Accessibility / Report Error

Comparative analysis of diet composition and its relation to morphological characteristics in juvenile fish of three lutjanid species in a Mexican Pacific coastal lagoon

ABSTRACT

The main goal of this research was to investigate the differences in diet composition among three species of the genus Lutjanus inhabiting a coastal lagoon as juveniles. The working hypothesis was that these species feed on a common base of food resources and therefore, some niche overlap is present in terms of general diet composition. However, changes in the trophic niche with size and differences in some morphological traits among species explain observed differences in diet. Fish were collected during 42 sampling trips conducted regularly from February 2011 to January 2012 using several types of fishing gear. Total number of analyzed stomachs was 288 for Lutjanus argentiventris from 2.3 to 19.9 cm total length (TL); 178 for Lutjanus colorado ranging from 2.4 to 30.1 cm TL; and 183 for Lutjanus novemfasciatus with 1.2 to 20.0 cm TL. Results indicate that juveniles of all three lutjanid species share a general diet based on decapods and fishes. However, L. novemfasciatus has a more piscivorous habit, which can be explained by a more slender body shape and larger teeth, characteristics, which increase fish catching performance. Larger fish of all three species eat larger prey, which is consistent with the optimum foraging theory.

Keywords:
Estuarine habitat; Feeding; Lutjanidae; Ontogenic changes; Trophic morphology

RESUMEN

Se investigaron las diferencias en la composición de la dieta de juveniles de tres especies del género Lutjanus que habitan una laguna costera. La hipótesis de trabajo fue que estas especies se alimentan de una base común de recursos alimentarios y, por tanto, alguna superposición del nicho está presente en términos de la composición general de la dieta. Sin embargo, los cambios en el nicho trófico con la talla y diferencias entre especies en algunas características morfológicas, explican las diferencias observadas en la dieta. Los peces fueron colectados durante 42 viajes de muestreo realizados de febrero del 2011 a enero del 2012 usando varios tipos de artes de pesca. Se analizaron 288 estómagos de Lutjanus argentiventris de 2.3 a 19.9 cm de largo total (LT); 178 de Lutjanus colorado entre 2.4 y 30.1 cm LT; y 183 de Lutjanus novemfasciatus de 1.2 a 20.0 cm LT. Los resultados indican que los juveniles de las tres especies de lutjánidos comparten una dieta general basada en decápodos y peces. Sin embargo, Lutjanus novemfasciatus tiene un hábito piscívoro mayor, el cual puede ser explicado por la forma del cuerpo más delgada y dientes mayores, características que incrementan la eficiencia para capturar peces. Los peces mayores de las tres especies comieron presas mayores y este cambio ontogénico es consistente con la teoría del forrajeo óptimo.

Palabras clave:
Alimentación; Cambios ontogénicos; Hábitat estuarino; Lutjanidae; Morfología trófica

Introduction

Species of the family Lutjanidae (snappers) are important components of artisanal fisheries in tropical regions. These fish are popular to eat, and are frequently sold in markets at an elevated price (Pimentel, Joyeux, 2010Pimentel CR, Joyeux JC. Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. J Fish Biol [serial on the Internet]. 2010; 76(10): 2299-317. Available from: http://dx.doi.org/10.1111/j.1095-8649.2010.02586.x
http://dx.doi.org/10.1111/j.1095-8649.20...
). More important from an ecological point of view, several species of lutjanids are ontogenetic habitat shifters (sensuAdams et al., 2006Adams AJ, Dahlgren CP, Kellison GT, Kendall MS, Layman CA, Ley JA, Nagelkerken I, Serafy JE. Nursery function of tropical back-reef systems. Mar Ecol Prog Ser [serial on the Internet]. 2006; 318:287-301. Available from: http://www.jstor.org/stable/24870766
http://www.jstor.org/stable/24870766...
) and use coastal lagoons as nursery areas (Cocheret de la Moriniere et al., 2003Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, van der Velde G. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar Coast Shelf Sci [serial on the Internet]. 2003; 57(5-6):1079-89. Available from: https://doi.org/10.1016/S0272-7714(03)00011-8
https://doi.org/10.1016/S0272-7714(03)00...
; Aburto-Oropeza et al., 2009Aburto-Oropeza O, Dominguez-Guerrero I, Cota-Nieto J, Plomozo-Lugo T. Recruitment and ontogenetic habitat shifts of the yellow snapper (Lutjanus argentiventris) in the Gulf of California. Mar Biol [serial on the Internet]. 2009; 156(12):2461-72. Available from: http://dx.doi.org/10.1007/s00227-009-1271-5
http://dx.doi.org/10.1007/s00227-009-127...
). The yellow snapper Lutjanus argentiventris (Peters, 1869), the Pacific dog snapper L. novemfasciatus Gill, 1862 and with less frequency the colorado snapper L. colorado Jordan & Gilbert, 1882, have been repeatedly reported as characteristic species of fish assemblages in Mexican Pacific coastal lagoons and estuaries (e.g.Yañez-Arancibia, 1978Yañez-Arancibia A. Taxonomía, ecología y estructura de las comunidades de peces en las lagunas costeras con bocas efímeras del Pacífico de Mexico. Distrito Federal: Universidad Nacional Autónoma de Mexico; 1978. (Publicaciones especiales, Centro de Ciencias del Mar y Limnologia; 2).; Flores-Verdugo et al., 1990Flores-Verdugo F, González-Farías F, Ramírez-Flores O, Amezcua-Linares F, Yáñez-Arancibia A, Alvarez-Rubio M, Day JW. Mangrove ecology, aquatic primary productivity, and fish community dynamics in the Teacapán-Agua Brava lagoon-estuarine system (Mexican Pacific). Estuaries [serial on the Internet]. 1990; 13(2):219-30. Available from: https://doi.org/10.2307/1351591
https://doi.org/10.2307/1351591...
; Tapia-Garcia et al., 1998Tapia-García M, Suárez Núñez C, Cerdenares-L Guevara G, Macuitl Montes MC, Garcia Abad MC. Composición y distribución de la ictiofauna en la laguna del Mar Muerto, Pacífico Mexicano. Rev Biol Trop [serial on the Internet]. 1998; 46 (2):277-84. Available from: http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77441998000200012&lng=en&nrm=iso&tlng=es
http://www.scielo.sa.cr/scielo.php?scrip...
; Castro-Aguirre et al., 1999Castro-Aguirre JL, Espinosa-Pérez H, Schmitter-Soto JJ. Ictiofauna estuarino-lagunar y vicaria de México. Mexico: Editorial Limusa; 1999.; Cabral-Solís, Espino-Barr, 2004Cabral-Solís EG, Espino-Barr E. Distribución y abundancia espacio-temporal de los peces en la laguna de Cuyutlán, Colima, México. Oceánides [serial on the Internet]. 2004; 19(1-2):19-27. Available from: http://oceanides.ipn.mx/index.php/cicimaroceanides/article/view/15
http://oceanides.ipn.mx/index.php/cicima...
; Díaz-Ruiz et al., 2006Díaz-Ruiz S, Aguirre-León A, Cano-Quiroga E. Ecological evaluation of fish community in two lagoon-estuarine systems of the south of Chiapas, Mexico. Hidrobiologica [serial on the Internet]. 2006; 16(2):197-210. Available from: http://www.scielo.org.mx/pdf/hbio/v16n2/v16n2a9.pdf
http://www.scielo.org.mx/pdf/hbio/v16n2/...
; Mendoza et al., 2009Mendoza E, Castillo-Rivera M, Zárate-Hernández R, Ortiz-Burgos S. Seasonal variations in the diversity, abundance, and composition of species in an estuarine fish community in the Tropical Eastern Pacific, Mexico. Ichthyol Res [serial on the Internet]. 2009; 56(4):330-39. Available from: https://doi.org/10.1007/s10228-009-0102-5
https://doi.org/10.1007/s10228-009-0102-...
). Recent studies in Barra de Navidad lagoon have reported these three species as regular components of the icthyofauna, appearing always as juveniles (González-Sansón et al., 2014aGonzález-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR, Hinojosa-Larios A, Silva-Bátiz FA. Species and size composition of fishes in Barra de Navidad lagoon, Mexican central Pacific. Rev Biol Trop [serial on the Internet]. 2014a; 62(1):129-44. Available from: https://doi.org/10.15517/rbt.v62i1.10001
https://doi.org/10.15517/rbt.v62i1.10001...
, 2014bGonzález-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR, Silva-Bátiz FA. Weight-length relationships for 38 fish species of Barra de Navidad coastal lagoon, Jalisco, Mexico. J Appl Ichthyol [serial on the Internet]. 2014b; 30(2):428-30. Available from: https://doi.org/10.1111/jai.12327
https://doi.org/10.1111/jai.12327...
, 2016González-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR. Spatial and temporal variations of juvenile fish abundance in Barra de Navidad coastal lagoon, Jalisco, México: Effects of hurricane Jova. Rev Biol Mar Oceanogr [serial on the Internet]. 2016; 51(1):123-36. Available from: https://doi.org/10.4067/S0718-19572016000100012
https://doi.org/10.4067/S0718-1957201600...
).

