Trophic Ecomorphology Of Cichlid Fishes Of Selva Lacandona .
Environ Biol hic ecomorphology of cichlid fishes of SelvaLacandona, Usumacinta, MexicoMiriam Soria-BarretoKirk O. Winemiller&Rocío Rodiles-Hernández &Received: 1 October 2018 / Accepted: 14 May 2019# Springer Nature B.V. 2019Abstract Neotropical cichlids exhibit great diversity of morphological traits associated with feeding,locomotion, and habitat use. We examined therelationship between functional traits and diet byanalyzing a dataset for 14 cichlid species from rivers inthe Selva Lacandona region, Usumacinta Basin, Chiapas, Mexico. Volumetric proportions of ingested fooditems were used to calculate diet breath and interspecificdietary overlap. Morphometric analysis was performedusing 24 traits associated with feeding. Associationsbetween morphological and dietary components wereassessed using canonical correspondence analysis.The most common feeding guilds were omnivore,herbivore and carnivore (the latter consumingElectronic supplementary material The online version of thisarticle (https://doi.org/10.1007/s10641-019-00884-5) containssupplementary material, which is available to authorized users.M. Soria-Barreto (*)Departamento de Conservación de la Biodiversidad,CONACYT-El Colegio de la Frontera Sur (ECOSUR), CarreteraPanamericana y Periférico Sur s/n, Barrio María Auxiliadora, SanCristóbal de Las Casas, Chiapas, Mexicoe-mail: mmsoriab@gmail.comR. Rodiles-HernándezDepartamento de Conservación de la Biodiversidad, El Colegio dela Frontera Sur (ECOSUR), Carretera Panamericana y PeriféricoSur s/n, Barrio María Auxiliadora, San Cristóbal de Las Casas,Chiapas, MexicoK. O. WinemillerDepartment of Wildlife and Fisheries Sciences and Program inEcology and Evolutionary Biology, Texas A&M University,College Station, TX, USAinvertebrates and/or fish), with detritivores represented by relatively few species and strict piscivore byone species. Dietary overlap was highest among carnivores (P. friedrichsthalii and T. salvini), herbivores(C. intermedium and C. pearsei) and detritivoreherbivores (V. melanura and K. ufermanni). Dietarycomponents were strongly correlated with several morphological traits, confirming patterns observed in othercichlids. For example, jaw protrusion and mandiblelength were positively correlated with consumption offish and terrestrial invertebrates. A longer gut and awider tooth plate on the lower pharyngeal jaw werecorrelated with ingestion of vegetation, algae and detritus. Findings confirmed a high degree of trophic specialization in certain species as well as interspecificdivergence of functional traits associated with feedingamong cichlids of the Usumacinta Basin, which is consistent with the idea that Middle American cichlidsrepresent an adaptive radiation.Keywords Cichlidae . Diet breadth . Diet overlap .Functional ecology . Morphometrics . NeotropicsIntroductionEcomorphology has been used to test hypotheses incommunity ecology based on the assumption that morphological traits that influence organism performancecan reveal ecological patterns and insights into ecological processes. Ecomorphology has been used to inferfactors influencing adaptive divergence of lineages
Environ Biol Fish(Streelman et al. 2002; Price et al. 2011; Arbour andLópez-Fernández 2013), community assembly from local to regional scales (Ricklefs and Miles 1994; Poff1997; Micheli and Halpern 2005), and community response to environmental change (Villéger et al. 2010).Research on freshwater fish communities hasestablished strong correlations between traits and function, principally with regard to habitat use and feeding(Gatz 1979; Watson and Balon 1984; Hugueny andPouilly 1999), including biomechanical and experimental studies of performance (Wainwright and Bellwood2002; Hulsey et al. 2005; Wainwright et al. 2007).Separation of species within functional trait space hasbeen interpreted as evidence of niche segregation inresponse to environmental