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First record of vertical movements of the totoaba (Totoaba macdonaldi) as evidenced by pop-up satellite tags in the Upper Gulf of California

Published online by Cambridge University Press:  14 January 2020

Cristina Hernández-Tlapale
Affiliation:
Centro de Investigaciones Biológicas de Noroeste, S.C. (CIBNOR), Instituto Politécnico Nacional # 195, Playa Palo de Santa Rita, La Paz, B.C.S., C.P. 23096, México
Juan Antonio De-Anda-Montañez*
Affiliation:
Centro de Investigaciones Biológicas de Noroeste, S.C. (CIBNOR), Instituto Politécnico Nacional # 195, Playa Palo de Santa Rita, La Paz, B.C.S., C.P. 23096, México
Armando Trasviña-Castro
Affiliation:
Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Unidad La Paz, 334 Fraccionamiento Bella Vista, La Paz, B.C.S., C.P. 23050, México
Fausto Valenzuela-Quiñonez
Affiliation:
CONACYT-Centro de Investigaciones Biológicas de Noroeste, S.C. (CIBNOR), Instituto Politécnico Nacional # 195, Playa Palo de Santa Rita, La Paz, B.C.S., C.P. 23096, México
James T. Ketchum
Affiliation:
Centro de Investigaciones Biológicas de Noroeste, S.C. (CIBNOR), Instituto Politécnico Nacional # 195, Playa Palo de Santa Rita, La Paz, B.C.S., C.P. 23096, México Pelagios Kakunjá A.C. 2016. Cuauhtémoc 155, entre Francisco I. Madero y Belisario Domínguez, Colonia Pueblo Nuevo, La Paz Baja California Sur, México
Arturo Muhlia-Melo
Affiliation:
Centro de Investigaciones Biológicas de Noroeste, S.C. (CIBNOR), Instituto Politécnico Nacional # 195, Playa Palo de Santa Rita, La Paz, B.C.S., C.P. 23096, México
*
Author for correspondence: Juan Antonio De-Anda-Montañez, E-mail: jdeanda@cibnor.mx

Abstract

The description of the movements and habitat preference of marine fishes is essential to understand their biology and in the evaluation of commercially exploited species and the conservation of endangered ones. In this regard, little is known about the movements of the totoaba (Totoaba macdonaldi), despite its being listed as critically endangered and having been a relevant fishery resource in the past century in Mexico. Totoaba is a fish species endemic to the Gulf of California characterized by late maturation, prolonged life and annual reproduction. Totoaba has maintained its known historical distribution range, although its movements and habitat occupancy in the water column have remained poorly understood. The present study describes, for the first time and at a daily fine scale, the vertical movements and habitat preferences of the totoaba in the Upper Gulf of California. Pop-up satellite archival tags (PSATs) were used to record depth and temperature at 4-minute intervals. Ten individuals were caught and tagged in May 2016 in the Upper Gulf of California and Colorado River Delta Biosphere Reserve. All PSATs were either prematurely released or lost. Data derived from two recovered tags that saved data for 43 and 75 tracking days, respectively, were analysed. The results showed that tagged fishes moved southward to the vicinity of Angel de la Guarda Island; these are consistent with spatial displacement patterns reported in the literature, with a linear displacement of 223 km from deployment to pop-up sites. Fish spent 47% of the time within a depth range of 25–35 m. Depth increased to 70 m for one fish in early summer (late June). The preferred temperature of fishes ranged between 21–23°C. A generalized linear model revealed that vertical movement was influenced by temperature. The vertical displacement of the totoaba shows a diurnal variation that may be associated with the distribution of its prey. Further work is needed to test this hypothesis with a larger number of organisms.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Abascal, FJ, Mejuto, J, Quintans, M and Ramos-Cartelle, A (2010) Horizontal and vertical movements of swordfish in the Southeast Pacific. ICES Journal of Marine Science 67, 466474.CrossRefGoogle Scholar