The coexistence of three lutjanid species which have much the same body shapes (Fischer et al., 1995Fischer W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem V. Rome: Food and Agriculture Organization of the United Nations ; 1995. vol. 3, Guía FAO para identificación de especies para los fines de la pesca: Pacífico centro-oriental, pt. 2, Vertebrados. Available from: http://www.fao.org/docrep/010/v6250s/v6250s00.htm
http://www.fao.org/docrep/010/v6250s/v62...
) and similar diets which are expected to be dominated by decapods and fishes (Rojas, 1997Rojas-M JR. Dieta del “pargo colorado” Lutjanus colorado (Pisces: Lutjanidae) en el Golfo de Nicoya, Costa Rica. Rev Biol Trop [serial on the Internet]. 1997; 45(3):1173-83. Available from: https://revistas.ucr.ac.cr/index.php/rbt/article/view/23864
https://revistas.ucr.ac.cr/index.php/rbt...
; Santamaría-Miranda et al., 2005Santamaría-Miranda A, Saucedo-Lozano M, Herrera-Moreno MN, Apún-Molina JP. Feeding habits of Lutjanus argentiventris and Lutjanus colorado (Pisces: Lutjanidae) in the north of Sinaloa, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2005; 40(1):33-44. Available from: http://www.revbiolmar.cl/resumenes/v401/401-33.pdf
http://www.revbiolmar.cl/resumenes/v401/...
; Ruiz-Nieto, 2005Ruiz-Nieto IC. Hábitos alimenticios de: Hoplopagrus guentherii, Lutjanus argentiventris, L. colorado, L. guttatus L. novemfasciatus y L. peru (Pisces: Lutjanidae) presentes en las costas del centro sur de Sinaloa. [MSc Thesis]. Ciudad de Mexico: Universidad Nacional Autónoma de México; 2005.; Flores-Ortega et al., 2010Flores-Ortega JR, Godínez-Domínguez E, Rojo-Vázquez JA, Corgos A, Galván-Piña VH, González-Sansón G. Interacciones tróficas de las seis especies de peces más abundantes en la pesquería artesanal en dos bahías del Pacífico Central Mexicano. Rev Biol Trop [serial on the Internet]. 2010; 58(1):383-97. Available from: https://doi.org/10.15517/rbt.v58i1.5217
https://doi.org/10.15517/rbt.v58i1.5217...
, 2014Flores-Ortega JR, Avila-Castro E, Haro-Preciado HJ, Godínez-Domínguez E. Food habits and trophic interactions of Anisotremus interruptus (Pisces: Haemulidae) and Lutjanus argentiventris (Pisces: Lutjanidae) in the Central Mexican Pacific. Lat Am J Aquat Res [serial on the Internet]. 2014; 42(1):276-82. Available from: http://www.lajar.cl/pdf/imar/v42n1/Articulo_42_1_24.pdf
http://www.lajar.cl/pdf/imar/v42n1/Artic...
) poses an important research question related to trophic niche overlap and the role played by morphological differences among these species. A well established ecological paradigm says that coexisting species must differ in their ecological requirements by at least some minimal amount to avoid competitive exclusion (Pianka, 1974Pianka ER. Niche overlap and diffuse competition. Proc Natl Acad Sci [serial on the Internet]. 1974; 71(5):2141-45. Available from: http://www.pnas.org/content/71/5/2141.full.pdf
http://www.pnas.org/content/71/5/2141.fu...
). Two main explanations can be invoked for understanding how similar species can share the same habitat avoiding competitive exclusion. Firstly, the extent to which dietary overlap occurs within and between species will most likely vary with body size due to size-specific changes in foraging ability (Pessanha, Araujo, 2014Pessanha ALM, Araújo FG. Shifts of the feeding niche along the size dimension of three juvenile fish species in a tidal mudflat in southeastern Brazil. Mar Biol [serial on the Internet]. 2014; 161(3):543-50. Available from: https://doi.org/10.1007/s00227-013-2356-8
https://doi.org/10.1007/s00227-013-2356-...
). Secondly, when biotic interactions are strong, species coexistence may be facilitated by functional trait complementarity that gives rise to some resource partitioning (Montaña et al., 2014Montaña CG, Winemiller KO, Sutton A. Intercontinental comparison of fish ecomorphology: null model tests of community assembly at the patch scale in rivers. Ecol Monogr [serial on the Internet]. 2014; 84(1):91-107. Available from: https://doi.org/10.1890/13-0708.1
https://doi.org/10.1890/13-0708.1...
). Therefore, subtle differences in morphology and dentition should be expected in otherwise very similar species, as is the case of the three species included in this study. The relationship between morphology and feeding characteristics in fishes has been investigated by numerous authors (Clifton, Motta, 1998Clifton KB, Motta PJ. Feeding morphology, diet, and ecomorphological relationships among five Caribbean labrids (Teleostei, Labridae). Copeia [serial on the Internet]. 1998; (4):953-66. Available from: http://www.jstor.org/stable/1447342
http://www.jstor.org/stable/1447342...
; Hugueny, Pouilly, 1999Hugueny B, Pouilly M. Morphological correlates of diet in an assemblage of West African freshwater fishes. J Fish Biol [serial on the Internet]. 1999; 54(6):1310-25. Available from: https://doi.org/10.1111/j.1095-8649.1999.tb02057.x
https://doi.org/10.1111/j.1095-8649.1999...
; Pouilly et al., 2003Pouilly M, Lino F, Bretenoux JG, Rosales C. Dietary-morphological relationships in a fish assemblage of the Bolivian Amazonian floodplain. J Fish Biol [serial on the Internet]. 2003; 62(5):1137-58. Available from: http://dx.doi.org/10.1046/j.1095-8649.2003.00108.x
http://dx.doi.org/10.1046/j.1095-8649.20...
; Ward-Campbell et al., 2005Ward-Campbell BMS, Beamish FWH, Kongchaiya C. Morphological characteristics in relation to diet in five coexisting Thai fish species. J Fish Biol [serial on the Internet]. 2005; 67(5): 1266-79. Available from: http://dx.doi.org/10.1111/j.1095-8649.2005.00821.x
http://dx.doi.org/10.1111/j.1095-8649.20...
; Wesneat, 2006Westneat MW. Skull biomechanics and suction feeding in fishes. In: Shadwick R, Lauder G, editors. Biomechanics. Elsevier Publishing; 2006. p.29-75. (Fish physiology series; v. 23).; Wittenrich et al., 2009Wittenrich ML, Rhody NR, Turingan RG, Main KL. Coupling osteological development of the feeding apparatus with feeding performance in common snook, Centropomus undecimalis, larvae: identifying morphological constraints to feeding. Aquaculture [serial on the Internet]. 2009; 294(3-4):221-27. Available from: http://doi.org/10.1016/j.aquaculture.2009.06.006
http://doi.org/10.1016/j.aquaculture.200...
; Pessanha et al., 2015Pessanha ALM, Araújo FG, Oliveira REM, Silva AF, Sales NS. Ecomorphology and resource use by dominant species of tropical estuarine juvenile fishes. Neotrop Ichthyol [serial on the Internet]. 2015; 13(2):401-12. Available from: http://dx.doi.org/10.1590/1982-0224-20140080
http://dx.doi.org/10.1590/1982-0224-2014...
; Novakowski et al., 2016Novakowski GC, Cassemiro FAS, Hahn NS. Diet and ecomorphological relationships of four cichlid species from the Cuibá River basin. Neotrop Ichthyol [serial on the Internet]. 2016; 14(3):150-51. Available from: http://dx.doi.org/10.1590/1982-0224-20150151
http://dx.doi.org/10.1590/1982-0224-2015...
). Based on results obtained from previous studies, Nanami, Shimose (2013Nanami A, Shimose T. Interspecific differences in prey items in relation to morphological characteristics among four lutjanid species (Lutjanus decussatus, L. fulviflamma, L. fulvus and L. gibbus). Environ Biol Fishes [serial on the Internet]. 2013; 96(5):591-602. Available from: https://doi.org/10.1007/s10641-012-0049-7
https://doi.org/10.1007/s10641-012-0049-...
) stated that body shape variations of fishes and the variety of their dentition affect feeding performance. These authors also remarked that clarifying the interspecific difference in prey items of fishes in relation to body shape variations is a fundamental aspect to understand the feeding ecology of fishes.

Main goals of this study were a) to perform comparative analyses of the diets of three sympatric species of the genus Lutjanus with emphasis in trophic niche breadth and overlap; b) to investigate the existence of ontogenic changes in feeding habits during their juvenile stages and c) to compare the species on the basis of some morphometric and teeth characteristics. The working hypothesis was that the species involved in this study feed on a common base of food resources formed by invertebrates and small benthic-pelagic fishes and therefore, some niche overlap is present in terms of general diet composition. However, changes in the feeding niche with size and differences in some morphological traits among species explain observed differences in diet composition and contribute to facilitate their coexistence in the same estuarine system.

Material and Methods

Barra de Navidad lagoon is located on the Pacific coast of Mexico (19°11′25″N 104°39′53″W). It has a total surface of 3.76 km3 and was categorized as III-A(III-B) by Lankford (1976Lankford RR. Coastal lagoons of Mexico: their origin and classification. In: Wiley M, editor. Estuarine processes. New York: Academic Press; 1976 . p.182-215. vol. 2, Circulation, sediments, and transfer of material in the estuary.), which means waves and coastal currents dominate its formation. The lagoon has a permanent inlet communicating with the sea. The freshwater input is strongly seasonal, due to a rainy season from June to October and a dry season with almost no rainfall from November to May. The lagoon is primarily euhaline (salinity 30-40), although it can be mixopolyhaline (salinity 18-30) during short periods during the rainy season (González-Sansón et al., 2014aGonzález-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR, Hinojosa-Larios A, Silva-Bátiz FA. Species and size composition of fishes in Barra de Navidad lagoon, Mexican central Pacific. Rev Biol Trop [serial on the Internet]. 2014a; 62(1):129-44. Available from: https://doi.org/10.15517/rbt.v62i1.10001
https://doi.org/10.15517/rbt.v62i1.10001...
).