filtering and present or pastcompetition (Wikramanayake 1990; Winemiller 1991;Montaña et al. 2014). Morphological diversificationamong closely related taxa is often cited as evidencefor competition and other kinds of species interactionsas agents influencing adaptive evolution and patterns ofspecies coexistence (Winemiller et al. 1995; Arbour andLópez-Fernández 2013).Cichlids are freshwater fishes distributed in Africa,Central and South America, the West Indies, Madagascar, Israel, Syria, India and Sri Lanka. Globally andregionally, cichlids reveal impressive morphological,behavioral and ecological diversity (Nelson et al.2016), and this diversity often has been described asan adaptive radiation (Burress 2015). Cichlids are particularly diverse in Mesoamerica where they are dominant components of most local fish assemblages(Hulsey et al. 2004; Matamoros et al. 2015). Studies ofcichlids from different regions of Mesoamerica haveexhibited similar patterns of morphological diversitybased on sets of traits associated with feeding and habitat use (Winemiller et al. 1995; Soria-Barreto andRodiles-Hernández 2008; Cochran-Biederman andWinemiller 2010; Montaña and Winemiller 2013; Ricanet al. 2016; Pease et al. 2018).Trophic morphology appears to have been key toadaptive radiation for many groups like Darwin’sfinches, Anolis lizards (Streelman and Danley 2003)and teleosts such as reef fish (Wainwright andBellwood 2002) and African rift-lake cichlids(Streelman and Danley 2003; Kocher 2004). In Mesoamerican cichlids, for example, feeding performance isstrongly influenced by jaw protrusion that allows predators to capture evasive prey, such as fish and shrimp(Waltzek and Wainwright 2003; Hulsey and García deLeón 2005). Modifications of oral and pharyngeal jaws,as well as cranial configuration and musculature, areassociated with dietary preference and feeding modes(Burress 2015, 2016; Rican et al. 2016). Although mostcichlid diets are diverse, species have been grouped intotrophic guilds, including piscivores that possess relatively specialized morphological traits for capture and ingestion of fish, and omnivores with more variable orintermediate traits and generalized diets (Barel 1983;Liem 1991; Burress 2016). Description of the relationship between morphology and diet is an essential stepfor understanding factors shaping cichlid diversification, community assembly and species coexistence.Here we investigate the trophic ecomorphology ofthe cichlid assemblage in the Tzendales River within theSelva Lacandona region of the upper Usumacinta Basin,the largest in Mesoamerica (De la Maza and Carabias2011). Fifteen native cichlid species inhabit the region’srivers and streams (Rodiles-Hernández et al. 1999;Lozano-Vilano et al. 2007; Soria-Barreto and RodilesHernández 2008) and support important artisanal fisheries (Carabias et al. 2015). Based on findings fromstudies of other cichlid faunas, we hypothesized strongcorrespondence between function traits and diets as wellas ecomorphological differentiation among species consistent with niche partitioning and adaptive radiation.MethodsStudy areaSelva Lacandona is a region of approximately1,300,000 ha within the Usumacinta Basin in Chiapas,Mexico. The region’s annual mean temperature rangesfrom 19 to 26 C and annual precipitation varies between 1890 and 4300 mm. The region contains severalprotected areas, the most important and largest of whichare the Montes Azules and Lacantun biosphere reserves.These areas contain rainforest and rivers that supportsome of the highest biodiversity in Mesoamerica (De laMaza and Carabias 2011; Carabias et al. 2015).Cichlids were collected from diverse habitats of theTzendales River within the Montes Azules Reserve (16 16′ 08″ to 16 19′ 08 N; 90 53′ 06″ to 90 59′ 44 W)using seines, gill nets, cast nets and baited hooks. Fishwere collected during dry season from February toMay 2006. Specimens were fixed in 10% formalin forfive days and then rinsed in water and stored in 70%
