Foraging patterns of four sympatric species of silversides (Atheriniformes: Atherinopsidae) in Lago de Pátzcuaro, Central Mexico
DOI:
https://doi.org/10.22458/urj.v6i1.312Abstract
ABSTRACT: Since Barbour proposed sympatric speciation to explain evolution of silversides in the Lerma-Santiago basin, relatively little subsequent study has been done. We assessed foraging patterns of four sympatric silversides species (Chirostoma estor, Chirostoma grandocule, Chirostoma attenuatum and Chirostoma patzcuaro) in Lago de Pátzcuaro to understand resource partitioning and their sympatric coexistence. We assessed the abundance of invertebrate prey in three feeding habitats and measured physical and chemical habitat parameters at two study sites. Fish were collected during the wet (September 1987) and dry (March 1988) seasons; a total of 242 gut contents were analyzed. We evaluated the trophic guild of each species using the index of relative importance (IRI), prey selectivity with the Ivlev Electivity Index (E), dietary diversity using Shannon and Wiener diversity index (H’), and diet overlap using Morisita index. All silverside species were determined to be predacious carnivores that feed mainly on nekton and periphyton. Dietary diversity and prey selectivity patterns were similar among species and diet overlap was >70%. Our data do not support the proposition that coexistence of these four fish species is maintained by dietary specialization. We hypothesize that sympatric coexistence of atherinopsids in Lago de Pátzcuaro is explained by food resource availability and ontogenetic variation in their diets. This study highlights the importance of analyzing ecological patterns and mechanisms as basic elements for designing conservation strategies of species flocks, especially under habitat loss and introduction of exotic species. Conservation efforts are urgent to preserve the rare evolutionary process of sympatric speciation (habitat segregation) that is occurring in other lakes in central Mexico, and probably already lost in the Lago de Pátzcuaro, as a result of poor management and inadequate conservation strategies.
KEY WORDS: Atherinopsidae, feeding interactions, species flocks, evolutionary process, conservation.
References
Alvarez del Villar, J. (1972). Ictiología Michoacana V. Origen y distribución de la ictiofauna dulceacuícola de Michoacán. Anales de la Escuela Nacional de Ciencias Biológicas México, 19, 155‒161.
Barbour, C. D. (1973a). A biogeographical history of Chirostoma (Pisces: Atherinidae): A species flock from the Mexican Plateau. Copeia, 3, 533‒566. Retrieved from http://www.jstor.org/stable/1443118
Barbour, C. D. (1973b). The systematics and evolution of the genus Chirostoma Swainson (Pisces, Atherinidae). Tulane Studies in Zoology and Botany, 18, 97‒143.
Barluenga, M., & Meyer, A. (2004). The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Molecular Ecology, 13, 2061‒2076. doi: 10.1111/j.1365-294X.2004.02211.x
Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719‒723. doi:10.1038/nature04325
Barriga-Sosa, I., Ibañez-Aguirre, A. L., & Arredondo-Figueroa, J. L. (2002). Morphological and genetic variation in seven species of the endangered Chirostoma “humboldtianum species group” (Atheriniformes: Atherinopsidae). Revista de Biología Tropical, 50, 199–216. Retrieved from http://biologiatropical.ucr.ac.cr/attachments/volumes/vol50-1/25-Barriga_Morpholog.pdf
Barriga-Sosa, I., Eguiarte, L. E., & Arredondo-Figueroa, J. L. (2004). Low but significant subdivision among populations of Chirostoma grandocule from Lake Patzcuaro, Mexico. Biotropica, 36, 85–98. doi: 10.1111/j.1744-7429.2004.tb00299.x
Berlanga-Robles, C. A., Madrid-Vera, J., & Ruiz-Luna, A. (2002). Fish abundance and trophic structure from the commercial catch in Lake Patzcuaro, Mexico. Hydrobiologia, 467, 117–122. doi: 10.1023/A:1014965504486
Bernal-Brooks, F. W., Gómez, T. R., & Alcocer, J. (2002). Lake Patzcuaro (Mexico): a controversy about the ecosystem water regimen approached by field references, climatic variables, and GIS. Hydrobiologia, 467, 187–197. doi: 10.1023/A:1014919032228
Berry, J., Lee, E., Walton, K., Wilson, A., & Bernal-Brooks, F. (2011). Microcystin production by a persistent cyanobacterial bloom in Lago de Pátzcuaro (Michoacán, México), and apparent bioaccumulation of the toxin in small commercial catches of fish. Environmental Toxicology & Chemistry, 30, 1621–1628. doi: 10.1002/etc.548
Bloom, D. D., Piller, K. R., Lyons J., Mercado-Silva, N., & Medina-Nava, M. (2009). Systematics and biogeography of the silverside tribe Menidiini (Teleostomi: Atherinopsidae) based on the mitochondrial ND2 gene. Copeia, 2, 408–417. doi: 10.1643/CI-07-151
Bouyoucos, G. J. (1936). Directions for making mechanical analysis of soils by the hydrometer method. Soil Science, 42, 225‒230.