Fish were collected during 42 regular sampling trips from February 2011 to January 2012. Sampling sites were chosen at random each month in an effort to cover the entire lagoon and to obtain a total sample representative of the water body. All sampling sites were characterized by a muddy substrate and relatively shallow depths (1-2 m). Monthly numbers of fish collected varied depending on natural abundance of the species, with 23 to 67 fish caught per month. Several supplementary samples were taken sporadically from 2013 to 2014. Fish were caught from late afternoon (4-5 pm) to midnight. Sampling gear included a beach purse seine (10 m long, 1 cm mesh size), a cast net (3 m, 2.5 cm mesh size) and four gill nets (60 m each) of different mesh sizes (7.0, 7.6, 8.9 and 10.2 cm). Sampled fish were taken to the laboratory where they were identified and their total lengths (TL) were measured. Stomachs were removed and contents preserved in 70% ethanol for later identification.

Stomach contents were examined under a dissecting DV4 Zeiss microscope and each food item was identified to the lowest possible taxonomic level, or recorded as unidentifiable. When possible, each item was measured to the nearest 0.1 mm. For shrimp and fish the total length was used, while for crabs the carapace width (Cw) was measured. Each food item was weighed using an Ohaus balance. The correlation of food item size with total fish length was analyzed using STATISTICA 7.1. To assess whether the number of sampled stomachs was sufficient to describe the diet, cumulative curves of trophic diversity were computed with EstimateS software (Colwell, 2013Colwell RK. EstimateS: Statistical estimation of species richness and shared species from samples, Version 9. User’s Guide and application 2013. [updated 2013 Jun 14; cited 2017 Feb 7]. Available from: Available from: http://purl.oclc.org/estimates .
http://purl.oclc.org/estimates...
) based on 100 randomizations without replacement to ensure that the curves really reached an asymptotic value. The value of the Shannon index (H’, Magurran, 2004Magurran AE. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.) was plotted against the cumulative number of stomachs examined (Figueiredo et al., 2005Figueiredo M, Morato T, Barreiros JP, Afonso P, Santos RS. Feeding ecology of the white seabream, Diplodus sargus, and the ballan wrasse, Labrus bergylta, in the Azores. Fish Res [serial on the Internet]. 2005; 75(1):107-19. Available from: https://doi.org/10.1016/j.fishres.2005.04.013
https://doi.org/10.1016/j.fishres.2005.0...
). Each diversity curve was considered asymptotic if at least two previous values to the total sample trophic diversity (H’tot) were in the range H’tot± 0.05H’tot (Alonso et al., 2002Alonso MK, Crespo EA, García NA, Pedraza SN, Mariotti PA, Mora NJ. Fishery and ontogenetic driven changes in the diet of the spiny dogfish, Squalus acanthias, in Patagonian waters, Argentina. Environ Biol Fishes [serial on the Internet]. 2002; 63(2):193-202. Available from: https://doi.org/10.1023/A:1014229432375
https://doi.org/10.1023/A:1014229432375...
). For further analyses, food items were pooled into food categories, using the family as the reference level. The relative importance of each food category in the diet was expressed after Hyslop (1980Hyslop EJ. Stomach contents analysis: a review of methods and their application. J Fish Biol [serial on the Internet]. 1980; 17(4):411-29. Available from: https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
ttps://doi.org/10.1111/j.1095-8649.1980....
) as percentage of numerical abundance (N%), frequency of occurrence of food items in stomachs (F%), and weight (W%). The prey-specific index of relative importance (PSIRI) was calculated to get a better grasp of the importance of food items for each species, using the following equation (Brown et al., 2012Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA. Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert 1896). Environ Biol Fishes [serial on the Internet]. 2012; 95(1):3-20. Available from: https://doi.org/10.1007/s10641-011-9959-z
https://doi.org/10.1007/s10641-011-9959-...
):

% P S I R I i = % F O i × % P N i + % P W i / 2

where %PSIRIi = PSIRI for prey i, expressed as percentage, %FOi = Frecuency of ocurrency for prey i, expressed as percentage, %PNi = Prey-specific numerical abundance for prey i, expressed as percentage, %PWi = Prey-specific weight abundance for prey i, expressed as percentage.

To analyze ontogenetic changes, fish were classified into three groups based on their total length as follows: group 1, TL less than or equal to 7 cm; group 2, TL higher than 7 cm and less than or equal to 21 cm; and group 3, TL higher than 21 cm.

For morphological analyses standard length (SL), maximum body height (BH), head height behind eye (HHBE) peduncle height (PH), eye diameter (ED), mouth width (MW) and mouth height (MH) were measured to the nearest millimeter in a subsample of the individuals analyzed for stomach contents. Gape area (GA) was calculated assuming an elliptical form using the formula g=(3.1416 * MW * MH)/2 (Fig. 1). Dentaries and premaxillas of ten specimens of each species were obtained by boiling the fish heads, extracting the bones and cleaning them with a sodium hypochlorite solution. Cleaned bones were then photographed (Figs. 2-3) and teeth lengths were measured to the nearest tenth of millimeter using the free software ImageJ 1.42q (Schneider et al., 2012Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods [serial on the Internet]. 2012; 9(7):671-75. Available from: http://dx.doi.org/10.1038/nmeth.2089
http://dx.doi.org/10.1038/nmeth.2089...
). Teeth were classified into three groups (Allen, 1985Allen GR. FAO species catalogue. Rome: Food and Agriculture Organization of the United Nations; 1985. vol. 6, Snappers of the world: An annotated and illustrated catalogue of Lutjanid species known to date. (FAO Fisheries Synopsis; no. 125). Available from: http://afrilib.odinafrica.org/handle/0/15796
http://afrilib.odinafrica.org/handle/0/1...
): (i) those in the dentary (DT), (ii) frontal large canine in the premaxilla (LCP) and (iii) smaller conical teeth in the premaxilla (SCP). All measures were expressed as ratios with respect to SL. Ratios were multiplied by convenient factors to avoid decimal zeros.

Fig. 1
Morphometric measures used for the study.

Fig. 2
Dentaries of three species of snappers. In brackets, standard lengths of fish. Lutarg: Lutjanus argentiventris; Lutcol: Lutjanus colorado; Lutnov: Lutjanus novemfasciatus

Fig. 3
Premaxillas of three species of snappers. In brackets, standard lengths of fish. LCP=Large canines in premaxillas; SCT=Smaller conical teeth in premaxillas. Lutarg: Lutjanus argentiventris; Lutcol: Lutjanus colorado; Lutnov: Lutjanus novemfasciatus.

All numerical analyses related to niche breadth and overlap were performed on W% values because we are primarily interested in future assessment of energy flow in the food web of the lagoon (Hansson, 1998Hansson S. Methods of studying fish feeding: a comment. Can J Fish Aquat Sci [serial on the Internet]. 1998; 55(12):2706-07. Available from: https://doi.org/10.1139/f98-158
https://doi.org/10.1139/f98-158...
). Statistical significance of differences among diet compositions of all pairs of species-size classes groups was assessed using numerical classification based on the Bray-Curtis index of similarity and UPGMA cluster algorithm. Similarity values were calculated on fourth-root transformed data of percentage weight diet composition to compensate the effect of dominant prey items in the comparisons. A SIMPROF test (Clarke et al., 2008Clarke KR, Somerfield PJ, Gorley RN. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Bio Ecol [serial on the Internet]. 2008; 366(1-2):56-69. Available from: https://doi.org/10.1016/j.jembe.2008.07.009
https://doi.org/10.1016/j.jembe.2008.07....
) was used to assess the significance of the groups in the dendrogram. To further explore diet relationships, a Principal Coordinate Analysis (PCO) was performed on the same similarity matrix used for classification and a vector overlay was superimposed on the scatterplot of the two first PCO-axes including only food categories with 0.5 or higher values of Spearman correlations with the axes. The relative size and position of the vector overlay on the graph is arbitrary with respect to the underlying plot (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth (UK): PRIMER-E; 2008.).

Trophic niche breadth was measured using Smith´s index (FT), using the following equation (Krebs, 1998Krebs CJ. Ecological methodology, 2nd ed. San Francisco: Benjamin Cummings; 1998.): FT=pjai , where pj = proportion of diet item j, aj = proportion of diet item j of total food items available (assumed equal for all items).

This measure was selected because its theoretical distribution is known and confidence intervals can be calculated (Krebs, 1998Krebs CJ. Ecological methodology, 2nd ed. San Francisco: Benjamin Cummings; 1998.). Diet overlap was calculated using Pianka´s index (Gotelli, Graves, 1996Gotelli NJ, Graves GR. Null Models in Ecology. Washington (D): Smithsonian Institution Press; 1996.). The null hypothesis of no niche overlap was tested using the methodology based in null models as described in Gotelli, Graves (1996Gotelli NJ, Graves GR. Null Models in Ecology. Washington (D): Smithsonian Institution Press; 1996.). The program ECOSIM v. 7.72 (Gotelli, Entsminger, 2004Gotelli NJ, Entsminger GL. EcoSim: Null models software for ecologists, version 7.0. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. 2004. Available from: http://garyentsminger.com/ecosim/index.htm.
http://garyentsminger.com/ecosim/index.h...
) was used for simulations with 1000 iterations, using resampling algorithm R3 (i.e. retention of niche breadth with zero states reshuffling) and defining resource states as equiprobable.

