RESEARCH NOTE A new record in a well-established population of Octopus hubbsorum

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1 A New Record in a Well-Established Population of Octopus hubbsorum (Cephalopoda: Octopodidae) Expands its Known Geographic Distribution Range and Maximum Size Author(s): José F. Domínguez-Contreras, Bertha P. Ceballos-Vázquez, Frederick G. Hochberg and Marcial Arellano-Martínez Source: American Malacological Bulletin, 31(1): Published By: American Malacological Society DOI: URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 Amer. Malac. Bull. 31(1): (2013) RESEARCH NOTE A new record in a well-established population of Octopus hubbsorum (Cephalopoda: Octopodidae) expands its known geographic distribution range and maximum size José F. Domínguez-Contreras 1, 2, Bertha P. Ceballos-Vázquez 2, Frederick G. Hochberg 3 and Marcial Arellano-Martínez 2 1 Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, A.P , México D.F , México 2 Centro Interdisciplinario de Ciencias Marinas, Departamento de Pesquerías y Biología Marina, Ave. IPN s/n, Col. Playa Palo de Santa Rita, A.P. 592, La Paz, Baja California Sur, 23096, México 3 Department of Invertebrate Zoology, Santa Barbara Museum of Natural History, 2559 Puesta del Sol, Santa Barbara, California 93105, U.S.A. Correspondence: Marcial Arellano-Martínez: marellam@ipn.mx Abstract. Octopus hubbsorum Berry, 1953 is an important fishery species off the Pacific coast of Mexico. It inhabits the intertidal and subtidal zones to depths of 30 m. Its occurrence has been documented in tropical and subtropical zones. In Mexico, it is in the Gulf of California and at some localities of the southern Mexican Pacific, including the Revillagigedo Islands. In this paper, the presence of a well-established population of O. hubbsorum in Bahía Magdalena (on the west coast of the Baja California peninsula) is presented. This new record expands the distribution range not only in distance but also into a temperate zone. Additionally, the maximum size records for this species are extended (1020 mm total length; 220 mm dorsal mantle length; and 3705 g total weight). Key words: cephalopod, occurrence of Octopus hubbsorum, Baja California peninsula, temperate zone At least nine octopus species inhabit the Pacific coast of Mexico (Roper et al. 1995). However, the distribution ranges of many of them are still poorly-known (López-Uriarte et al. 2005), with implications for their management, as in many localities this resource is subject to exploitation without even knowing which species is being caught (Sánchez 2003). Octopus hubbsorum Berry, 1953 is a benthic species that is known to inhabit the intertidal and subtidal zones to depths of 30 m (Keen 1971). It was first described from specimens captured in Bahía San Carlos, Gulf of California (Berry 1953) and, since then, its scientific name has remained unchanged (Norman and Hochberg 2005). Its presence has been recorded in other localities throughout the Gulf (Hochberg 1980, Roper et al. 1995, Pliego-Cárdenas et al. 2011), and has even been considered as endemic to this region (Hendrickx et al. 2005). Nevertheless, this species also has been recorded at some other localities of the southern Mexican Pacific, including the Revillagigedo Islands (Gotshall 1987) and Melaque, Jalisco (Aguilar and Godínez-Domínguez 1995). The most recent report confirmed its presence in 24 additional localities along the southern Mexican Pacific, thus expanding its distribution range to Salina Cruz, Oaxaca, México (16 10 N, W) (López-Uriarte et al. 2005). However, the occurrence of this species in the northern Mexican Pacific has not been previously reported. 95 This note documents a new record of O. hubbsorum in Bahía Magdalena, a locality on the west coast of the Baja California peninsula, which expands its northernmost distribution limit and also increases its maximum size reported. As part of a larger study on octopus reproduction, 300 specimens of Octopus hubbsorum were captured from November 2008 through November 2009 at Bahía Magdalena, Baja California Sur (B.C.S.) México (24 37 N, W) (Fig. 1). The specimens were caught using a hook by skin-diving at a maximum depth of 5 m. The specimens were transported to the Laboratory of Marine Invertebrates of the Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN) where their total length (TL), dorsal mantle length (DML) and total body mass (TW) were recorded, with ± 1 mm and ± 0.1 g accuracy, respectively. The specimens were examined and identified using the Hochberg (1980) s and Roper et al. (1995) s taxonomic keys together with the Berry (1953) s original description. Several preserved voucher specimens were sent to the Santa Barbara Museum of Natural History (SBMNH), where the identification was confirmed. The voucher specimens are housed in the collections at the museum (SBMNH ). The main diagnostic features that confirm the occurrence of Octopus hubbsorum in Bahía Magdalena were:

3 96 AMERICAN MALACOLOGICAL BULLETIN Figure 1. Octopus hubbsorum: Distribution on the Pacific coast of Mexico, including the Gulf of California. The star indicates the sampling zone for O. hubbsorum described in this study. 1) mantle shape round to oval; 2) arms robust, proximal ends thick and muscular, distal ends tapered to thin tips; 3) arm lengths 3 to 4 times mantle length; 4) second pair of arms longer than other three pairs; 5) second and third pair of proximal suckers enlarged in both sexes; 6) hectocotylus very small (approximately 1.4 mm), ligula and calamus conical in shape; 7) gills with 9 to 10 lamellae per demibranch; and 8) small eggs. These characteristic features of this species are very similar to those of Octopus bimaculatus Verrill, 1983, except for the absence of ocelli in O. hubbsorum. Living specimens are dark grey-, green-, or red-colored. Specimens preserved in formalin show a purple coloration (Berry 1953, Hochberg 1980, Roper et al. 1995). Unfortunately, for O. hubbsorum a body patterning ethogram does not exist, which may help in their identification in the field, as occurs in other species of octopuses (Packard and Hochberg 1977, Hanlon 1988, Roper and Hochberg 1988, Hochberg et al. 2005, Huffard 2007). The number of specimens captured during our sampling (N = 300) confirms the fact that a large population of O. hubbsorum exists in Bahía Magdalena, B.C.S. The size of the specimens ranged between 50 and 220 mm DML (mean = mm) and between 280 and 1020 mm TL (mean = mm). Total body mass ranged from 89.1 to 3705 g (mean = g). Table 1 shows the size and weight ranges that have been reported for Octopus hubbsorum at various localities along its distribution range. Data for Espíritu Santo Island, and Loreto and Puerto Ángel bays come from massive samplings (N = 230, 281, and 352 respectively), those for Jalisco coasts (N = 6000) come from the local artisanal fishery, whereas those for Bahía San Carlos come from a small sample (N = 2). Specimens of O. hubbsorum from Bahía Magdalena had the largest size and weight values compared to those previously reported, followed by the specimens caught off the coast of Jalisco. It has been considered that both temperature and food availability are causes of interspecific variation in the growth of many animal species (Griffiths and Griffiths 1987). In this regard, the localities where smaller sizes have been reported are Bahía Puerto Ángel, which is a tropical zone, and the Gulf of California, which is a transitional tropical-subtropical zone (Hendrickx et al. 2005) with a maximum temperature of 30 C (Villalejo-Fuerte et al. 2004). On the other hand, Farias et al. (2009) mentioned that cold-water cephalopod species could be more efficient than tropical species and suggested that physiological adaptations

4 RANGE EXTENSION AND SIZE OF OCTOPUS HUBBSORUM 97 Table 1. Octopus hubbsorum: Maximum sizes (length and weight) reported at various locations in its geographical range: DML, dorsal mantle length; TL, total length; TW, total body mass; unk, unknown; averages are shown in parenthesis, when available. Locality TL (mm) DML (mm) TW (g) Reference Gulf of California Coast Bahía San Carlos unk Berry (1953) (27 56 N, W) unk 70 unk Hochberg (1980) unk ~90 unk Roper et al. (1995) Bahía de Loreto 790 unk 1108 Bravo-Olivas (2008) (25 59 N, W) (526) unk (516) Isla Espíritu Santo 650 unk 1400 Pliego-Cárdenas et al. (2011) (24 24 N, W) Pacific Coast Bahía Magdalena Present study (24 37 N, W) (554.5) (120.6) (766.6) Bahía de Puerto Ángel unk Alejo-Plata et al. (2009) (15 40 N, W) Jalisco López-Uriarte (2006) (20 40 N, W) (447.2) (99.9) (586.3) are present that allow them to optimally exploit environmental conditions through the year despite the low temperatures. This likely explains the larger size of Octopus hubbsorum in Bahía Magdalena, which is a temperate zone (Briggs 1974) with minimum temperatures of 15 C maximum temperatures ranging from 20.3 to 26.6 C (Lluch-Belda et al. 2000), and with high primary productivity (Gómez-Gutiérrez et al. 2001). Figure 1 shows the distribution of historical records of Octopus hubbsorum in the northeastern Pacific Ocean including those archived at the U.S. National Museum of Natural History (NMNH ), the SBMNH ( ), those reported by López-Uriarte et al. (2005), and those obtained in this study. This historical analysis shows that this