Chacón-Torres, A., Ross, L. G., & Beveridge, M. C. (1989). Lake Patzcuaro, Mexico: results of a new morphometric study and its implications for productivity assessments. Hydrobiologia ,184, 125‒132. doi: 10.1007/BF00014307
Chacón-Torres, A. (1993). Lake Patzcuaro, Mexico: Watershed and water quality deterioration in a tropical high-altitude Latin American lake. Lake Reservoir Management, 8, 37–47. doi: 10.1080/07438149309354457
Chacón-Torres, A., & Rosas-Monge, C. (1998). Water quality characteristics of a high altitude oligotrophic Mexican lake. Aquatic Ecosystem Health & Management, 1, 237‒243. doi: 10.1080/14634989808656920
Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Science, 54, 726‒738. doi: 10.1139/f96-316
Davies, S. J., Metcalfe, S. E., Bernal-Brooks, F., Chacón-Torres, A., Farmer, J. G., MacKenzie, A. B., & Newton, A. J. (2005). Lake sediments record sensitivity of two hydrologically closed upland lakes in Mexico to human impact. AMBIO: A Journal of the Human Environment, 34, 470‒475. doi: http://dx.doi.org/10.1579/0044-7447-34.6.470
Dean, W. E. (1974). Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. Journal of Sedimentary Petrology, 44, 242–248. doi: 10.1306/74D729D2-2B21-11D7-8648000102C1865D
De Buen, F. (1941). El Lago de Pátzcuaro. Revista Geográfica del Instituto Panamericano e Historia, 1, 1‒44.
De Buen, F. (1944a). Limnobiología de Pátzcuaro. Anales del Instituto de Biología de la Universidad Nacional Autónoma de México, 15, 69‒78.
De Buen, F. (1944b). Los lagos Michoacanos II: Pátzcuaro. Revista de la Sociedad Mexicana de Historia Natural, 5, 99‒125.
De Buen, F. (1945). Investigaciones sobre ictiología mexicana. Atherinidae en aguas continentales de México. Anales del Instituto de Biología de la Universidad Nacional Autónoma de México, 16, 475‒532.
Echelle, A. A., & Echelle, A. F. (1984). Evolutionary genetics of a ‘‘species flock’’: Atherinid fishes on the Mesa Central of Mexico. In A.A. Echelle & I. Kornfield (Ed.), Evolution of Fish Species Flocks (pp. 93–110). USA: University of Maine Press.
Echelle, A. A., & Kornfield, I. (1984). Evolution of fish species flocks. USA: University of Maine Press.
Edmonson, W. T. (Ed.). (1959). Fresh-Water Biology. New York: John Wiley & Sons.
García de León, F. J. (1985). Relaciones alimenticias y reproductivas entre Chirostoma estor y Micropterus salmoides en el Lago de Pátzcuaro, Michoacán. Memorias de VIII Congreso Nacional de Zoología. Sociedad Mexicana de Zoología , 1, 41‒59.
González, M. L. (1977). La Muerte de un Lago. Técnica Pesquera, 116, 22‒28.
Greenwood, P. H. (1984). What is a species flock? In A. A. Echelle & I. Kornfield (Ed.). Evolution of Fish Species Flocks (pp. 13‒19). USA: University of Maine Press.
Herder, F., Nolte, A. W., Pfaender, J., Schwarzer, J., Hadiaty, R. K., & Schliewen, U. K. (2006). Adaptive radiation and hybridization in Wallace’s Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi. Proceedings of the Royal Society, 273, 2209–2217. doi:10.1098/rspb.2006.3558
Hutchinson, G. E. (1965). The niche: an abstractly inhabited hypervolume. In G. E. Hutchinson (Ed.). The ecological theater and the evolutionary play (pp. 26‒78). New Haven, C.T.: Yale University Press.
Hyslop, E. J. (1980). Stomach contents analysis a review of methods and their application. Journal of Fish Biology,17, 411‒429. doi: 10.1111/j.1095-8649.1980.tb02775.x
Ivlev, V.S. (1961). Experimental Ecology of the Feeding of Fishes. New Haven, C.T.: Yale University Press.