The significance of differences in morphological variables among species was tested using one-way fixed effects ANOVAs followed by the Student-Newman-Keuls multiple comparisons test when F ratios were significant. Prior to ANOVAs the assumptions of normality and homoscedasticity were checked following the criteria of Underwood (1997Underwood AJ. Experiments in ecology: Their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press; 1997.). Analyses were made with packages STATISTICA 7.1 (StatSoft, 2006StatSoft, Inc. STATISTICA [Data analysis software system], version 7.1. 2006. Available from: http://www.statsoft.com.
http://www.statsoft.com...
), PRIMER 6.0 (Clarke, Gorley, 2006Clarke KR, Gorley RN. PRIMER v6: User manual/Tutorial. Plymouth (UK): PRIMER-E; 2006.) and PERMANOVA+ for PRIMER (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth (UK): PRIMER-E; 2008.). Significance level for all tests was α = 0.05.

Results

The total number of analyzed stomachs was 288 (97 empty) for Lutjanus argentiventris from 2.3 to 19.9 cm TL; 178 (43 empty) for Lutjanus colorado ranging from 2.4 to 30.1 TL; and 183 (62 empty) for Lutjanus novemfasciatus from 1.2 to 20.0 cm TL. Diets of the three species were dominated by fish and decapods (Tab. 1).

Tab. 1
Diet composition of three species of snappers in Barra de Navidad lagoon. W%: percentage weight; N%: percentage number; F%: percentage frequency; P%: percentage of prey-specific index of relative importance (PSIRI). NI=Not identified.

The diet of L. argentiventris was composed mainly of decapods (62% PSIRI) with an important contribution of fish in weight (21% PSIRI) and much smaller contributions of stomatopods and other invertebrates (Tab. 1). Decapods pertained mostly to four families (in descending order of their contributions as % PSIRI): i) Penaeidae, which was represented by juveniles of Penaeus californiensis Holmes, 1900 (5.3-15 mm TL); ii) Portunidae, dominated by juvenile Callinectes arcuatus Ordway, 1863 (1.8-16.0 mm Cw); iii) Xanthidae, represented mainly by Panopeus sp. (4.5-16.0 Cw) with small quantities of Lophoxanthus lamellipes (Stimpson, 1860) (4.5-7.7 mm Cw), Actea sp., Eurypanopeus sp., and Lophopanopeus sp; and iv) Alpheidae, represented by four species dominated by Alpheus mazatlanicus Wicksten, 1983 (10.0-14.0 mm TL) and A. pacificus Dana, 1852 (7.7-16.0 mm TL), with small contributions by A. floridanus Kingsley, 1878 (one specimen of 5.4 mm TL) and A. cylindricus Kingsley, 1878 (not measured, partially digested). Identifiable fish remains were dominated by Gobiidae (not measured, partially digested) with a smaller representation of Congridae (one species of genus Heteroconger Bleeker, 1868, 42 mm TL), Lutjanidae (genus Lutjanus Bloch, 1790, 15.0-18.0 mm TL), Eleotridae (Erotelis armiger (Jordan & Richardson, 1895), 20 mm TL) and Paralichthydae (not measured, partially digested).

The main components in the diet of L. colorado were decapods (68% PSIRI) and in less proportion fish which contributed 28% of total PSIRI. Incidental contributions of stomatopods, mollusks and other invertebrates were found (Tab. 1). Decapods were dominated by five families (in descending order of their contributions as % PSIRI): i) Portunidae, represented by juveniles of C. arcuatus (1.7-37.0 mm Cw); ii) Upogebiidae, mainly Upogebia dawsoni Williams, 1986 (19.0-23.0 mm TL); iii) Alpheidae with only one species, A. mazatlanicus (8.0-29.0 mm Cw); iv) Penaeidae, represented by juveniles of F. californiensis (7.0-10.0 mm TL) and v) Grapsidae, represented by Goniopsis pulchra (Lockington, 1877) (7.2-21.0 mm Cw) and Grapsus grapsus (Linnaeus, 1758) (8.6 mm Cw). A high percentage of fish remains found in stomachs of this species were too digested for identification to any taxonomical level. Of those which were identifiable, the dominant family was Eleotridae, represented by Erotelis armiger (80.0-95.0 mm TL).

The diet of L. novemfasciatus was dominated almost equally by decapods (50% PSIRI) and fishes (44% PSIRI) with a small amount of other invertebrates (Tab. 1). Decapods were dominated by four families (in descending order of their contributions as % PSIRI): i) Palaemonidae, dominated by Palaemon hiltoni (Schmitt, 1921) (6.2-12.9 mm TL); ii) Penaeidae, represented by juveniles of F. californiensis (7.0-15.0 mm TL); iii) Portunidae, represented by juveniles of C. arcuatus (2.0-14.0 mm Cw) and iv) Upogebiidae, mainly U. dawsoni (14.0-22.0 mm TL). Although a high percentage of fish remains found in stomachs of this species were too digested, a portion was identifiable and revealed higher prey diversity (seven families) in this species compared to the other two species included in this research. Those fish which were less damaged by digestion and could be measured included: an unidentified specimen of Ariidae (possibly Sciades guatemalensis (Günther, 1864), 27.0 mm TL); Centropomus robalito Jordan & Gilbert, 1882 (22.0-24.0 mm TL); unidentified specimens of Gerreidae (14.0-16.0 mm TL); Heteroconger sp. (50.0-70.0 mm TL) and the genus Anchoa Jordan & Evermann, 1927 (22.0-54.0 mm TL).

Fish longer than 21 cm were not present in sampled individuals of the species L. argentiventris and L. novemfasciatus. Therefore, only seven groups resulted from the combination of species and length classes. In all groups the cumulative curves of trophic diversity reached an asymptote, indicating adequate sample sizes (Fig. 4).

Fig. 4
Cumulative curves of food items. Lutarg: Lutjanus argentiventris; Lutcol: Lutjanus colorado; Lutnov: Lutjanus novemfasciatus. Numbers indicate size classes: 1 for LT < 7 cm; 2 for LT ≥ 7 cm and LT < 21 cm; 3 for LT ≥ 21 cm.

Numerical classification of the seven species-size groups yielded two significant clusters (Fig. 5a). The first cluster (I) included both size-classes of Lutjanus novemfasciatus joining at a similarity value of 86.7. The second cluster (II) was formed by all size-classes pertaining to L. colorado and L. argentiventris which join at a similarity level of 58.8%. The first axis of PCO explained 50.2% of total variation while the second axis explained 23.2%, resulting in an easily interpretable two dimensional diagram with a 73.4% of explained variation (Fig. 5b). Based on the vector overlay of prey categories it can be concluded that the main food items explaining the ordination of samples along the first axis are most fish categories and some invertebrate categories (e.g. Palaemonidae, Callianassidae) to the left side while Eleotridae, Paralichthyiidae and most decapod families (e.g. Solecurtidae, Alpheidae, Portunidae, Gecarcinidae, Ocypodidae, Grapsidae) dominated in the right side of this axis. This can be considered as a gradient of decreasing piscivory. Ordination of species-size groups along the first axis match well with numerical classification results separating L. novemfasciatus from the two other species. Projection on the second axis allows further separation of L. argentiventris from L. colorado, supporting the clustering observed in the numerical classification which was, however, a non-significant grouping after the SIMPROF test. Considering the percentage prey weight and the vector overlay, it is evident that the separation along this axis is due mainly to Eleotridae and Portunidae, which are dominant preys items in L. colorado, and Gobiidae, Panaeidae and Xanthidae, which are dominant in L. argentiventris diet (Tab. 1).

Fig. 5
a: Dendrogram showing the result of numerical classification of stomach contents. Results of SIMPROF test separating significant groups are given. b: Principal coordinate analysis plot. Vector overlay shows food categories with Spearman’s correlation values of 0.5 or higher with ordination axes. Data pooled by species (circles: Lutjanus novemfasciatus; squares: Lutjanus argentiventris; triangles: Lutjanus colorado) and size classes (black: ≤ 7 mm TL; grey: > 7 y ≤ 21 mm TL; white: > 21 mm TL).

Estimates of Smith’s index (niche breadth) varied from 0.732 to 0.890 with lower values associated to larger sizes and higher percentage of fish by weight in diet composition inside each species (Fig. 6). Estimates of Pianka’s index (niche overlap) varied between 0.598 and 0.990 (Tab. 2). In all cases pairs of size-classes within each species showed higher values than pairs of size-classes between species. Mean observed overlap was 0.761 and was significantly higher (p=0.001) than mean expected overlap (0.193) yielded by simulation under the null model of no diet overlapping. Variance of overlap values was 0.011 and was not significantly different (p=0.058) with the mean of simulated variance values (0.023) obtained under the null model.

Fig. 6
Estimated values of Smith´s index of niche breadth (black circle, continuous line) and 95% confidence intervals (vertical lines). Also shown percentage weight of fish in diet (white circles, dashed lines). Data pooled by species (Lutarg: Lutjanus argentiventris; Lutcol: Lutjanus colorado; Lutnov: Lutjanus novemfasciatus) and size classes (1: ≤ 7 mm TL; 2: > 7 y ≤ 21 mm TL; 3: > 21 mm TL).