Environ Biol Fishethanol. Formalin preservation can cause shrinkage offish specimens (Parker 1963), but here we assume thatdistortion from preservation was minor and, given thatall specimens were treated in the same way, interspecific comparisons of morphology should be largelyunbiased. Fourteen cichlid species were captured(Online Resource 1); only adult size classes were included in the analysis to avoid allometric effects associated with ontogeny. We chose specimens larger thanminimum size of first maturity reported by ChávezLomelí et al. (1988); Konings (1989); and Miller et al.(2005). Specimens were deposited in the Fish Collectionof El Colegio de la Frontera Sur, Chiapas, Mexico.based on the standardized Levin’s index, BA [(1 / Σpjj 2) - 1)] / (n-1), where pjj is the proportion of items i inthe diet for species j, and n is total number of itemsconsidered (Krebs 1998). Trophic niche overlap wascomputed for every possible species pairing usingPianka’s index, Oik Σ (pij pik) / ( Σ pij 2 pik 2)for species j and k and diet categories i 1 to n (Krebs1998). To assess the statistical significance of overlap,we performed a null model test with 1000 iterationsusing the RA3 algorithm in the EcosimR package(Gotelli et al. 2015).Dietary analysisMorphometric data were obtained from 20 specimens ofeach species (Table 1), including the same specimensused for diet analysis. Twenty-four traits associated withfeeding were measured using calipers with precision to0.1 mm (Table 2). The lower pharyngeal jaw was extracted and stained with alizarin solution before takinglinear measurements. We measured the gut length ofeach specimen after extracting and uncurling the entiregastrointestinal tract.All morphological measurements were log transformed to increase normality. Size correction was performed by linear regression of each measure againststandard length. Principal components analysis (PCA)based on the correlation matrix was performed to ordinate species according to dominant gradients of morphological variation. Morphological traits with highestloadings were selected for use as variables to performcanonical correspondence analysis (CCA). Spearmancorrelation was performed with these morphologicaltraits; large significant correlations were indicative offunctional redundancy, and redundant traits were eliminated prior to performing CCA. Canonical correspondence analysis was performed to evaluate associationsbetween dietary and morphological variables, with statistical significance of ordination axes assessed based on999 random permutations. Multivariate analyses wereperformed with the vegan package (Oksanen et al. 2009)in R version 3.3.1 (R Core Team 2016).Dietary analysis was performed based on examinationof stomachs of 30 specimens per species, except toP. friedrichsthalli for which 28 specimens were available (Table 1). The ingested items were analyzed usingthe volumetric method described by Hyslop (1980) andWinemiller (1990). Estimates of the volume of recovered food items were obtained by water displacement ina graduate cylinder or, for very small items, by visualcomparison with a water droplet of determined volume.Food items were removed from the anterior portion ofgut and were identified using the keys in Merritt andCummins (1996) and Springer et al. (2010). Somestomachs were empty or with high level of digestion,and these were not considered in our sample sizes. Toverify that sample sizes were sufficient to describe dietary variation, accumulation curves for trophic diversitywere plotted for each species using the EstimateS software (Colwell 2013; Online Resources 2). To facilitateinterspecific comparisons, food items were grouped according to seven broad categories: detritus, aquatic insect larvae (AIL) (Coleoptera, Diptera, Hemiptera, Lepidoptera, Tricoptera, Odonata), terrestrial invertebrates(Coleoptera, Hemiptera, Formicidae, arachnids), algae,mollusks (Bivalvia and