexico, Sonora, Gulf of California, El Sahuaral  1966  NMNH 2011 
USNM 753653  27°N-110°W  Mexico, Sonora, Gulf of California, El Sahuaral  1966  NMNH 2011 
10  CAS-81809  23°N-106°W  Mexico, Sinaloa, Gulf of California, Gaviotas Beachs  1953  CAS 2011 
11  CNMO 1783**  23°N-106°W  Mexico, Sinaloa, Gulf of California, Cerro Crestón Beachs  1987  Zamora-Silva and Naranjo-García 2008 
12  —  23°N-106°W  Mexico, Sinaloa, Gulf of California, Mazatlán  —  ASDM 2011, Hendrickx et al. 2005 
13  CMLE  19°13'N- 104°42'W  Mexico, Jalisco, Melaque  1987-1989  Holguín-Quiñones and González-Pedraza 1994 
14  —  19°14'N- 104°46'W  Mexico, Jalisco, Cuastecomate Bay, La Calechosa  1993–1994  Esqueda-González 1995, Esqueda et al. 2000 
15  CMLE  19°06'N-104°20'W  Mexico, Colima, Las Hadas, Club de Yates Beach  1987–1989  Holguín-Quiñones and González-Pedraza 1994 
16  —  18°N-103°W  Mexico, Michoacán  —  Villaseñor-Gómez 2005 
17  CMLE  18°20'N-103°30'W  Mexico, Michoacán, Faro de Bucerías town  1987–1989  Holguín-Quiñones and González-Pedraza 1994 
18  CMLE  18°16'N-103°20'W  Mexico, Michoacán, Maruata town  1987–1989  Holguín-Quiñones and González-Pedraza 1994 
19  CMLIECS§,b  17°47'N-101°44'W  Mexico, Guerrero, Troncones Beach  2000/2001/2005  a, b, d, e, g 
20  —  17°32'N-101°26'W  Mexico, Guerrero, Barra de Potosí Beach  2000/2001/2005  a, d, e, g 
21  —  17°15'N-101°01'W  Mexico, Guerrero, Tlacoyunque Beach  2000/2001/2005  a, d, e, g 
22  —  16°49'N-99°54'W  Mexico, Guerrero, La Roqueta- “Palmitas” Island  2000/2001/2005  a, e, g, h 
23  —  16°42'N-99°54'W  Mexico, Guerrero, La Roqueta- “Zoológico” Island  2000/2001/2005  a, c, e, g, h 
24  —  16°33'N-98°46'W  Mexico, Guerrero, Las Peñitas Beach  2000/2001/2005  a, e, g 
25  —  16°32'N-98°54'W  Mexico, Guerrero, Ventura Beach  2000/2001/2005  a, e, f, g 
26  —  16°19'N-98°34'W  Mexico, Guerrero, Punta Maldonado Beach  2000/2001/2005  a, e, g 
27  —  15°46'N-96°05'W  Mexico, Oaxaca, Tangolunda Bay  —  León-Herrera 2001,2000 
28  —  15°46'N-96°04'W  Mexico, Oaxaca, Conejo Beach  2011  This study 
29  —  15°45'N-96°07'W  Mexico, Oaxaca, Violin Beach  —  León-Herrera 2001,2000 
30  —  15°45'N-96°07'W  Mexico, Oaxaca, Arroyo Beach  —  Ramírez-González 2008, León-Herrera 2001, 2000 
31  —  15°44'N-96°07'W  Mexico, Oaxaca, India Beach  —  León-Herrera 2001,2000 
32  —  15°43'N-96°10'W  Mexico, Oaxaca, Cacaluta Island  2005  Ramírez-González 2008 
33  —  15°41'N-96°26'W  Mexico, Oaxaca, Tijera Bay  —  León-Herrera 2001,2000 
34  USNM 1155112  15°39'N-96°30'W  Mexico, Oaxaca, Rierto Ángel, El Faro  2011  This study 
35  UMAR-Gast-001  15°39'N-96°29'W  Mexico, Oaxaca, Puerto Ángel town  2011  This study 
36  —  15°39'N-96°29'W  Mexico, Oaxaca, Rierto Ángel  —  Rodríguez-Palacios et al. 1988, León-Herrera 2001, 2000 
*

Collected date only mentioned by Marcus and Marcus (1967)

**

Colección Nacional de Moluscos (CNMO), Instituto de Biología, Universidad Nacional Autónoma de México (UNAM).

***

Questionable localities, outside of the Tropical Eastern Pacific Region, possible errors. Feedback was sent to NMNH for its review.