Afonso, P, McGinty, N, Graca, G, Fontes, J, Inácio, M, Totland, A and Menezes, G (2014) Vertical migrations of a deep-sea fish and its prey. PLoS ONE 9, 110.CrossRefGoogle ScholarPubMed
Alvarez, LG, Suárez-Vidal, F, Mendoza-Borunda, R and González-Escobar, M (2009) Bathymetry and active geological structures in the Upper Gulf of California. Boletin de La Sociedad Geologica Mexicana 61, 129141.CrossRefGoogle Scholar
Alvarez-Borrego, S (2010) Physical, chemical and biological oceanography of the Gulf of California. In Brusca, RC (ed.), The Gulf of California Biodiversity and Conservation, 1st Edn. Tucson, AZ: The University of Arizona Press and The Arizona-Sonora Desert Museum, pp. 2448.Google Scholar
Arvizu, J and Chávez, H (1972) Sinopsis sobre la biología de la totoaba, Cynoscion macdonaldi Gilbert, 1890. FAO Fisheries Synopsis 108, 26.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 1, 148.Google Scholar
Bobadilla, M, Alvarez-Borrego, S, Avila-Foucat, S, Lara-Valencia, F and Espejel, I (2011) Evolution of environmental policy instruments implemented for the protection of totoaba and the vaquita porpoise in the Upper Gulf of California. Environmental Science and Policy 14, 9981007.CrossRefGoogle Scholar
Bone, Q and Moore, RH (2008) Behavior and cognition. In Biology of Fishes, 3rd Edn. New York, NY: Taylor & Francis Group, pp. 409433.CrossRefGoogle Scholar
Broell, F, Taylor, AD, Litvak, MK, Bezanson, A and Taggart, CT (2016) Post-tagging behaviour and habitat use in shortnose sturgeon measured with high-frequency accelerometer and PSATs. Animal Biotelemetry 4, 113.CrossRefGoogle Scholar
Brusca, RC, Álvarez-Borrego, S, Hastings, PA and Findley, LT (2017) Colorado river flow and biological productivity in the Northern Gulf of California, Mexico. Earth-Science Reviews 164, 130.CrossRefGoogle Scholar
Chao, LN (1978) Sciaenidae. In Fischer, W (ed.), FAO Species Identification Sheets for Fishery Purposes. Rome: FAO, pp. 15831603.Google Scholar
Chiang, WC, Musyl, MK, Sun, CL, Chen, SY, Chen, WY, Liu, DC, Su, WC, Yeh, SZ, Fu, SC and Huang, TL (2011) Vertical and horizontal movements of sailfish (Istiophorus platypterus) near Taiwan determined using pop-up satellite tags. Journal of Experimental Marine Biology and Ecology 397, 129135.CrossRefGoogle Scholar
Cisneros-Mata, MA, Montemayor-López, G and Román-Rodríguez, MJ (1995) Life history and conservation of Totoaba macdonaldi. Conservation Biology 9, 806814.CrossRefGoogle Scholar
De Anda-Montañez, JA, García-De León, FJ, Zenteno-Savin, T, Balart-Paez, EF, Méndez-Rodríguez, LC, Bocanegra-Castillo, MJ, MArtínez-Aguilar, S, Campos-Dávila, L, Román-Rodríguez, MJ, Valenzuela-Quiñonez, F, Rodríguez-Jaramillo, ME, Meza-Chávez, ME, Ramírez-Rosas, JJ, Saldaña-Hernández, IJ, Olguín-Monroy, NO and Martínez-Delgado, ME (2013) Estado de salud y estatus de conservación de la(s) población (es) de totoaba (Totoaba macdonaldi) en el Golfo de California: una especie en peligro de extinción. Informe Final, SNIB-CONABIO. Proyecto No. HK050. https://doi.org/10.1017/CBO9781107415324.004.CrossRefGoogle Scholar
Flanagan, CA and Hendrickson, JR (1976) Observation on the commercial fishery and reproductive biology of the totoaba, Cynoscion macdonaldi, in the Northern Gulf of California. Fishery Bulletin 74, 531544.Google Scholar
Goding, G (1972) Analysis of Tides. Toronto: University of Toronto Press.Google Scholar
Hammann, MG, Baumgartner, TR and Badan-Dangon, A (1988) Coupling of the pacific sardine (Sardinops sagax caeruleus) life cycle with the Gulf of California pelagic environment. CalCOFI Report XXIX, 102109.Google Scholar