Gastropoda), fish (complete,fragments and scales) and vegetation material (VM)(including seeds). These categories describe basictrophic niches and better facilitate exploration ofrelationships between morphology and diet by reducing the frequency of zeros in the data matrix.For each diet item for each species, data wererecorded as the percentage of the total volumesummed for all diet items. Proportional volumetricdiet data were used to compute niche breadthMorphometric analysisResultsThe first two PCA axes explained 54.9% of total morphological variation among cichlids (Table 3). Largepositive loadings on PC1 were associated with
Environ Biol FishTable 1 Number of specimens examined and standard length ranges (SL in mm) for cichlid species from the Tzendales River, SelvaLacandona, Chiapas, MexicoSpeciesAbbreviationMorphometricsDiet analysisChuco intermediumCi20 (200.9–103.9)30 (200.9–91.4)Cincelichthys pearseiCp20 (236.7–111.3)30 (236.7–111.3)Kihnichthys ufermanniKu20 (208–107.2)30 (208–82.8)Maskaheros argenteusMa20 (224.9–92.2)30 (209.5–83.3)Parachromis friedrichsthaliiPf20 (193.8–104.7)28 (193.8–104.7)Petenia splendidaPs20 (232.5–109.4)30 (247.2–116.3)Rheoheros lentiginosusRl20 (138.3–91.3)30 (138.3–52.2)Theraps irregularisTi20 (179.4–112.9)30 (190–94.8)Thorichthys helleriTh20 (106.7–71.7)30 (106.7–63.7)Thorichthys meekiTm20 (102.7–44.7)30 (102.7–44.7)Trichromis salviniTs20 (118.5–72)30 (109.4–64.5)Vieja bifasciataVb20 (192.9–87.3)30 (198.3–77)Vieja melanuraVm20 (182–142.5)30 (182–95.2)Wajpamheros nourissatiWn20 (202–136.6)30 (202–103.1)subterminal mouths, large guts and an obtuse snoutangle; negative loadings were associated with long firstceratobranchial and epibranchial arches and large heads.PC2 separated fish with longer mandibles, longer upperjaws, and greater jaw protrusibility (positive loadings)from those with a wider tooth plate on the lower pharyngeal jaw, wider lower pharyngeal jaw and an obtusesnout angle (negative loadings) (Fig. 1, Table 3). Tworheophilic species, Theraps irregularis and Rheoheroslentiginosus, were distinguished by having subterminalmouths, long guts and snouts with an obtuse angle.Petenia splendida had the longest upper jaw and mandible, longest head, greatest jaw protrusion, and a superiorly positioned mouth. Parachromis friedrichsthalii,Trichromis salvini and Wajpamheros nourissati weresimilar to P. splendida in many respects, and alsohave long first ceratobranchial and epibranchialarches. Chuco intermedium, Cincelichthys pearsei,Kihnichthys ufermanni, Maskaheros argenteus,Vieja bifasciata and V. melanura have a broadtooth plate on the lower pharyngeal jaw, a widelower pharyngeal jaw, obtuse snout angle, long gutand subterminal mouth. Thorichthys meeki andThorichthys helleri were similar to species in thisgroup in many traits.Dietary analysis indicated that P. splendida consumed fish almost exclusively, T. salvini andP. friedrichsthalii consumed mostly aquatic insects andfish, T. irregularis fed on aquatic insects and algae, andR. lentiginosus consumed a combination of mollusksand aquatic insects. Vegetation material dominated thediets of C. pearsei and C. intermedium, K. ufermanniand V. melanura consumed a combination of vegetationmaterial and detritus, and V. bifasciata consumed vegetation material, detritus and algae. W. nourissati andM. argenteus fed on plant material and aquatic invertebrates. Thorichthys helleri and T. meeki both consumedaquatic invertebrates, with the former having a greaterdietary fraction of mollusks. These benthivorous fishesalso consumed large fractions of detritus, which likelywas ingested incidentally during winnowing of sediment and food within the orobranchial chamber(López-Fernández et al. 2014). Diet breadth was highestfor omnivorous M. argenteus (0.41) and T. helleri (0.37)and herbivorous V. bifasciata (0.37); in contrast, thepiscivore P. splendida had lowest diet breadth (0.03)(Table 4).Diet overlap was high between the carnivoresT. salvini and P. friedrichsthalii. High overlap also wasobserved between the herbivores C. intermedium andC. pearsei, the detritivore-herbivores V. melanura andK. ufermanni, and among certain pairs of herbivorous,detritivores-herbivorous and omnnivorous cichlids(V. melanura and C. intermedium; V. melanura andV. bifasciata; M. argenteus and W. nourissati;K. ufermanni and V. bifasciata) (Table 5). Overlapvalues were significantly higher than expected basedon randomized simulations (p 0.001), the average