Tab. 2
Pianka’s overlap inices among species size classes. Highlighted values correspond to pairs including size-classes of the same species. Lutarg: Lutjanus argentiventris; Lutcol: Lutjanus colorado; Lutnov: Lutjanus novemfasciatus ; 1: ≤ 7 mm TL; 2: > 7 y ≤ 21 mm TL; 3: > 21 mm TL.

A significant rank correlation between prey size and fish length was found for food items classified as decapods (Fig. 7) and fishes (Fig. 8) for pooled data. The analyses for decapod prey made for each species separately yielded significant correlations for L. argentiventris (rs=0.43, p<0.001, n=113) and L. colorado (rs=0.72, p<0.001, n=73) but no significant correlation for L. novemfasciatus (rs=0.06, p=0.561, n=80). Fish prey showed significant correlations with predator size for L. colorado (rs=0.92, p=0.003, n=7) and L. novemfasciatus (rs=0.69, p=0.018, n=11) but not for L. argentiventris (rs=0.74, p=0.153, n=5), where the sample size was too low.

Fig. 7
Scatterplot of prey size vs. fish size for decapods found in the stomachs of three species of snappers. Main food categories identified by different symbols: White diamons = Alpheidae; white triangles = Palaemonidae; White circles = Penaeidae; White squares = Upogebiidae; black diamonds = Grapsidae; black triangles = Portunidae; black circles = Porcellanidae; black squares = Xanthidae; crosses = other items.

Fig. 8
Scatterplot of prey size vs. fish size for fishes found in the stomachs of three species of snappers (data pooled for all species). Main food categories identified by different symbols: White circles = Eleotridae; Black circles = Congridae; Triangles = Engraulidae; White triangles = Lutjanidae; Crosses = Centropomide; Black square = Other.

Most morphometric measures showed significant differences among species (Tab. 3). Relative body height and head height behind the eye were not different between L. argentiventris and L. colorado, but were significantly greater in those two species than L. novemfasciatus, which resulted to be the more slender species. Relative eye diameter was different among species, with L. argentiventris having the largest eye and L. colorado the smallest. Relative peduncle height and mouth width were significantly larger in L. novemfasciatus compared to the other species, which showed no statistical differences between them. Relative mouth gape was not different between L. novemfasciatus and L. colorado, but was significantly greater in these two species compared to L. argentiventris. In pooled data for all three species, a high correlation was found between length and mouth gape (Fig. 9). Relative length of dentary and conical premaxilla teeth were significantly higher in L. novemfasciatus compared to the other two species. In addition, the conical premaxilla teeth were relatively larger in L. colorado compared to L. argentiventris.

Fig. 9
Variation of gape size (log transformed) with standard length (SL, log transformed) for individuals of three species of Lutjanus. Filled circles: L. argentiventris; Open circles: L. novemfasciatus; Squares: L. colorado.

Tab. 3
Means, standard errors (SE) and ANOVAs results for the morphometric variables of Lutjanus argentiventris (Lutarg), L. colorado (Lutcol) and L. novemfasciatus (Lutnov) expressed as ratios on standard length. SL: standard length, BH: maximum body height, ED: eye diameter, HHBE: Head height behind eye, PH: peduncle height, MH: mouth height, MW: mouth width, GA: Gape area, DT: length of dentary’s teeth, LCP: length of large canines in premaxilla, SCT: length of small conical teeth in premaxila. Different letters besides the means indicate significant differences after the SNK test.

Discussion

The present study showed clear difference in diet composition among three lutjanid species. Both the numerical classification and simulation using null models support the idea of some niche overlap. At the same time, slight but significant differences in diet composition were present and significant among species. This result matches well with the fact that diet overlap among size classes inside each species is always higher than diet overlap among size classes of different species. Interspecific differences in diet composition found in this study result from variations in the proportion of decapod and fish prey, with an increase in the proportion of fish from Lutjanus argentiventris and L. colorado to L. novemfasciatus. These results indicate a more piscivorous habit in L. novemfasciatus compared to the other two species. A similar pattern emerges from the following summary of the results obtained for the same three species by several authors in other places of the Mexican Pacific. Flores-Ortega et al. (2010Flores-Ortega JR, Godínez-Domínguez E, Rojo-Vázquez JA, Corgos A, Galván-Piña VH, González-Sansón G. Interacciones tróficas de las seis especies de peces más abundantes en la pesquería artesanal en dos bahías del Pacífico Central Mexicano. Rev Biol Trop [serial on the Internet]. 2010; 58(1):383-97. Available from: https://doi.org/10.15517/rbt.v58i1.5217
https://doi.org/10.15517/rbt.v58i1.5217...
; 2014Flores-Ortega JR, Avila-Castro E, Haro-Preciado HJ, Godínez-Domínguez E. Food habits and trophic interactions of Anisotremus interruptus (Pisces: Haemulidae) and Lutjanus argentiventris (Pisces: Lutjanidae) in the Central Mexican Pacific. Lat Am J Aquat Res [serial on the Internet]. 2014; 42(1):276-82. Available from: http://www.lajar.cl/pdf/imar/v42n1/Articulo_42_1_24.pdf
http://www.lajar.cl/pdf/imar/v42n1/Artic...
) found a diet based in crustaceans and fishes for L. argentiventris collected off Jalisco. Vazquez et al. (2008Vázquez RI, Rodríguez J, Abitia LA, Galván F. Food habits of the yellow snapper Lutjanus argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2008; 43(2):295-302. Available from: http://www.revbiolmar.cl/resumenes/v432/432-295.pdf
http://www.revbiolmar.cl/resumenes/v432/...
) investigated the diet of same species in La Paz bay (Gulf of California) and reported that main items in the diet of juvenile fish were non identified organic matter, the decapod Upogebia pugettensis and penaeid shrimps. Ruiz-Nieto (2005Ruiz-Nieto IC. Hábitos alimenticios de: Hoplopagrus guentherii, Lutjanus argentiventris, L. colorado, L. guttatus L. novemfasciatus y L. peru (Pisces: Lutjanidae) presentes en las costas del centro sur de Sinaloa. [MSc Thesis]. Ciudad de Mexico: Universidad Nacional Autónoma de México; 2005.) reported the feeding habits of L. argentiventris in Sinaloa and found a diet dominated by shrimps and crabs for medium sized fishes (14-26 cm) while larger fish (27-58.8 cm) fed mainly on fishes. Santamaría-Miranda et al. (2005Santamaría-Miranda A, Saucedo-Lozano M, Herrera-Moreno MN, Apún-Molina JP. Feeding habits of Lutjanus argentiventris and Lutjanus colorado (Pisces: Lutjanidae) in the north of Sinaloa, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2005; 40(1):33-44. Available from: http://www.revbiolmar.cl/resumenes/v401/401-33.pdf
http://www.revbiolmar.cl/resumenes/v401/...
) analyzed stomach contents of L. colorado (14.4-40 cm LT) caught with long-line in coastal waters of the Gulf of California and found a diet based on invertebrates dominated by decapods and stomatopods with no fish reported in stomach contents. In contrast with the two former species, a diet dominated by fishes with a small proportion of crustaceans was reported for L. novemfasciatus by Yañez-Arancibia (1978Yañez-Arancibia A. Taxonomía, ecología y estructura de las comunidades de peces en las lagunas costeras con bocas efímeras del Pacífico de Mexico. Distrito Federal: Universidad Nacional Autónoma de Mexico; 1978. (Publicaciones especiales, Centro de Ciencias del Mar y Limnologia; 2).) in several coastal lagoons from Guerrero, Ruiz-Nieto (2005Ruiz-Nieto IC. Hábitos alimenticios de: Hoplopagrus guentherii, Lutjanus argentiventris, L. colorado, L. guttatus L. novemfasciatus y L. peru (Pisces: Lutjanidae) presentes en las costas del centro sur de Sinaloa. [MSc Thesis]. Ciudad de Mexico: Universidad Nacional Autónoma de México; 2005.) in estuarine habitats of Sinaloa, both.

Comparative analyses of morphometric characteristics help explain the interspecific differences in the diet of the three studied species. The significant lower relative body height (BH) and head height behind the eye (HHBE) found for L. novemfasciatus implies flatter body and head, a characteristic which Nanami, Shimose (2013Nanami A, Shimose T. Interspecific differences in prey items in relation to morphological characteristics among four lutjanid species (Lutjanus decussatus, L. fulviflamma, L. fulvus and L. gibbus). Environ Biol Fishes [serial on the Internet]. 2013; 96(5):591-602. Available from: https://doi.org/10.1007/s10641-012-0049-7
https://doi.org/10.1007/s10641-012-0049-...
) associated with a higher proportion of fishes in the diet of snapper species. These authors also found that fish were the major prey items for species of snappers with a shallower body depth and longer teeth, which match well with the findings for L. novemfasciatus reported here.