Hernández-Aguilar, SB, Zenteno-Savin, T, De-Anda-Montañez, JA and Méndez-Rodríguez, LC (2018) Temporal variation in oxidative stress indicators in liver of totoaba (Totoaba macdonaldi) Perciformes: Sciaenidae. Journal of the Marine Biological Association of the United Kingdom 98, 833844. https://doi.org/10.1017/S0025315416001909.CrossRefGoogle Scholar
Hobson, VJ, Righton, D, Metcalfe, JD and Hays, GC (2009) Link between vertical and horizontal movement patterns of cod in the North Sea. Aquatic Biology 5, 133142.CrossRefGoogle Scholar
Hoolihan, JP, Luo, J, Abascal, FJ, Campana, SE, De Metrio, G, Dewar, H, Domeier, ML, Howey, LA, Lutcavage, ME, Musyl, MK, Neilson, JD, Orbesen, ES, Prince, ED and Rooker, JR (2011) Evaluating post-release behaviour modification in large pelagic fish deployed with pop-up satellite archival tags. ICES Journal of Marine Science 68, 880889.CrossRefGoogle Scholar
IUCN (2019) The IUCN Red List of Threatened Species. Version 2019-3. https://www.iucnredlist.org/.Google Scholar
Klimley, AP, Castillo Geniz, J and Cabrera Mancilla, I (1993) Descripción de los movimientos horizontales y verticales del tiburón martillo Sphyrna lewini, del sur del Golfo de California, México. Ciencias Marinas 19, 95115.CrossRefGoogle Scholar
Lavin, MF and Marinone, SG (2003) An overview of the physical oceanography of Gulf of California. In Velasco-Fuentes, O, Sheinbaum, J and Ochoa, J (eds), Nonlinear Processes in Geophysical Fluid Dynamics. Dordrecht: Kluwer, pp. 173204.CrossRefGoogle Scholar
Lavin, MF, Godínez, MV and Alvarez, LG (1998) Inverse-estuarine features of the Upper Gulf of California. Estiuarine, Coastal and Shelf Science 47, 769795.CrossRefGoogle Scholar
Lluch-Belda, D, Magallon, FJ and Schwartzlose, RA (1986) Large fluctuations in the sardine fishery in the Gulf of California: possible causes. CalCOFI Report XXVII, 136140.Google Scholar
Lluch-Cota, SE, Aragón-Noriega, EA, Arreguín-Sánchez, F, Aurioles-Gamboa, D, Jesús Bautista-Romero, J, Brusca, RC, Cervantes-Duarte, R, Cortés-Altamirano, R, Del-Monte-Luna, P, Esquivel-Herrera, A, Fernández, G, Hendrickx, ME, Hernández-Vázquez, S, Herrera-Cervantes, H, Kahru, M, Lavín, M, Lluch-Belda, D, Lluch-Cota, DB, López-Martínez, J, Marinone, SG, Nevárez-Martínez, MO, Ortega-García, S, Palacios-Castro, E, Parés-Sierra, A, Ponce-Díaz, G, Ramírez-Rodríguez, M, Salinas-Zavala, CA, Schwartzlose, RA and Sierra-Beltrán, AP (2007) The Gulf of California: review of ecosystem status and sustainability challenges. Progress in Oceanography 73, 126.CrossRefGoogle Scholar
Marinone, SG and Lavín, MF (2003) Residual flow and mixing in the large islands region of the central Gulf of California. In Velasco Fuentes, O, Sheinbaum, J and Ochoa, J (eds), Nonlinear Processes in Geophysical Fluid Dynamics. Dordrecht: Kluwer, pp. 213236.CrossRefGoogle Scholar
Márquez-Farías, JF and Rosales-Juárez, FJ (2013) Intrinsic rebound potential of the endangered (Totoaba macdonaldi) population, endemic to the Gulf of California, México. Fisheries Research 147, 150153.CrossRefGoogle Scholar
Musyl, MK, Brill, RW, Boggs, CH, Curran, DS, Kazama, TK and Seki, MP (2003) Vertical movements of bigeye tuna (Thunnus obesus) associated with islands, buoys, and seamounts near the main Hawaiian Islands from archival tagging data. Fisheries Oceanography 12, 152169.CrossRefGoogle Scholar
Næsje, TF, Cowley, PD, Diserud, OH, Childs, A-R, Kerwath, SE and Thorstad, EB (2012) Riding the tide: estuarine movements of a sciaenid fish, Argyrosomus japonicus. Marine Ecology Progress Series 460, 221232.CrossRefGoogle Scholar
Peklova, I, Hussey, NE, Hedges, KJ, Treble, MA and Fisk, AT (2012) Depth and temperature preferences of the deepwater flatfish Greenland halibut Reinhardtius hippoglossoides in an Arctic marine ecosystem. Marine Ecology Progress Series 467, 193205.CrossRefGoogle Scholar
