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Trophic Ecomorphology of Cichlid Fishes of Selva Lacandona, Usumacinta, Mexico

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Trophic Ecomorphology of Cichlid Fishes of Selva Lacandona, Usumacinta, Mexico Environ Biol Fish https://doi.org/10.1007/s10641-019-00884-5 Trophic ecomorphology of cichlid fishes of Selva Lacandona, Usumacinta, Mexico Miriam Soria-Barreto & Rocío Rodiles-Hernández & Kirk O. Winemiller Received: 1 October 2018 /Accepted: 14 May 2019 # Springer Nature B.V. 2019 Abstract Neotropical cichlids exhibit great diversi- invertebrates and/or fish), with detritivores repre- ty of morphological traits associated with feeding, sented by relatively few species and strict piscivore by locomotion, and habitat use. We examined the one species. Dietary overlap was highest among carni- relationship between functional traits and diet by vores (P. friedrichsthalii and T. salvini), herbivores analyzing a dataset for 14 cichlid species from rivers in (C. intermedium and C. pearsei) and detritivore- the Selva Lacandona region, Usumacinta Basin, Chia- herbivores (V. melanura and K. ufermanni). Dietary pas, Mexico. Volumetric proportions of ingested food components were strongly correlated with several mor- items were used to calculate diet breath and interspecific phological traits, confirming patterns observed in other dietary overlap. Morphometric analysis was performed cichlids. For example, jaw protrusion and mandible using 24 traits associated with feeding. Associations length were positively correlated with consumption of between morphological and dietary components were fish and terrestrial invertebrates. A longer gut and a assessed using canonical correspondence analysis. wider tooth plate on the lower pharyngeal jaw were The most common feeding guilds were omnivore, correlated with ingestion of vegetation, algae and detri- herbivore and carnivore (the latter consuming tus. Findings confirmed a high degree of trophic spe- cialization in certain species as well as interspecific Electronic supplementary material The online version of this divergence of functional traits associated with feeding article (https://doi.org/10.1007/s10641-019-00884-5) contains among cichlids of the Usumacinta Basin, which is con- supplementary material, which is available to authorized users. sistent with the idea that Middle American cichlids represent an adaptive radiation. M. Soria-Barreto (*) Departamento de Conservación de la Biodiversidad, CONACYT-El Colegio de la Frontera Sur (ECOSUR), Carretera Keywords Cichlidae . Diet breadth . Diet overlap . Panamericana y Periférico Sur s/n, Barrio María Auxiliadora, San Functional ecology. Morphometrics . Neotropics Cristóbal de Las Casas, Chiapas, Mexico e-mail: [email protected] R. Rodiles-Hernández Introduction Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur (ECOSUR), Carretera Panamericana y Periférico Sur s/n, Barrio María Auxiliadora, San Cristóbal de Las Casas, Ecomorphology has been used to test hypotheses in Chiapas, Mexico community ecology based on the assumption that mor- phological traits that influence organism performance K. O. Winemiller Department of Wildlife and Fisheries Sciences and Program in can reveal ecological patterns and insights into ecolog- Ecology and Evolutionary Biology, Texas A&M University, ical processes. Ecomorphology has been used to infer College Station, TX, USA factors influencing adaptive divergence of lineages Environ Biol Fish (Streelman et al. 2002; Price et al. 2011; Arbour and León 2005). Modifications of oral and pharyngeal jaws, López-Fernández 2013), community assembly from lo- as well as cranial configuration and musculature, are cal to regional scales (Ricklefs and Miles 1994;Poff associated with dietary preference and feeding modes 1997; Micheli and Halpern 2005), and community re- (Burress 2015, 2016; Rican et al. 2016). Although most sponse to environmental change (Villéger et al. 2010). cichlid diets are diverse, species have been grouped into Research on freshwater fish communities has trophic guilds, including piscivores that possess relative- established strong correlations between traits and func- ly specialized morphological traits for capture and in- tion, principally with regard to habitat use and feeding gestion of fish, and omnivores with more variable or (Gatz 1979; Watson and Balon 1984; Hugueny and intermediate traits and generalized diets (Barel 1983; Pouilly 1999), including biomechanical and experimen- Liem 1991;Burress2016). Description of the relation- tal studies of performance (Wainwright and Bellwood ship between morphology and diet is an essential step 2002;Hulseyetal.2005;Wainwrightetal.2007). for understanding factors shaping cichlid diversifica- Separation of species within functional trait space has tion, community assembly and species coexistence. been interpreted as evidence of