Prey sizes showed positive correlation with fish size, which in turn was strongly correlated with mouth gape. This result is explained by the ability of predators with larger gape for capturing and ingesting larger prey, and it is an important ontogenetic change that has also been identified for other fish species (Edgar, Shaw, 1995Edgar GJ, Shaw C. The production and trophic ecology of shallow-water fish assemblages in southern Australia III. General relationships between sediments, seagrasses, invertebrates and fishes. J Exp Mar Bio Ecol [serial on the Internet]. 1995; 194(1):107-31. Available from: https://doi.org/10.1016/0022-0981(95)00085-2
https://doi.org/10.1016/0022-0981(95)000...
; Hyndes et al., 1997Hyndes GA, Platell ME, Potter IC. Relationships between diet and body size, mouth morphology, habitat and movements of six sillaginid species in coastal waters: implications for resource partitioning. Mar Biol [serial on the Internet]. 1997; 128(4):585-98. Available from: https://doi.org/10.1007/s002270050125
https://doi.org/10.1007/s002270050125...
; Duarte, Garcia, 1999Duarte LO, García CB. Diet of the mutton snapper Lutjanus analis (Cuvier) from the Gulf of Salamanca, Colombia, Caribbean Sea. Bull Mar Sci [serial on the Internet]. 1999; 65(2):453-65. Available from: http://www.ingentaconnect.com/content/umrsmas/bullmar
http://www.ingentaconnect.com/content/um...
; Saucedo-Lozano et al., 1999Saucedo-Lozano M, González-Sansón G, Chiappa-Carraza X. Natural feeding of juveniles of Lutjanus peru (Nichols and Murphy, 1922) (Lutjanidae: Perciformes) off the coast of Jalisco and Colima, Mexico. Cienc Mar [serial on the Internet]. 1999; 25(3):381-400. Available from: http://dx.doi.org/10.7773/cm.v25i3.716
http://dx.doi.org/10.7773/cm.v25i3.716...
; Scharf et al., 2000Scharf FS, Juanes F, Rountree RA. Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser [serial on the Internet]. 2000; 208:229-48. Available from: http://www.jstor.org/stable/24863819
http://www.jstor.org/stable/24863819...
; Cocheret de la Moriniere et al., 2003Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, van der Velde G. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar Coast Shelf Sci [serial on the Internet]. 2003; 57(5-6):1079-89. Available from: https://doi.org/10.1016/S0272-7714(03)00011-8
https://doi.org/10.1016/S0272-7714(03)00...
; Pessanha, Araujo, 2014Pessanha ALM, Araújo FG. Shifts of the feeding niche along the size dimension of three juvenile fish species in a tidal mudflat in southeastern Brazil. Mar Biol [serial on the Internet]. 2014; 161(3):543-50. Available from: https://doi.org/10.1007/s00227-013-2356-8
https://doi.org/10.1007/s00227-013-2356-...
). The decrease in niche breadth for increasing size-classes inside each species found in our research, can be interpreted as a progressive specialization in feeding habits. This is consistent with the increase in the percentage of fish in the diet of larger size-classes inside each species. As snappers become larger, invertebrates play a lesser role in their diets and fish adopt a more piscivorous feeding behavior narrowing their food spectra. A similar result has been found for species of genus Lutjanus by other authors (Ruiz-Nieto, 2005Ruiz-Nieto IC. Hábitos alimenticios de: Hoplopagrus guentherii, Lutjanus argentiventris, L. colorado, L. guttatus L. novemfasciatus y L. peru (Pisces: Lutjanidae) presentes en las costas del centro sur de Sinaloa. [MSc Thesis]. Ciudad de Mexico: Universidad Nacional Autónoma de México; 2005.; Vazquez et al., 2008Vázquez RI, Rodríguez J, Abitia LA, Galván F. Food habits of the yellow snapper Lutjanus argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2008; 43(2):295-302. Available from: http://www.revbiolmar.cl/resumenes/v432/432-295.pdf
http://www.revbiolmar.cl/resumenes/v432/...
; Wells et al., 2008Wells RJD, Cowan JH Jr, Fry B. Feeding ecology of red snapper Lutjanus campechanus in the northern Gulf of Mexico. Mar Ecol Prog Ser [serial on the Internet]. 2008; 361:213-25. Available from: http://www.jstor.org/stable/24872550
http://www.jstor.org/stable/24872550...
; Pimentel, Joyeux, 2010Pimentel CR, Joyeux JC. Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. J Fish Biol [serial on the Internet]. 2010; 76(10): 2299-317. Available from: http://dx.doi.org/10.1111/j.1095-8649.2010.02586.x
http://dx.doi.org/10.1111/j.1095-8649.20...
). A transition from invertebrates to fishes in diet appears to be very general in ram-suction feeding fishes and is probably driven largely by the constraints of mouth size on prey capture ability (Wainwright, Richards, 1995Wainwright PC, Richard BA. Predicting patterns of prey use from morphology of fishes. Environ Biol Fish [serial on the Internet]. 1995; 44:97-113. Available from: https://doi.org/10.1007/978-94-017-1356-6_7
https://doi.org/10.1007/978-94-017-1356-...
). This is to be expected after the optimum foraging theory, which states that with an increase in size, predators tend to consume heavier prey, thus maximizing the energetic gain relative to capture effort (Duarte, Garcia, 1999Duarte LO, García CB. Diet of the mutton snapper Lutjanus analis (Cuvier) from the Gulf of Salamanca, Colombia, Caribbean Sea. Bull Mar Sci [serial on the Internet]. 1999; 65(2):453-65. Available from: http://www.ingentaconnect.com/content/umrsmas/bullmar
http://www.ingentaconnect.com/content/um...
). This result supports also our working hypothesis.

Numerical classification did not show differences in diet composition among size-classes for any species. This seems contradictory with the well supported ontogenic changes discussed above. A plausible explanation for this inconsistency is that the significance test used to define interpretable clusters (SIMPROF) is sensitive to the number of samples (in our case seven combinations of species by size-classes). More specifically, the power of the test to detect structure will tend to increase as the number of samples increases, so that the similarity profile displays a richer set of similarities (Clarke et al., 2008Clarke KR, Somerfield PJ, Gorley RN. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Bio Ecol [serial on the Internet]. 2008; 366(1-2):56-69. Available from: https://doi.org/10.1016/j.jembe.2008.07.009
https://doi.org/10.1016/j.jembe.2008.07....
). In other words, the SIMPROF test was able to detect differences in diet composition among species (number of samples = 7) but was not powerful enough for detecting differences among size-classes inside each species (number of samples = 2 or 3).

After Gotelli, Graves (1996Gotelli NJ, Graves GR. Null Models in Ecology. Washington (D): Smithsonian Institution Press; 1996.) a significantly large overlap might indicate shared resource utilization and a lack of competition. These authors argument that it is also possible that high overlap implies strong competition that has not yet led to divergence in resource use. In our case, additional data on resource availability and species interactions would be necessary for a definitive answer (Raborn et al., 2004Raborn SW, Miranda LE, Driscoll MT. Diet overlap and consumption patterns suggest seasonal flux in the likelihood for exploitative competition among piscivorous fishes. Ecol Freshw Fish [serial on the Internet]. 2004; 13(4):276-84. Available from: http://dx.doi.org/10.1111/j.1600-0633.2004.00066.x
http://dx.doi.org/10.1111/j.1600-0633.20...
). It should be emphasized, however, that fish included in our study are juvenile individuals which are part of the lagoon´s fish assemblage just for a short period (compared to their life spans). For this reason, any competition by food resources inside the lagoon (in case such resources were in shortage) will be transitory. In addition, ontogenetic changes towards larger preys as fishes grow have also played a fundamental role to reduce inter and intraspecific competition (Cocheret de la Moriniere et al., 2003Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, van der Velde G. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar Coast Shelf Sci [serial on the Internet]. 2003; 57(5-6):1079-89. Available from: https://doi.org/10.1016/S0272-7714(03)00011-8
https://doi.org/10.1016/S0272-7714(03)00...
; Pimentel, Joyeux, 2010Pimentel CR, Joyeux JC. Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. J Fish Biol [serial on the Internet]. 2010; 76(10): 2299-317. Available from: http://dx.doi.org/10.1111/j.1095-8649.2010.02586.x
http://dx.doi.org/10.1111/j.1095-8649.20...
; Pessanha, Araujo, 2014Pessanha ALM, Araújo FG. Shifts of the feeding niche along the size dimension of three juvenile fish species in a tidal mudflat in southeastern Brazil. Mar Biol [serial on the Internet]. 2014; 161(3):543-50. Available from: https://doi.org/10.1007/s00227-013-2356-8
https://doi.org/10.1007/s00227-013-2356-...
).

In summary, the results obtained indicate that juveniles of three lutjanid species cohabiting an estuarine lagoon share a general diet based on decapods and fishes. However, one of these species, Lutjanus novemfasciatus, has a significantly more piscivorous habit and this can be explained by a more slender body shape and larger teeth, characteristics which increase fish catching performance. Size-related changes in the proportion of food categories in the diet could not be demonstrated for any species but larger fish of all three species eat larger prey, and this ontogenetic change is consistent with the optimum foraging theory.

Acknowledgments

This study was partially supported by a COECYTJAL-UDG Project (5-2010-1-746) and a PROMEP Grant for a new fulltime professor (103.5/12/3418). Comments made by Francisco Gerson Araujo to an earlier version of the manuscript helped improve it and are highly appreciated. Special thanks to the marine biology students from the University of Guadalajara for their valuable help in the field and the lab work.