Environ Biol FishTable 2 Morphological traits measured in cichlids from Selva LacandonaMeasurementsDescriptionStandard lengthMeasured from the tip of upper lip to the origin of the caudal fin (Barel et al. 1977).Head lengthMeasured from the tip of the upper lip with the mouth completely closed to the caudal edge of theoperculum (Gatz 1979; Winemiller 1991).Head heightVertical distance measured through the center of the eye, between the dorsal and ventral edges ofthe head (Gatz 1979; Winemiller 1991).Head widthMeasured from the left to right preorbital bone (Barel et al. 1977)Eye diameterHorizontal distance between the anterior and posterior edges of the eye (Gatz 1979; Winemiller 1991).Snout lengthDistance from the anterior edge of the orbit to the center the upper lip (Winemiller 1991).Upper jaw lengthMeasured from the tip of the snout to posterior corner of maxilla.Mandible lengthDistance measured from the lower tip of mandible to caudal tip of retroarticular process(Barel et al. 1977).Gape widthDistance horizontal internal between the tips of the premaxilla with the mouth fully open andprotruded (Gatz 1979).Cheek depthDistance vertical from ventral margin of preopercule to margin ventral of eye (Barel et al. 1977).Eye positionVertical distance between the center of the eye and the ventral edge of the head (Gatz 1979;Winemiller 1991).Jaw protrusionDistance from the anterior edge of the orbit to the center the upper lip, when the mouth fullyprotruded (Gatz 1979).Snout angleIn lateral view, the angle between the dorsal outline of premaxillary and line along the ventralborder of the lower jaw (Barel et al. 1977).Mouth positionEstimate by drawing a horizontal line that passes from the corner of the mouth to the middle ofthe insertion of caudal rays in the caudal peduncle. Other line is traced from anterior-mostpoint of the orbit, and another corresponding to the tip of the upper lip. The angle between thetwo lines is measured with a protractor (Gatz 1979; Winemiller 1991).Length of first ceratobranchial archDistance between join of ceratobranchial with basibranchial to the join to ceratobranchial withepibranchial (Cochran-Biederman and Winemiller 2010).Length of epibranchial archDistance between of the epibranchial in the first arch.Distance between gillrakersAverage distance between gillrakers of first ceratobranchial arch (Cochran-Biederman andWinemiller 2010).Gillraker widthWith of gillrakers in the first ceratobranchial arch (Cochran-Biederman and Winemiller 2010).Gillraker heightAverage distance from the base to the tip of gillrakers in the first ceratobranchial arch(Cochran-Biederman and Winemiller 2010).Lower pharyngeal jaw widthDistance measured between the tips of the horns (Barel et al. 1977; Trapani 2003).Length of lower pharyngeal jawDistance of the symphysis measured from the anterior tip to posterior center of the plate(Barel et al. 1977; Trapani 2003).Width of the tooth plate on the lowerpharyngeal jawDistance between the lateral margins of the tooth plate, of the most lateral left and right(Barel et al. 1977; Trapani 2003).Length of the tooth plate on the lowerpharyngeal jawDistance of tooth plate at symphysis, measured from the rostral to caudal margin(Barel et al. 1977; Trapani 2003).Gut lengthLength of entire digestive tract from esophagus to anus (Gatz 1979; Winemiller 1991).observed index was 0.45 and average index calculatedby null model was 0.38.CCA revealed a statistically significant relationshipbetween morphology and diet (p 0.001). The first axisexplained 40.5% of variance and the second axis explained 21.7%. The first axis was strongly influenced byan association between mandible length, jaw protrusion,length of first ceratobranchial arch and head length andthe consumption of fish and terrestrial invertebrates(high loadings for carnivorous P. splendida, P.friedrichsthalii and T. salvini) and an association between an obtuse snout angle and subterminal mouth