Jiménez-Badillo, M. L., & Gracia, A. G. (1995). Evaluación de la pesquería multiespecífica de charales (Chirostoma spp., Pisces, Atherinidae) del Lago de Pátzcuaro, Michoacán, México. Anales del Instituto de Biología de la Universidad Nacional Autónoma de México, Serie Zoología, 66, 205‒231. Retrieved from http://revistas.unam.mx/index.php/zoo/article/view/7136
Ledesma-Ayala, P. C., & García de León, F. J. (1991). Analysis of primary ontogenetic phases and recognition of the hybrid obtained by artificial fertilization between Chirostoma attenuatum and Chirostoma patzcuaro (Pisces: Atherinidae) from Lake Patzcuaro, Michoacán, Mexico. Abstracts from American Fisheries Society, 1, 8‒12.
MacArthur, R., & Levins, R. (1964). Competition, habitat selection and character displacement in a patchy environment. Proceedings of the National Academy of Sciences, 51, 1207‒1210. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC300237/
Mar-Silva, V. (2011). Variación espacio-temporal de la comunidad de peces en el lago de Pátzcuaro, Michoacán, México. Thesis. Facultad de Biología. Universidad Michoacana de San Nicolás de Hidalgo. Morelia, Michoacán, Mexico.
McCrary, J., van der Berghe, E., McKaye, K. R., & López Pérez, L. (2001). El cultivo de tilapias: una amenaza a las especies ícticas nativas en Nicaragua. Encuentro, 58, 9–19.
Merrit, R. W., & Cummins, K.W. (1978). An Introduction to the Aquatic Insects. Dubuque, IA, USA: Kendall Hunt Publishing.
Miller, R. R., Minckley, W. L. & Norris, S. M. (2005). Freshwater fishes of Mexico. Chicago, USA: The University of Chicago Press.
Moncayo-Estrada, R., Owen, T. L., & Escalera-Gallardo, C. (2010). Trophic partitioning of sympatric zooplanktivorous silverside in a tropical shallow lake: fish morphometry and diet composition. Copeia, 3,431‒436. doi: 10.1643/CE-08-024
Moncayo-Estrada, R., Owen, T.L. & Escalera-Gallardo, C. (2011). Trophic interactions among sympatric zooplanktivorous fish species in volume change conditions in a large, shallow, tropical lake. Neotropical Ichthyology 9, 169‒176. doi: http://dx.doi.org/10.1590/S1679-62252011005000003
Morelos-López, M. M., & García de León, F.J. (1987). Aspectos reproductivos del charal prieto, Chirostoma attenuatum, Meek 1902 (Pisces: Atherinidae) en el Lago de Pátzcuaro, Michoacán, Méx. Memorias del IX Congreso Nacional de Zoología, Sociedad Mexicana de Zoología, 1, 77-84.
Oseguera-Figueroa, L., & García de León, F.J. (1991). Morphology of larvae and juveniles of Chirostoma grandocule Steindachner (1896) and its hybrids with Chirostoma attenuatum Meek (1902) from Lake Patzcuaro, Michoacán, Mexico. Abstracts from American Fisheries Society, 1, 12‒16.
Page, L. M., Espinosa-Pérez, H., Findley, L. T., Gilbert, C. R., Lea, R. N., Mandrak, N. E., Mayden, R. L., & Nelson, J. S. (2013). Common and scientific names of fishes from the United States, Canada, and Mexico. Bethesda, M.D.: American Fisheries Society.
Pennak, R. W. (1978). Freshwater Invertebrates of the United States. New York, USA: John Wiley & Sons.
Pinkas, L., Oliphant, M., & Iverson, I. (1971). Food habits of albacore, bluefin tuna, and bonito in California waters. California Department of Fish and Game, 152, 1‒105.
Rauda-Ortega, J., & García de León, F. J. (1987). Análisis trófico de Chirostoma patzcuaro Meek 1902 (Pisces: Atherinidae) del Lago de Pátzcuaro, Mich., México.Memorias del IX Congreso Nacional de Zoologia, Sociedad Mexicana de Zoología, 1, 85‒94.
Rosas, I., Mazari, M., Saavedra, J., & Báez, P. (1985). Benthic organisms as indicators of water quality in Lake Pátzcuaro, México. Water, Air, and SoilPollution, 25, 401–414. doi: 10.1007/BF00283792
Rosas, M. M. (1976). Datos biológicos de la ictiofauna del Lago de Pátzcuaro, con especial énfasis en la alimentación de sus especies. Memorias del Simposio de Pesquerías de Aguas Continentales. Instituto Nacional de la Pesca de México,11, 299‒366.