Peklova, I, Hussey, NE, Hedges, KJ, Treble, MA and Fisk, AT (2014) Movement, depth and temperature preferences of an important bycatch species, Arctic skate Amblyraja hyperborea, in Cumberland Sound, Canadian Arctic. Endangered Species Research 23, 229240.CrossRefGoogle Scholar
Ramcharitar, J, Gannon, DP and Popper, AN (2006) Bioacoustics of fishes of the family Sciaenidae (croakers and drums). Transactions of the American Fisheries Society 135, 14091431.CrossRefGoogle Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Román-Rodríguez, MJ (1990) Análisis de los contenidos estomacales de la totoaba Totoaba macdonaldi (Gilbert 1891) (Pisces: Scianidae) durante la epoca reproductiva en la parte norte del Alto Golfo de California. Ecologica 1, 19.Google Scholar
Rubio-Rodríguez, U, Villalobos, H and Nevarez-Martinez, MO (2018) Acoustic observations of the vertical distribution and latitudinal range of small pelagic fish schools in the Midriff Islands Region, Gulf of California, México. Latin American Journal of Aquatic Research 46, 9891000.CrossRefGoogle Scholar
Seitz, AC, Wilson, D, Norcross, BL and Nielsen, JL (2003) Pop-up archival transmitting (PAT) tags: a method to investigate the migration and behavior of Pacific halibut Hippoglossus stenolepis in the Gulf of Alaska. Alaska Fishery Research Bulletin 10, 124136.Google Scholar
SEMARNAT (2002) Normal Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres- Categorías de riesgo y especificaciones para su inclusion, exclusión o cambio- Lista de especies. en riesgo. Diario Oficial de la F.Google Scholar
Sims, DW, Southall, EJ, Humphries, NE, Hays, GC, Bradshaw, CJA, Pitchford, JW, James, A, Ahmed, MZ, Brierley, AS, Hindell, MA, Morritt, D, Musyl, MK, Righton, D, Shepard, ELC, Wearmouth, VJ, Wilson, RP, Witt, MJ and Metcalfe, JD (2008) Scaling laws of marine predator search behaviour. Nature 451, 10981102.CrossRefGoogle ScholarPubMed
Soto-Mardones, L, Marinone, SG and Parés-Sierra, A (1999) Time and spatial variability of sea surface temperature in the Gulf of California. Ciencias Marinas 25, 130.CrossRefGoogle Scholar
Thorstad, EB, Rikardsen, AH, Alp, A and Okland, F (2013) The use of electronic tags in fish research – an overview of fish telemetry methods. Turkish Journal of Fisheries and Aquatic Sciences 13, 881896.Google Scholar
Thygesen, HU, Sommer, L, Evans, K and Patterson, TA (2016) Dynamic optimal foraging theory explains vertical migrations of bigeye tuna. Ecology 97, 18521861.CrossRefGoogle ScholarPubMed
True, CD, Loera, AS and Castro, NC (1997) Technical notes: acquisition of broodstock of Totoaba macdonaldi: field handling, decompression, and prophylaxis of an endangered species. The Progressive Fish-Culturist 59, 246248.2.3.CO;2>CrossRefGoogle Scholar
Turnure, JT, Able, KW and Grothues, TM (2015) Patterns of intra-estuarine movement of adult weakfish (Cynoscion regalis): evidence of site affinity at seasonal and diel scales. Fishery Bulletin 113, 167179.CrossRefGoogle Scholar
Valenzuela-Quiñonez, F, Arreguín-Sánchez, F, Salas-Márquez, S, García-De León, FJ, Garza, JC, Román-Rodríguez, MJ and De-Anda-Montañez, JA (2015) Critically endangered totoaba Totoaba macdonaldi: signs of recovery and potential threats after a population collapse. Endangered Species Research 29, 111.CrossRefGoogle Scholar
Williams, A, Allain, V, Nicol, SJ, Evans, KJ, Hoyle, SD, Dupoux, C, Vourey, E and Dubosc, J (2015) Vertical behavior and diet of albacore tuna (Thunnus alalunga) vary with latitude in the South Pacific Ocean. Deep-Sea Research Part II: Topical Studies in Oceanography 113, 154169. https://doi.org/10.1016/j.dsr2.2014.03.010.CrossRefGoogle Scholar
Zuur, AF, Ieno, EN, Saveliev, AA, Walker, NJ and Smith, GM (2009) Meet the exponential family. In Mixed Effects Models and Extensions in Ecology with R. New York, NY: Springer, pp. 193206.CrossRefGoogle Scholar