Environ Biol FishTable 3 Factor loadings (eigenvalues) for the first two dimensionsfrom principal components analysis of morphometrics of cichlidsfrom Selva Lacandona. Abbreviations are in parenthesis. Morphological traits used in subsequent correlation analysis are in boldPCAaxis 1PCAaxis 2Eigenvalue7.5995.033Variance explained33.0%21.9%Head length 1.5200.492Head height 0.394 1.234Morphological variableHead width 0.263 1.151Eye diameter 0.653 0.163Snout length0.032 0.227Upper jaw length 1.4531.003Mandible length 1.4640.939Gape width 1.4860.033Cheek depth 0.784 0.409Eye position 0.576 1.080Jaw protrusion 0.5930.757Snout angle0.743 1.353Mouth position1.214 0.869Length of first ceratobranquialarch (LCA)Length of epibranchial arch (LEA) 1.6580.254 1.509 0.335Distance between gillrakers 0.770 0.753Gillraker width 1.4170.112Gillraker height 1.1250.182Width of lower pharyngeal jaw (WLPJ) 0.925 1.310Length of lower pharyngeal jaw (LLPJ) 1.179 1.069Width of tooth plate on lowerpharyngeal jaw (WTLPJ)Length of the tooth plate on the lowerpharyngeal plate (LTLPJ)Gut length (Gut L) 0.705 1.477 1.201 1.0740.798 0.998and consumption of vegetation, algae and detritus withdetritivorous and herbivorous cichlids. The secondCCA axis was strongly influenced by an association between gut length and wide tooth plate onthe lower jaw with consumption of vegetation,algae and detritus. Herbivores (C. pearsei, C.intermedium, V. bifasciata) and detritivore-herbivores(K. ufermanni, V. melanura) had longest guts, and species that consumed mostly invertebrates (aquatic and/orterrestrial) had shorter guts (R. lentiginosus, T. helleri,M. argenteus, W. nourissati, P. friedrichsthalli, T. salviniand T. irregularis) (Fig. 2).DiscussionCichlids of Selva Lacandona exhibited extensive interspecific differences in morphological traits known toinfluence foraging and processing of ingestedfoods. Assemblage trophic diversity and patternsof trait-diet association were very consistent withthose reported from ecomorphological studies ofother Neotropical cichlid faunas (e.g., CochranBiederman and Winemiller 2010; López-Fernándezet al. 2013; Montaña and Winemiller 2013; Ricanet al. 2016; Pease et al. 2018).Jaw protrusion and the length of the head mandible,and first ceratobranchial arch were correlated with consumption of fish and terrestrial invertebrates. In carnivorous fishes, head length and mouth gape tend to becorrelated prey size (Gatz 1979; Watson and Balon1984; Hugueny and Pouilly 1999; López-Fernándezet al. 2013). Longer mandibles and first ceratobranchialarches can enhance suction feeding by piscivores andzooplanktivores (Barel 1983). Jaw protrusion is correlated with piscivory in other Neotropical cichlids(Cochran-Biederman and Winemiller 2010; Montañaand Winemiller 2013; Pease et al. 2018). Functionalmorphology research has shown that that jaw protrusionpaired with a large oro-branchial chamber volume increases efficiency of suction feeding in teleosts (Barel1983; Liem 1991). In cichlids, as in other teleost fishes,the premaxilla and maxilla undergo rotational movements that enhances jaw protrusion and suction(Westneat 2005). Our result confirmed that Peteniasplendida has extremely protrusible jaws and long mandibles that should facilitate both suction feeding onelusive prey, mainly fish (Barel 1983; Waltzek andWainwright 2003; Hulsey and García de León 2005).Similar functional traits and feeding habits are observedin P. friedrichsthalii and