Rosas, C. V. (1983). El pescado blanco de Pátzcuaro (Chirostoma estor Jordan), presente pasado y futuro de una especie en peligro de extinción. Ocelote, 1, 12‒15.
Ross, L. G., Martínez-Palacios, C., Aguilar-Valdez, M., Beveridge, M., & Chavez-Sánchez, M. (2006). Determination of feeding mode in fishes: the importance of using structural and functional feeding studies in conjunction with gut analysis in a selective zooplanktivore Chirostoma estor estor Jordan 1880. Journal of Fish Biology, 68, 1782–1794. doi: 10.1111/j.1095-8649.2006.01061.x
Sánchez-Hernández, J., Vieira-Lanero, R., Servia, M. J., & Cobo, F. (2011). Feeding habits of four sympatric fish species in the IberianPeninsula: keys to understanding coexistence using prey traits. Hydrobiologia, 667, 119–132. doi: 10.1007/s10750-011-0643-2
Saiki, M. (1976). Mean bulk index. Method of fish food analysis. The Progressive Fish Culturist, 38, 55‒56. doi: 10.1577/1548-8659(1976)38[55:MBIMOF]2.0.CO;2
Seehausen, O., van Alphen, J. J. M., & Witte, F. (1997). Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808‒1811. doi: 10.1126/science.277.5333.1808
Smith, E. P., & Zaret, T. M. (1982). Bias in estimating niche overlap. Ecology, 63, 1248‒253. Retrieved from http://www.jstor.org/stable/1938851
Solórzano, P. A. (1955). La pesca en el Lago de Pátzcuaro, Michoacán y su importancia económica regional. México: Secretaría de Marina, Dirección General de Pesca.
Solórzano, P. A. (1961). Contribución al conocimiento de la biología del charal prieto del Lago de Patzcuaro, Chirostoma bartoni Jordan y Everman, 1986. México: Secretaría de Industria y Comercio. Dirección General de Pesca.
Solórzano, P. A. (1963). Algunos aspectos biológicos del pescado blanco del Lago de Pátzcuaro, Mich. México: Secretaría de Industria y Comercio. Dirección General de Pesca.
Soria-Barreto, M., & Paulo-Maya, J. (2005). Morfometría comparada del aparato mandibular en especies de Chirostoma (Atheriniformes: Atherinopsidae) del Lago de Pátzcuaro, Michoacán, Mexico. Hidrobiológica, 15, 161‒168. Retrieved from http://investigacion.izt.uam.mx/rehb/publicaciones/index.htm
Usinger, L.R. (1956). Aquatic Insects of California. Berkeley, CA: University of California Press.
Vital-Rodríguez, B. (2011). Hábitos alimentarios del género Chirostoma del lago de Pátzcuaro, Michoacán, México. Master’s Thesis. Universidad Michoacana de San Nicolás de Hidalgo. Morelia, Michoacán, Mexico.
Ward, H. P., & Whipple, G. (1945). Fresh-Water Biology. New York, USA: John Wiley & Sons.
Williams, E. E. (1972). The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. Evolutionary Biology, 6, 47‒89. doi: 10.1007/978-1-4684-9063-3_3
Wetzel, R. G., & Likens, G. E. (2000). Limnological Analyses. New York, USA: Springer-Verlag.
Yañez, A. A., Curiel, G., &Yañez, V. L. (1976). Prospección biológica y ecológica del bagre marino Galeichthys caerulescens (Gunther) en el sistema lagunar costero de Guerrero, México (Pisces: Ariidae). Anales del Centro de Ciencias del Mar y Limnología, Universidad NacionalAutónoma de México, 3, 125‒180.
Zar, J. H. (1999). Biostatistical Analysis. Upper Saddle River, NJ, USA: Prentice Hall.
Downloads
How to Cite
Issue
Section
License
Note: This abstract contains an incorrect copyright due to technical issues. Authors who publish with this journal agree to the following terms: Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal
All journal contents are freely available through a CC BY 4.0 license.
CC BY 4.0 is a Creative Commons: you can copy, modify, distribute, and perform, even for commercial reasons, without asking permission, if you give appropriate credit.
Contents can be reproduced if the source and copyright are acknowledged according to the Open Access license CC BY 4.0. Self-storage in preprint servers and repositories is allowed for all versions. We encourage authors to publish raw data and data logs in public repositories and to include the links with all drafts so that reviewers and readers can consult them at any time.
The journal is financed by public funds via Universidad Estatal a Distancia and editorial independence and ethical compliance are guaranteed by the Board of Editors, UNED. We do not publish paid ads or receive funds from companies.