References

  • Aburto-Oropeza O, Dominguez-Guerrero I, Cota-Nieto J, Plomozo-Lugo T. Recruitment and ontogenetic habitat shifts of the yellow snapper (Lutjanus argentiventris) in the Gulf of California. Mar Biol [serial on the Internet]. 2009; 156(12):2461-72. Available from: http://dx.doi.org/10.1007/s00227-009-1271-5
    » http://dx.doi.org/10.1007/s00227-009-1271-5
  • Adams AJ, Dahlgren CP, Kellison GT, Kendall MS, Layman CA, Ley JA, Nagelkerken I, Serafy JE. Nursery function of tropical back-reef systems. Mar Ecol Prog Ser [serial on the Internet]. 2006; 318:287-301. Available from: http://www.jstor.org/stable/24870766
    » http://www.jstor.org/stable/24870766
  • Allen GR. FAO species catalogue. Rome: Food and Agriculture Organization of the United Nations; 1985. vol. 6, Snappers of the world: An annotated and illustrated catalogue of Lutjanid species known to date. (FAO Fisheries Synopsis; no. 125). Available from: http://afrilib.odinafrica.org/handle/0/15796
    » http://afrilib.odinafrica.org/handle/0/15796
  • Alonso MK, Crespo EA, García NA, Pedraza SN, Mariotti PA, Mora NJ. Fishery and ontogenetic driven changes in the diet of the spiny dogfish, Squalus acanthias, in Patagonian waters, Argentina. Environ Biol Fishes [serial on the Internet]. 2002; 63(2):193-202. Available from: https://doi.org/10.1023/A:1014229432375
    » https://doi.org/10.1023/A:1014229432375
  • Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth (UK): PRIMER-E; 2008.
  • Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA. Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert 1896). Environ Biol Fishes [serial on the Internet]. 2012; 95(1):3-20. Available from: https://doi.org/10.1007/s10641-011-9959-z
    » https://doi.org/10.1007/s10641-011-9959-z
  • Cabral-Solís EG, Espino-Barr E. Distribución y abundancia espacio-temporal de los peces en la laguna de Cuyutlán, Colima, México. Oceánides [serial on the Internet]. 2004; 19(1-2):19-27. Available from: http://oceanides.ipn.mx/index.php/cicimaroceanides/article/view/15
    » http://oceanides.ipn.mx/index.php/cicimaroceanides/article/view/15
  • Castro-Aguirre JL, Espinosa-Pérez H, Schmitter-Soto JJ. Ictiofauna estuarino-lagunar y vicaria de México. Mexico: Editorial Limusa; 1999.
  • Clarke KR, Gorley RN. PRIMER v6: User manual/Tutorial. Plymouth (UK): PRIMER-E; 2006.
  • Clarke KR, Somerfield PJ, Gorley RN. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Bio Ecol [serial on the Internet]. 2008; 366(1-2):56-69. Available from: https://doi.org/10.1016/j.jembe.2008.07.009
    » https://doi.org/10.1016/j.jembe.2008.07.009
  • Clifton KB, Motta PJ. Feeding morphology, diet, and ecomorphological relationships among five Caribbean labrids (Teleostei, Labridae). Copeia [serial on the Internet]. 1998; (4):953-66. Available from: http://www.jstor.org/stable/1447342
    » http://www.jstor.org/stable/1447342
  • Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, van der Velde G. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar Coast Shelf Sci [serial on the Internet]. 2003; 57(5-6):1079-89. Available from: https://doi.org/10.1016/S0272-7714(03)00011-8
    » https://doi.org/10.1016/S0272-7714(03)00011-8
  • Colwell RK. EstimateS: Statistical estimation of species richness and shared species from samples, Version 9. User’s Guide and application 2013. [updated 2013 Jun 14; cited 2017 Feb 7]. Available from: Available from: http://purl.oclc.org/estimates
    » http://purl.oclc.org/estimates
  • Díaz-Ruiz S, Aguirre-León A, Cano-Quiroga E. Ecological evaluation of fish community in two lagoon-estuarine systems of the south of Chiapas, Mexico. Hidrobiologica [serial on the Internet]. 2006; 16(2):197-210. Available from: http://www.scielo.org.mx/pdf/hbio/v16n2/v16n2a9.pdf
    » http://www.scielo.org.mx/pdf/hbio/v16n2/v16n2a9.pdf
  • Duarte LO, García CB. Diet of the mutton snapper Lutjanus analis (Cuvier) from the Gulf of Salamanca, Colombia, Caribbean Sea. Bull Mar Sci [serial on the Internet]. 1999; 65(2):453-65. Available from: http://www.ingentaconnect.com/content/umrsmas/bullmar
    » http://www.ingentaconnect.com/content/umrsmas/bullmar
  • Edgar GJ, Shaw C. The production and trophic ecology of shallow-water fish assemblages in southern Australia III. General relationships between sediments, seagrasses, invertebrates and fishes. J Exp Mar Bio Ecol [serial on the Internet]. 1995; 194(1):107-31. Available from: https://doi.org/10.1016/0022-0981(95)00085-2
    » https://doi.org/10.1016/0022-0981(95)00085-2
  • Figueiredo M, Morato T, Barreiros JP, Afonso P, Santos RS. Feeding ecology of the white seabream, Diplodus sargus, and the ballan wrasse, Labrus bergylta, in the Azores. Fish Res [serial on the Internet]. 2005; 75(1):107-19. Available from: https://doi.org/10.1016/j.fishres.2005.04.013
    » https://doi.org/10.1016/j.fishres.2005.04.013
  • Fischer W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem V. Rome: Food and Agriculture Organization of the United Nations ; 1995. vol. 3, Guía FAO para identificación de especies para los fines de la pesca: Pacífico centro-oriental, pt. 2, Vertebrados. Available from: http://www.fao.org/docrep/010/v6250s/v6250s00.htm
    » http://www.fao.org/docrep/010/v6250s/v6250s00.htm
  • Flores-Ortega JR, Avila-Castro E, Haro-Preciado HJ, Godínez-Domínguez E. Food habits and trophic interactions of Anisotremus interruptus (Pisces: Haemulidae) and Lutjanus argentiventris (Pisces: Lutjanidae) in the Central Mexican Pacific. Lat Am J Aquat Res [serial on the Internet]. 2014; 42(1):276-82. Available from: http://www.lajar.cl/pdf/imar/v42n1/Articulo_42_1_24.pdf
    » http://www.lajar.cl/pdf/imar/v42n1/Articulo_42_1_24.pdf
  • Flores-Ortega JR, Godínez-Domínguez E, Rojo-Vázquez JA, Corgos A, Galván-Piña VH, González-Sansón G. Interacciones tróficas de las seis especies de peces más abundantes en la pesquería artesanal en dos bahías del Pacífico Central Mexicano. Rev Biol Trop [serial on the Internet]. 2010; 58(1):383-97. Available from: https://doi.org/10.15517/rbt.v58i1.5217
    » https://doi.org/10.15517/rbt.v58i1.5217
  • Flores-Verdugo F, González-Farías F, Ramírez-Flores O, Amezcua-Linares F, Yáñez-Arancibia A, Alvarez-Rubio M, Day JW. Mangrove ecology, aquatic primary productivity, and fish community dynamics in the Teacapán-Agua Brava lagoon-estuarine system (Mexican Pacific). Estuaries [serial on the Internet]. 1990; 13(2):219-30. Available from: https://doi.org/10.2307/1351591
    » https://doi.org/10.2307/1351591
  • González-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR, Hinojosa-Larios A, Silva-Bátiz FA. Species and size composition of fishes in Barra de Navidad lagoon, Mexican central Pacific. Rev Biol Trop [serial on the Internet]. 2014a; 62(1):129-44. Available from: https://doi.org/10.15517/rbt.v62i1.10001
    » https://doi.org/10.15517/rbt.v62i1.10001
  • González-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR, Silva-Bátiz FA. Weight-length relationships for 38 fish species of Barra de Navidad coastal lagoon, Jalisco, Mexico. J Appl Ichthyol [serial on the Internet]. 2014b; 30(2):428-30. Available from: https://doi.org/10.1111/jai.12327
    » https://doi.org/10.1111/jai.12327
  • González-Sansón G, Aguilar-Betancourt C, Kosonoy-Aceves D, Lucano-Ramírez G, Ruiz-Ramírez S, Flores-Ortega JR. Spatial and temporal variations of juvenile fish abundance in Barra de Navidad coastal lagoon, Jalisco, México: Effects of hurricane Jova. Rev Biol Mar Oceanogr [serial on the Internet]. 2016; 51(1):123-36. Available from: https://doi.org/10.4067/S0718-19572016000100012
    » https://doi.org/10.4067/S0718-19572016000100012
  • Gotelli NJ, Graves GR. Null Models in Ecology. Washington (D): Smithsonian Institution Press; 1996.
  • Gotelli NJ, Entsminger GL. EcoSim: Null models software for ecologists, version 7.0. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. 2004. Available from: http://garyentsminger.com/ecosim/index.htm
    » http://garyentsminger.com/ecosim/index.htm
  • Hansson S. Methods of studying fish feeding: a comment. Can J Fish Aquat Sci [serial on the Internet]. 1998; 55(12):2706-07. Available from: https://doi.org/10.1139/f98-158
    » https://doi.org/10.1139/f98-158
  • Hugueny B, Pouilly M. Morphological correlates of diet in an assemblage of West African freshwater fishes. J Fish Biol [serial on the Internet]. 1999; 54(6):1310-25. Available from: https://doi.org/10.1111/j.1095-8649.1999.tb02057.x
    » https://doi.org/10.1111/j.1095-8649.1999.tb02057.x
  • Hyndes GA, Platell ME, Potter IC. Relationships between diet and body size, mouth morphology, habitat and movements of six sillaginid species in coastal waters: implications for resource partitioning. Mar Biol [serial on the Internet]. 1997; 128(4):585-98. Available from: https://doi.org/10.1007/s002270050125