T. salvini.A strong association was found between longer guts,wider tooth plates on the pharyngeal jaws and an obtusesnout angle and consumption of vegetation, algae anddetritus by herbivores (C. pearsei, C. intermedium andV. bifasciata) and detritivore-herbivores (K. ufermanni,V. melanura). Long gastrointestinal tracts in detritivoresand herbivores and shortest guts in carnivores apparently is a robust relationship among freshwater fishes (Gatz1979; Winemiller et al. 1995; Hugueny and Pouilly1999; Pease et al. 2018). A longer intestine facilitatesdigestion and absorption of plant material, which tendsto be less nutritious and more recalcitrant than animal
Environ Biol FishFig. 1 PCA ordination of Selva Lacandona cichlids based on morphological traits associated with feeding. Circles represent means forspecies and abbreviations are in Table 1Table 4 Proportional dietary composition of food items and diet breadth (standardized Levin’s index) for cichlids from Selva LacandonaAlgaeMollusksAquaticinsect 20.120.410.270.03SpeciesnVegetationmaterialChuco intermedium300.66Cincelichthys pearsei300.80Kihnichthys ufermanni300.43Maskaheros argenteus270.410.250.19Parachromis friedrichsthalii250.060.050.56Petenia splendida28Rheoheros lentiginosus300.02Theraps irregularis170.080.22Thorichthys helleri280.050.030.230.21Thorichthys meeki300.010.210.030.160.02Trichromis salvini230.010.700.28Vieja bifasciata290.360.250.05Vieja melanura300.450.05Wajpamheros 0.570.250.010.340.370.030.420.260.070.370.12
Environ Biol FishTable 5 Interspecific dietary overlap among cichlids from Selva 0.61TiThTmTsVbVmtissue (Kramer and Bryant 1995). The correlation between snout angle and herbivory and detritivory likelyreflects feeding behavior, because these fishes eitherscrape or bite and tear tufts epilithic algae fromsubstrates. Compact jaws (i.e., small mouth gape, shortupper jaw and mandibles, less jaw protrusion, obtusesnout angle) facilitate strong biting force (Liem 1991).Molluscivores also had relatively short heads and bluntFig. 2 CCA ordination of cichlid species from Selva Lacandona based on morphology and diet; abbreviations are explained in Tables 1 and3 and methods section. Vectors portray correlations of morphological variables with axis 1 and 2
Environ Biol Fishsnouts, traits likely associated with muscle attachmentand mechanics for crushing shells within the pharyngealjaws (Barel 1983; Wainwright 1987; Hulsey et al. 2005;Burress 2016).Mouth orientation tends to be associated with bothdiet and the position within the water column wherefeeding takes place (Keast and Webb 1966; Gatz 1979;Wikramanayake 1990). For example, Petenia splendidahas a superior positioned mouth that should facilitatefeeding on prey positioned higher in the water column,P. friedrichsthalii and T. salvini have terminal mouthsthat should facilitate capture of prey at the same verticalposition, and R. lentiginosus and T. irregularis havesubterminal mouths that permit them to forage onsubstrates while maintaining position in flowingwater. A wide pharyngeal tooth plate was associated with herbivory and detritivory. Although notanalyzed here, interspecific differences in dentitionof pharyngeal jaws were noted. In cichlids, theshape and dentition of pharyngeal jaws have shown tobe plastic in response to diet (Huysseune 1995; Trapani2003; Muschick et al. 2011) and genetic effects(Fruciano et al. 2016). The plasticity of pharyngeal jawsis considered an adaptation that facilitates exploitationof diverse food resources and a significant contributor tothe trophic diversification of cichlids in Africa (Meyer1987) and the Neotropics (Trapani 2003; Burress 2015,2016; Rican et al. 2016).Some cichlids from Selva Lacandona have morphology and diets that are convergent with cichlids fromSouth America and other regions of Central America.Petenia splendida has are specialized piscivores(Chávez-Lomelí et al. 1988; Cochran-Biederman andWinemiller 2010; Pease et al. 2018) with