niche segregation in Here we investigate the trophic ecomorphology of response to environmental filtering and present or past the cichlid assemblage in the Tzendales River within the competition (Wikramanayake 1990; Winemiller 1991; Selva Lacandona region of the upper Usumacinta Basin, Montaña et al. 2014). Morphological diversification the largest in Mesoamerica (De la Maza and Carabias among closely related taxa is often cited as evidence 2011). Fifteen native cichlid species inhabit the region’s for competition and other kinds of species interactions rivers and streams (Rodiles-Hernández et al. 1999; as agents influencing adaptive evolution and patterns of Lozano-Vilano et al. 2007; Soria-Barreto and Rodiles- species coexistence (Winemiller et al. 1995;Arbourand Hernández 2008) and support important artisanal fish- López-Fernández 2013). eries (Carabias et al. 2015). Based on findings from Cichlids are freshwater fishes distributed in Africa, studies of other cichlid faunas, we hypothesized strong Central and South America, the West Indies, Madagas- correspondence between function traits and diets as well car, Israel, Syria, India and Sri Lanka. Globally and as ecomorphological differentiation among species con- regionally, cichlids reveal impressive morphological, sistent with niche partitioning and adaptive radiation. behavioral and ecological diversity (Nelson et al. 2016), and this diversity often has been described as an adaptive radiation (Burress 2015). Cichlids are par- Methods ticularly diverse in Mesoamerica where they are domi- nant components of most local fish assemblages Study area (Hulsey et al. 2004; Matamoros et al. 2015). Studies of cichlids from different regions of Mesoamerica have Selva Lacandona is a region of approximately exhibited similar patterns of morphological diversity 1,300,000 ha within the Usumacinta Basin in Chiapas, based on sets of traits associated with feeding and hab- Mexico. The region’s annual mean temperature ranges itat use (Winemiller et al. 1995; Soria-Barreto and from 19 to 26 °C and annual precipitation varies be- Rodiles-Hernández 2008; Cochran-Biederman and tween 1890 and 4300 mm. The region contains several Winemiller 2010; Montaña and Winemiller 2013;Rican protected areas, the most important and largest of which et al. 2016; Pease et al. 2018). are the Montes Azules and Lacantun biosphere reserves. Trophic morphology appears to have been key to These areas contain rainforest and rivers that support adaptive radiation for many groups like Darwin’s some of the highest biodiversity in Mesoamerica (De la finches, Anolis lizards (Streelman and Danley 2003) Maza and Carabias 2011;Carabiasetal.2015). and teleosts such as reef fish (Wainwright and Cichlids were collected from diverse habitats of the Bellwood 2002) and African rift-lake cichlids Tzendales River within the Montes Azules Reserve (16° (Streelman and Danley 2003;Kocher2004). In Meso- 16′ 08″ to 16° 19′ 08^ N; 90° 53′ 06″ to 90° 59′ 44^ W) american cichlids, for example, feeding performance is using seines, gill nets, cast nets and baited hooks. Fish strongly influenced by jaw protrusion that allows pred- were collected during dry season from February to ators to capture evasive prey, such as fish and shrimp May 2006. Specimens were fixed in 10% formalin for (Waltzek and Wainwright 2003;HulseyandGarcíade five days and then rinsed in water and stored in 70% Environ Biol Fish ethanol. Formalin preservation can cause shrinkage of based on the standardized Levin’sindex,BA=[(1/Σ 2 fish specimens (Parker 1963), but here we assume that pjj ) - 1)] / (n-1), where pjj is the proportion of items i in distortion from preservation was minor and, given that the diet for species j, and n is total number of items all specimens were treated in the same way, inter- considered (Krebs 1998). Trophic niche overlap was specific comparisons of morphology should be largely computed for every possible species pairing using 2 2 unbiased. Fourteen cichlid species were captured Pianka’sindex,Oik = Σ (pij ∗ pik)/(√ Σ pij ∗ pik ) (Online Resource 1); only adult size classes were in- for species j and k and diet categories i =1ton (Krebs cluded in the analysis to avoid allometric effects associ- 1998). To assess the statistical significance of overlap, ated with ontogeny. We chose specimens larger than we performed a null model test with 1000 iterations minimum size of first maturity reported by Chávez- using the RA3 algorithm in the EcosimR package Lomelí et al. (1988); Konings (1989); and Miller et al. (Gotelli et al. 2015). (2005). Specimens were deposited in the Fish Collection of El Colegio de la Frontera Sur, Chiapas, Mexico. Morphometric analysis Dietary analysis Morphometric data were obtained from 20 specimens of each species (Table 1), including the same specimens Dietary analysis was performed based on examination used
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