species had not been previously recorded from the west coast of the Baja California peninsula. The closest locality record was from Cabo San Lucas, at the southern tip of the Baja California peninsula (Hochberg, 1971, López-Uriarte et al. 2005, Hochberg pers. obs.). Our findings of a well-established population not only expand the known geographical range of O. hubbsorum approximately 320 km northwards in the eastern Pacific but its occurrence in Bahía Magdalena also indicates that this species is able to inhabit temperate waters, and not only the tropical or subtropical waters where it had been previously recorded. In addition, the NMNH collection archive contains a total of 13 records of this species which, according to their database, come from the Sonora coast in the Gulf of California. The origin of one of these records, however, is confusing as the coordinates provided (32 00 N, W) actually correspond to a locality on the coast near Ensenada, off the northwestern part of the Baja California peninsula, some 949 km north of Bahía Magdalena. The above opens up the possibility of its also being periodically present in other localities farther north in the Eastern Pacific, including the Ensenada coast (Jesús María, El Rosario, San Quintín), where an important fishery operates on a yet undetermined octopus species. On the other hand, specimens of Octopus hubbsorum also have been recorded in the southeastern Pacific and the Gulf of California. A total of 13 records from the Mexican Pacific are archived in the NMNH and they mostly correspond to those reported by López-Uriarte et al. (2005), except for those from the Revillagigedo Islands (18 47 N, W) and the Gulf of Panama (8 02 N, W). Of the seven records archived in the SBMNH, four were collected in the Gulf of California and the other three from the Malpelo Islands (4 59 N, W) off the Pacific coast of Colombia. These records suggest that O. hubbsorum is an octopus species with one of the broadest distribution ranges in the eastern Pacific, encompassing approximately 4300 km, from northwest Mexico (Bahía Magdalena) down to the coast of Cauca in Colombia. Unfortunately, no records of Octopus hubbsorum from countries in Central America (Guatemala, El Salvador, Honduras, Nicaragua, or Costa Rica) that bridge the distribution from Mexico to Colombia (Salina Cruz, Oaxaca, Mexico to Malpelo Island, Colombia) have been reported in the literature or identified in museum collections. On the other hand, the identification of specimens from Panama and Colombia should be taken with caution as the morphological similarity with O. mimus Gould, 1852 is high and these two species have been considered as cryptic, still undifferentiated species (Hochberg, pers. obs.). Because of this, we recommend: 1) using molecular analyses to determine interspecific identification; 2) obtaining new records from along the coasts of Central America; 3) updating databases for species of octopus that

5 98 AMERICAN MALACOLOGICAL BULLETIN inhabit the eastern Pacific; and 4) studying living O. hubbsorum in order to develop a body patterning ethogram to help with species identification in the field. These recommendations could help to better define the actual distribution range of O. hubbsorum. An important octopus fishery is present in the Mexican Pacific and the Gulf of California that mostly targets Octopus bimaculatus and O. hubbsorum (Alejo-Plata et al. 2009). The latter species predominates in the catches at most localities where its occurrence has been reported (López-Uriarte et al. 2005), including Bahía Magdalena, where it accounts for approximately 80% of the total catch as opposed to the total catch of O. bimaculatus which is about 20% (local fishermen, pers. comm.). Despite the importance of this and other octopus species, their geographical ranges, life histories, and biology are still poorly-known. Additional research efforts are therefore necessary to determine what species occur in the region and what their geographical distribution range is, as well as to better understand their biology. ACKNOWLEDGMENTS This research was funded by projects SIP , SIP and SIP M Arellano-Martínez and B.P. Ceballos-Vázquez received grants from SIBE (COFAA), EDI (IPN), and SNI-CONACYT. J.F. Domínguez-Contreras received a scholarship from CONACyT (226153); the results here presented are part of his Master s thesis. Thanks to M. Sánchez-Salazar for translating the manuscript. LITERATURE CITED Aguilar, S. C. and E. Godínez-Domínguez E Presencia del pulpo Octopus hubbsorum (Cephalopoda: Octopoda) en el Pacífico Central Mexicano. Revista de Biología Tropical 45: 678. [In Spanish] Alejo-Plata, M., J. L. Gómez-Márquez, S. Ramos-Carrillo, and J. E. Herrera-Galindo Reproducción, dieta y pesquería del pulpo Octopus hubbsorum (Mollusca: Cephalopoda) en la costa de Oaxaca, México. Revista de Biología Tropical 57: [In Spanish] Berry, S. S Preliminary diagnoses of six west American species of octopus. Leaflets in Malacology 1: Bravo-Olivas, M. L Aspectos Reproductivos del Pulpo Octopus hubbsorum Berry, 1953 en el Parque Nacional Bahía de Loreto Golfo de California. M.S. Thesis. Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, La Paz, México. [In Spanish] Briggs, J. C Marine Zoogeography. McGraw Hill, New York. Farías, A., I. Uriarte, J. Hernández, S. Pino, C. Pascual, C. Cammal, P. Domíngues, and C. Rosas How size relates to oxygen consumption, ammonia excretion, and ingestion rates in cold (Enteroctopus megalocyathus) and tropical (Octopus maya) octopus species. Marine Biology 156: Gómez-Gutiérrez, J., R. Palomares-García, S. Hernández-Trujillo, and A. Carballido-Carranza Community structure of zooplankton in the main entrance of Bahía Magdalena, México during Revista de Biología Tropical 49: Gotshall, D. W Marine Animals of Baja California: A Guide to the Common Fishes and Invertebrates. Sea Challenger, Monterey, California. Griffiths, C. L. and J. S. Griffiths Bivalvia. In: J. H. Pandian. and F. J. Vernberg, eds., Animals Energetics. Vol. 2. Academic Press, New York. Pp Hanlon, R. T Behavioral and body patterning characters useful in taxonomy and field identification of cephalopods. Malacologia. 29: Hendrickx, E. M., R. C. Brusca, and L. T. Findley A distributional checklist of the macrofauna of the Gulf of California, México. Part I. Invertebrates. Desert Museum and Conservation International, Arizona-Sonora. Hochberg, F. G Class Cephalopoda. In: R. C. Brusca, ed., Common Intertidal Invertebrates of the Gulf of California. University of Arizona Press, Tucson, Arizona. Pp Hochberg, F. G., M. D. Norman and C. L. Huffard Summary of CIAC Octopus Workshop. In: C. Chotiyaputta, E.M.C. Hatfield and C.-C. Lu, eds., Cephalopod Biology, Recruitment and Culture: International Cephalopod Symposium and Workshops, February Phuket Marine Biological Center Research Bulletin 66: 5 9. Huffard, C. L Ethogram of Abdopus aculeatus (d Orbigny, 1834) (Cephalopoda: Octopodidae): Can behavioural characters inform octopodid taxonomy and systematics? Journal of Molluscan Studies 73: Keen, A. M Sea Shells of Tropical West America. Stanford University Press, California. López-Uriarte, E Ciclo Vital y Pesca del Pulpo Octopus hubbsorum Berry 1953 (Cephalopoda: Octopodidae) en la Costa de Jalisco, México. Ph.D. Dissertation. Universidad de Guadalajara. Guadalajara, México. [In Spanish] López-Uriarte, E., E. Ríos-Jara, and M. Pérez-Peña Range extension for Octopus hubbsorum Berry, 1953 (Mollusca: Octopodidae) in the Mexican Pacific. Bulletin of Marine Science 77: Lluch-Belda, D., M. E. Hernández-Rivas, R. Saldierna-Martínez, and R. Guerrero-Caballero Variabilidad de la temperatura superficial del mar en Bahía Magdalena, B.C.S. Oceánides 15: [In Spanish] Norman, M. D. and F. G. Hochberg The current status of octopus taxonomy. Phuket Marine Biological Center Research Bulletin 66: Packard, A. and F. G. Hochberg Skin patterning in Octopus and other genera. In: M. Nixon and J. B. Messenger, eds., The Biology of Cephalopods. Symposium of the Zoological Society, London 138: Pliego-Cárdenas, R., F. A. García-Domínguez, B. P. Ceballos- Vázquez, M. Villalejo-Fuerte, and M. Arellano-Martínez

6 RANGE EXTENSION AND SIZE OF OCTOPUS HUBBSORUM 99 Reproductive aspects of Octopus hubbsorum (Cephalopoda: Octopodidae) from Espiritu Santo Island, southern Gulf of California, México. Ciencias Marinas 37: Roper, C. F. E. and F. G. Hochberg Behavior and systematics of cephalopods from Lizard Island, Australia, based on color and body patterns. Malacologia 29: Roper, C. F. E., M. J. Sweeney, and F. G. Hochberg Cefalópodos. In: W. Fischer, F. Krupp, W. Schneider, C. Sommer, K. E. Carpenter, and V. H. Niem, eds., Guía FAO para la Identificación para los Fines de la Pesca. Pacifico Ventro-Oriental. Volumen I. Plantas e Invertebrados. FAO, Roma, Italy. Pp [In Spanish] Sánchez, P Cephalopods from off the Pacific coast of Mexico: Biological aspects of the most abundant species. Scientia Marina 67: Villalejo-Fuerte, M., M. Arellano-Martínez, M. Robles-Mungaray, and B. P. Ceballos-Vázquez Notes on the growth, survival, and reproduction of the lion s paw scallop Nodipecten subnodosus maintained in a suspended culture. Hidrobiológica 14: Submitted: 1 February 2012; accepted: 4 August 2012; final revisions received: 6 October 2012

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