§

Colección de Moluscos del Laboratorio de Investigación en Ecología Costera y Sustentabilidad (CMLIECS), Unidad Académica de Ecología Marina, Universidad Autónoma de Guerrero, Mexico.

Colección de Moluscos del Laboratorio de Ecología (CMLE), Escuela Nacional de Ciencias Biológicas, Mexico.

Colección Científica de Invertebrados, Laboratorio de Sistemática de Invertebrados Marinos (LABSIM), Universidad del Mar, campus Rierto Ángel, Oaxaca, Mexico.

Figure 4.

Geographical distribution of Hoffmannola hansi along the Tropical Eastern Pacific. Records (R) according to Table 1. A star (⋆) marks 2 questionable localities, outside the Tropical Eastern Pacific (catalog numbers USNM 771808 and USNM 710013; NMNH 2011).

(0.11MB).
Discussion

The checklist and map presented here show many more records of Hoffmannola hansi towards the Mexican south Pacific (records No. 13 to 36, total 24: Table 1; Fig. 4) than northern locations, where it has been termed as “endemic” to the Gulf of California ((records No. 3 to 12, total 10: Table 1; Fig. 4). Thus, H. hansi has been previously recorded in Jalisco (Esqueda et al., 2000), Jalisco, Colima and Michoacán (Holguín-Quiñones and González-Pedraza, 1994), Michoacán (Villaseñor-Gómez, 2005), Guerrero (Flores-Garza et al., 2005; 2007; Flores-Rodríguez et al., 2001, 2003, 2007, 2012; Flores-Rodríguez, 2004; Valdés-González et al., 2004) and Oaxaca (Rodríguez-Palacios et al., 1988; León-Herrera, 2000; 2001; Ramírez-González, 2008).

Based on information presented here, the localities of Puerto Angel, El Faro, and Conejos Bay of Huatulco, all in the state of Oaxaca, Mexico, should be incorporated into the species geographical distribution, as well as the states of Jalisco, Colima, Michoacán, and Guerrero, in Mexico, where H. hansi (Mexican intertidal leather slug) has been mentioned from the rocky intertidal.

In any case, H. hansi is not endemic to the Gulf of California, but is distributed throughout the Mexican Pacific, although its distribution is quite discontinuous. However, H. hansi requires rocky shores to live and large parts of the coast between the Gulf of California and southern Mexico are sandy beaches, especially the Sinaloan gap (Hastings, 2000). However, additional work is still needed to explore in more detail the complete geographical range of H. hansi populations on the entire Mexican Pacific Coast.

Currently, as only morphological data are available and as populations from the Gulf of California and those from Oaxaca are not distinguishable, it is more parsimonious to regard them all as part of the same species, H. hansi. However, it cannot be excluded that molecular data could reveal the existence of 2 cryptic but separate species, one in the North (Gulf of California) and one in the South, both separated geographically by the long Sinaloan gap. Various types of patterns of distribution have been found by authors for rocky, intertidal species from the tropical Eastern Pacific (e.g., Hastings, 2000; Wares, 2001; Craig et al., 2006; Pitombo and Burton, 2007; Wares et al., 2009). Both onchidiid species, H. hansi and Onchidella binneyi (also distributed all along the Mexican Pacific), seem ideal candidates for such population studies (Dayrat et al. 2011b).

On the other hand, some errors were unveiled in the literature as well as online databases. Two museum records for H. hansi (NMNH 2011: USNM 771808 and USNM 710013) are likely to be incorrect, or at least questionable, since they are outside of the tropical Eastern Pacific and even in a different region of the Western Atlantic (Fig. 4). Feedback has been sent to NMNH Customer Service for its review (Avila-Poveda, pers. comm.).

Acknowledgments

This work was personally assured by Avila-Poveda OH with SNI-Conacyt stimulus (record No. 44175, from January to July 2012). Avila-Poveda OH gives special thanks for the family grant that covered his stay in the location during the course of this study. Thanks to Saúl Jaime Serrano- Guzmán for transporting the specimens to Benoît Dayrat at the School of Natural Sciences, University of California at Merced, California, USA. Thanks to Francisco Benitez- Villalobos for transporting and depositing some specimens in the NMNH (USNM 1155112). All rare references were downloaded via the Biodiversity Heritage Library (http://www.biodiversitylibrary.org/), Bioline International (http://www.bioline.org.br/), BioStor (http://biostor.org/), and Internet Archive (http://www.archive.org/).

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