traits similarto those described for piscivorous cichlids in the SouthAmerican genera Cichla, Crenicichla (LópezFernández et al. 2012; Montaña and Winemiller 2013)and Caquetaia (Winemiller et al. 1995; Rican et al.2016) and the Central American piscivore Parachromisdovii (Winemiller et al. 1995). Thorichthys helleri andT. meeki are benthic feeders that use winnowing toseparate invertebrate prey from sediments in a mannerconvergent with behavioral patterns observed in theSouth American cichlid genera Geophagus andSatanaperca species (López-Fernández et al. 2012,2014). The invertebrate feeders R. lentiginosus andT. irregularis that inhabit fast-flowing riffles (SoriaBarreto and Rodiles-Hernández 2008) are quite similarmorphologically and ecologically to rheophilicHypsophrys and Tomocichla species in southern CentralAmerica (Rican et al. 2016).In contrast with cichlid assemblages in South American that tend to be dominated by the invertivore guild(López-Fernández et al. 2012; Montaña and Winemiller2013), the Selva Lacandona cichlid assemblage hasmany omnivorous and herbivorous species. These cichlids would be considered trophic generalist (Montañaand Winemiller 2013), because they had broad dietsconsisting mostly of vegetation, algae and detritus butincluding aquatic insects. These cichlids had high dietary overlap, which suggests a potential for competitionunder conditions of food resource limitation and orability to switch to alternative food resources as availabilities shift. Coexistence of species with simil
Trophic ecomorphology of cichlid fishes of Selva Lacandona, Usumacinta, Mexico Miriam Soria-Barreto & Rocío Rodiles-Hernández & Kirk O.
Feeding ecology and ecomorphology of cichlid assemblages in a large Mesoamerican river delta Allison A. Pease & Manuel Mendoza-Carranza& Kirk O. Winemiller Received: 17 August 2017/Acce
A general account of commercially Important fishes and Shell fishes. 4.1 Fresh Water Fishes 4.2 Brackish water fishes 4.3 Shell-fishes 4.4 Marine fishes 35 5. Different methods of fishing in Fresh water 5.1 Hooks & Lines used in fishing 5.2 Di
with cichlid origins prior to Gondwanan landmass frag-mentation 121-165 MYA, considerably earlier than the first known cichlid fossils from Eocene [5]. Cichlid fishes found in the lakes of Africa have served as model systems
Vocabulary Trophic Level: The position an organism occupies in a food chain. Trophic levels are often represented by numbers, starting at level 1 with primary producers such as plants. Further trophic levels are numbered subsequently according to how far the organism is along the food chain.
6 Algebraic and Discrete Mathematical Methods for Modern Biology TABLE S2.1 Solution to Exercise 2.2 Species Trophic Level (Shortest Path) Shark 3 Sea otter 2 Sea stars 2 Sea urchins 1 Abalone 1 Large crabs 2 Smaller predatory fishes 2 Small (herbivorous) fishes and invertebrates 1 Kelp 0 Large fishes and octopus 2 Sessile invertebrates 1 .
Class - Osteichthyes 1. Class Osteichthyes includes all bony fishes. Like all fishes, Osteichthyes are cold-blooded vertebrates that breathe through gills and use fins for swimming. Bony fishes share several distinguishing features: a skeleton of bone, scales, paired fins,
applied in ecotoxicological studies for the estimation of trophic . baseline δ15N, or individual . refs 18 and 19. Thus, a focus on assessing uncertainty and variability in bioaccumulation models, e.g., refs 20 and 21, is needed for reducing uncertainty in TMF estimates while incorporating variability in these factors. However, most TMF
Studi Pendidikan Akuntansi secara keseluruhan adalah sebesar Rp4.381.147.409,46. Biaya satuan pendidikan (unit cost) pada Program Studi Akuntansi adalah sebesar Rp8.675.539,42 per mahasiswa per tahun. 2.4 Kerangka Berfikir . Banyaknya aktivitas-aktivitas yang dilakukan Fakultas dalam penyelenggaraan pendidikan, memicu biaya-biaya dalam penyelenggaraan pendidikan. Biaya dalam pendidikan .