    » https://doi.org/10.1007/s002270050125
  • Hyslop EJ. Stomach contents analysis: a review of methods and their application. J Fish Biol [serial on the Internet]. 1980; 17(4):411-29. Available from: https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
    » ttps://doi.org/10.1111/j.1095-8649.1980.tb02775.x
  • Krebs CJ. Ecological methodology, 2nd ed. San Francisco: Benjamin Cummings; 1998.
  • Lankford RR. Coastal lagoons of Mexico: their origin and classification. In: Wiley M, editor. Estuarine processes. New York: Academic Press; 1976 . p.182-215. vol. 2, Circulation, sediments, and transfer of material in the estuary.
  • Magurran AE. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.
  • Mendoza E, Castillo-Rivera M, Zárate-Hernández R, Ortiz-Burgos S. Seasonal variations in the diversity, abundance, and composition of species in an estuarine fish community in the Tropical Eastern Pacific, Mexico. Ichthyol Res [serial on the Internet]. 2009; 56(4):330-39. Available from: https://doi.org/10.1007/s10228-009-0102-5
    » https://doi.org/10.1007/s10228-009-0102-5
  • Montaña CG, Winemiller KO, Sutton A. Intercontinental comparison of fish ecomorphology: null model tests of community assembly at the patch scale in rivers. Ecol Monogr [serial on the Internet]. 2014; 84(1):91-107. Available from: https://doi.org/10.1890/13-0708.1
    » https://doi.org/10.1890/13-0708.1
  • Nanami A, Shimose T. Interspecific differences in prey items in relation to morphological characteristics among four lutjanid species (Lutjanus decussatus, L. fulviflamma, L. fulvus and L. gibbus). Environ Biol Fishes [serial on the Internet]. 2013; 96(5):591-602. Available from: https://doi.org/10.1007/s10641-012-0049-7
    » https://doi.org/10.1007/s10641-012-0049-7
  • Novakowski GC, Cassemiro FAS, Hahn NS. Diet and ecomorphological relationships of four cichlid species from the Cuibá River basin. Neotrop Ichthyol [serial on the Internet]. 2016; 14(3):150-51. Available from: http://dx.doi.org/10.1590/1982-0224-20150151
    » http://dx.doi.org/10.1590/1982-0224-20150151
  • Pessanha ALM, Araújo FG. Shifts of the feeding niche along the size dimension of three juvenile fish species in a tidal mudflat in southeastern Brazil. Mar Biol [serial on the Internet]. 2014; 161(3):543-50. Available from: https://doi.org/10.1007/s00227-013-2356-8
    » https://doi.org/10.1007/s00227-013-2356-8
  • Pessanha ALM, Araújo FG, Oliveira REM, Silva AF, Sales NS. Ecomorphology and resource use by dominant species of tropical estuarine juvenile fishes. Neotrop Ichthyol [serial on the Internet]. 2015; 13(2):401-12. Available from: http://dx.doi.org/10.1590/1982-0224-20140080
    » http://dx.doi.org/10.1590/1982-0224-20140080
  • Pianka ER. Niche overlap and diffuse competition. Proc Natl Acad Sci [serial on the Internet]. 1974; 71(5):2141-45. Available from: http://www.pnas.org/content/71/5/2141.full.pdf
    » http://www.pnas.org/content/71/5/2141.full.pdf
  • Pimentel CR, Joyeux JC. Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. J Fish Biol [serial on the Internet]. 2010; 76(10): 2299-317. Available from: http://dx.doi.org/10.1111/j.1095-8649.2010.02586.x
    » http://dx.doi.org/10.1111/j.1095-8649.2010.02586.x
  • Pouilly M, Lino F, Bretenoux JG, Rosales C. Dietary-morphological relationships in a fish assemblage of the Bolivian Amazonian floodplain. J Fish Biol [serial on the Internet]. 2003; 62(5):1137-58. Available from: http://dx.doi.org/10.1046/j.1095-8649.2003.00108.x
    » http://dx.doi.org/10.1046/j.1095-8649.2003.00108.x
  • Raborn SW, Miranda LE, Driscoll MT. Diet overlap and consumption patterns suggest seasonal flux in the likelihood for exploitative competition among piscivorous fishes. Ecol Freshw Fish [serial on the Internet]. 2004; 13(4):276-84. Available from: http://dx.doi.org/10.1111/j.1600-0633.2004.00066.x
    » http://dx.doi.org/10.1111/j.1600-0633.2004.00066.x
  • Rojas-M JR. Dieta del “pargo colorado” Lutjanus colorado (Pisces: Lutjanidae) en el Golfo de Nicoya, Costa Rica. Rev Biol Trop [serial on the Internet]. 1997; 45(3):1173-83. Available from: https://revistas.ucr.ac.cr/index.php/rbt/article/view/23864
    » https://revistas.ucr.ac.cr/index.php/rbt/article/view/23864
  • Ruiz-Nieto IC. Hábitos alimenticios de: Hoplopagrus guentherii, Lutjanus argentiventris, L. colorado, L. guttatus L. novemfasciatus y L. peru (Pisces: Lutjanidae) presentes en las costas del centro sur de Sinaloa. [MSc Thesis]. Ciudad de Mexico: Universidad Nacional Autónoma de México; 2005.
  • Santamaría-Miranda A, Saucedo-Lozano M, Herrera-Moreno MN, Apún-Molina JP. Feeding habits of Lutjanus argentiventris and Lutjanus colorado (Pisces: Lutjanidae) in the north of Sinaloa, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2005; 40(1):33-44. Available from: http://www.revbiolmar.cl/resumenes/v401/401-33.pdf
    » http://www.revbiolmar.cl/resumenes/v401/401-33.pdf
  • Saucedo-Lozano M, González-Sansón G, Chiappa-Carraza X. Natural feeding of juveniles of Lutjanus peru (Nichols and Murphy, 1922) (Lutjanidae: Perciformes) off the coast of Jalisco and Colima, Mexico. Cienc Mar [serial on the Internet]. 1999; 25(3):381-400. Available from: http://dx.doi.org/10.7773/cm.v25i3.716
    » http://dx.doi.org/10.7773/cm.v25i3.716
  • Scharf FS, Juanes F, Rountree RA. Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser [serial on the Internet]. 2000; 208:229-48. Available from: http://www.jstor.org/stable/24863819
    » http://www.jstor.org/stable/24863819
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods [serial on the Internet]. 2012; 9(7):671-75. Available from: http://dx.doi.org/10.1038/nmeth.2089
    » http://dx.doi.org/10.1038/nmeth.2089
  • StatSoft, Inc. STATISTICA [Data analysis software system], version 7.1. 2006. Available from: http://www.statsoft.com
    » http://www.statsoft.com
  • Tapia-García M, Suárez Núñez C, Cerdenares-L Guevara G, Macuitl Montes MC, Garcia Abad MC. Composición y distribución de la ictiofauna en la laguna del Mar Muerto, Pacífico Mexicano. Rev Biol Trop [serial on the Internet]. 1998; 46 (2):277-84. Available from: http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77441998000200012&lng=en&nrm=iso&tlng=es
    » http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77441998000200012&lng=en&nrm=iso&tlng=es
  • Underwood AJ. Experiments in ecology: Their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press; 1997.
  • Vázquez RI, Rodríguez J, Abitia LA, Galván F. Food habits of the yellow snapper Lutjanus argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Rev Biol Mar Oceanogr [serial on the Internet]. 2008; 43(2):295-302. Available from: http://www.revbiolmar.cl/resumenes/v432/432-295.pdf
    » http://www.revbiolmar.cl/resumenes/v432/432-295.pdf
  • Wainwright PC, Richard BA. Predicting patterns of prey use from morphology of fishes. Environ Biol Fish [serial on the Internet]. 1995; 44:97-113. Available from: https://doi.org/10.1007/978-94-017-1356-6_7
    » https://doi.org/10.1007/978-94-017-1356-6_7
  • Ward-Campbell BMS, Beamish FWH, Kongchaiya C. Morphological characteristics in relation to diet in five coexisting Thai fish species. J Fish Biol [serial on the Internet]. 2005; 67(5): 1266-79. Available from: http://dx.doi.org/10.1111/j.1095-8649.2005.00821.x
    » http://dx.doi.org/10.1111/j.1095-8649.2005.00821.x
  • Wells RJD, Cowan JH Jr, Fry B. Feeding ecology of red snapper Lutjanus campechanus in the northern Gulf of Mexico. Mar Ecol Prog Ser [serial on the Internet]. 2008; 361:213-25. Available from: http://www.jstor.org/stable/24872550
    » http://www.jstor.org/stable/24872550
  • Westneat MW. Skull biomechanics and suction feeding in fishes. In: Shadwick R, Lauder G, editors. Biomechanics. Elsevier Publishing; 2006. p.29-75. (Fish physiology series; v. 23).
  • Wittenrich ML, Rhody NR, Turingan RG, Main KL. Coupling osteological development of the feeding apparatus with feeding performance in common snook, Centropomus undecimalis, larvae: identifying morphological constraints to feeding. Aquaculture [serial on the Internet]. 2009; 294(3-4):221-27. Available from: http://doi.org/10.1016/j.aquaculture.2009.06.006
    » http://doi.org/10.1016/j.aquaculture.2009.06.006
  • Yañez-Arancibia A. Taxonomía, ecología y estructura de las comunidades de peces en las lagunas costeras con bocas efímeras del Pacífico de Mexico. Distrito Federal: Universidad Nacional Autónoma de Mexico; 1978. (Publicaciones especiales, Centro de Ciencias del Mar y Limnologia; 2).

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    09 Feb 2017
  • Accepted
    05 Nov 2017
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br