Show simple item record

Lip service: Histological phenotypes correlate with diet and feeding ecology in herbivorous pacus

dc.contributor.authorCohen, Karly E.
dc.contributor.authorLucanus, Oliver
dc.contributor.authorSummers, Adam P.
dc.contributor.authorKolmann, Matthew A.
dc.date.accessioned2023-02-01T18:59:28Z
dc.date.available2024-03-01 13:59:24en
dc.date.available2023-02-01T18:59:28Z
dc.date.issued2023-02
dc.identifier.citationCohen, Karly E.; Lucanus, Oliver; Summers, Adam P.; Kolmann, Matthew A. (2023). "Lip service: Histological phenotypes correlate with diet and feeding ecology in herbivorous pacus." The Anatomical Record 306(2): 326-342.
dc.identifier.issn1932-8486
dc.identifier.issn1932-8494
dc.identifier.urihttps://hdl.handle.net/2027.42/175791
dc.description.abstractComplex prey processing requires the repositioning of food between the teeth, as modulated by a soft tissue appendage like a tongue or lips. In this study, we trace the evolution of lips and ligaments, which are used during prey capture and prey processing in an herbivorous group of fishes. Pacus (Serrasalmidae) are Neotropical freshwater fishes that feed on leaves, fruits, and seeds. These prey are hard or tough, require high forces to fracture, contain abrasive or caustic elements, or deform considerably before failure. Pacus are gape-limited and do not have the pharyngeal jaws many bony fishes use to dismantle and/or transport prey. Despite their gape limitation, pacus feed on prey larger than their mouths, relying on robust teeth and a hypertrophied lower lip for manipulation and breakdown of food. We used histology to compare the lip morphology across 14 species of pacus and piranhas to better understand this soft tissue. We found that frugivorous pacus have larger, more complex lips which are innervated and folded at their surface, while grazing species have callused, mucus-covered lips. Unlike mammalian lips or tongues, pacu lips lack any intrinsic skeletal or smooth muscle. This implies that pacu lips lack dexterity; however, we found a novel connection to the primordial ligament which suggests that the lips are actuated by the jaw adductors. We propose that pacus combine hydraulic repositioning of prey inside the buccal cavity with direct oral manipulation, the latter using a combination of a morphologically heterodont dentition and compliant lips for reorienting food.
dc.publisherJohn Wiley & Sons, Inc.
dc.subject.othertongues
dc.subject.otherproboscis
dc.subject.otherprey manipulation
dc.subject.otherhistology
dc.subject.otherchewing
dc.titleLip service: Histological phenotypes correlate with diet and feeding ecology in herbivorous pacus
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biology
dc.subject.hlbtoplevelHealth Sciences
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175791/1/ar25075-sup-0003-supinfo_3.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175791/2/ar25075.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/175791/3/ar25075_am.pdf
dc.identifier.doi10.1002/ar.25075
dc.identifier.sourceThe Anatomical Record
dc.identifier.citedreferencePelicice, F. M., Agostinho, A. A., & Thomaz, S. M. ( 2006 ). Fish assemblages associated with Egeria in a tropical reservoir: investigating the effects of plant biomass and diel period. Acta Oecologica, 27 ( 1 ), 9 – 16.
dc.identifier.citedreferenceOwen-Smith, R. N. ( 1975 ). The social ethology of the white rhinoceros Ceratotherium simum (Burchell 1817). Zeitschrift für Tierpsychologie, 38, 337 – 384.
dc.identifier.citedreferencePeterson, R. D., Sullivan, J. P., Hopkins, C. D., Santaquiteria, A., Dillman, C. B., Pirro, S., Betancur-R, R., Arcila, D., Hughes, L. C., & Ortí, G. ( 2022 ). Phylogenomics of bony-tongue fishes (Osteoglossomorpha) shed light on the craniofacial evolution and biogeography of the weakly electric clade (Mormyridae). Systematic Biology, 71, syac001.
dc.identifier.citedreferencePereira, P. R., Agostinho, C. S., Oliveira, R. J. D., & Marques, E. E. ( 2007 ). Trophic guilds of fishes in sandbank habitats of a Neotropical river. Neotropical Icthyolofy, 5, 399 – 404.
dc.identifier.citedreferencePrudente, B. D. S., Carneiro-Marinho, P., Valente, R. D. M., & Montag, L. F. D. A. ( 2016 ). Feeding ecology of Serrasalmus gouldingi (Characiformes: Serrasalmidae) in the lower Anapu River region, eastern Amazon, Brazil. Acta Amazonica, 46, 259 – 270.
dc.identifier.citedreferenceRamos, T. P. A., Maia, J. S., Costa, S. Y. L., Silva, M. J., Avellar, R. C., & Silva, L. O. ( 2018 ). Continental ichthyofauna from the Paraíba do Norte River basin pre-transposition of the São Francisco River, Northeastern Brazil. Biota Neotropica, 18, 1 – 13.
dc.identifier.citedreferenceRevell, L. J. ( 2012 ). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217 – 223.
dc.identifier.citedreferenceRoss, C. F., Eckhard, A., Herrel, A., Hylander, W. L., Metzger, K. A., Schaerlaeken, V., Washington, R. L., & Williams, S. H. ( 2007 ). Modulation of intra-oral processing in mammals and lepidosaurs. Integrative and Comparative Biology, 47, 118 – 136.
dc.identifier.citedreferenceSasko, D. E., Dean, M. N., Motta, P. J., & Hueter, R. E. ( 2006 ). Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus. Zoology, 109, 171 – 181.
dc.identifier.citedreferenceSazima, I. ( 1986 ). Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities. Journal of Fish Biology, 29, 53 – 65.
dc.identifier.citedreferenceSchaefer, S. A., & Lauder, G. V. ( 1986 ). Historical transformation of functional design: Evolutionary morphology of feeding mechanisms in loricarioid catfishes. Systematic Zoology, 35, 489 – 508.
dc.identifier.citedreferenceSchwarz, D., Konow, N., Roba, Y. T., & Heiss, E. ( 2020 ). A salamander that chews using complex, three-dimensional mandible movements. Journal of Experimental Biology, 223 ( 5 ), jeb220749. https://doi.org/10.1242/jeb.220749
dc.identifier.citedreferenceShellis, R. P., & Berkovitz, B. K. B. ( 1976 ). Observations on the dental anatomy of piranhas (Characidae) with special reference to tooth structure. Journal of Zoology, 180, 69 – 84.
dc.identifier.citedreferenceShoshani, J. ( 1998 ). Understanding proboscidean evolution: A formidable task. Trends in Ecology & Evolution, 13, 480 – 487.
dc.identifier.citedreferenceSilva, G., Moreira, A., & Alves, J. ( 2011 ). Histological processing of teeth and periodontal tissues for light microscopy analysis. Methods in Molecular Biology (Clifton, N.J.), 689, 19 – 36.
dc.identifier.citedreferenceSilva-Camacho, D. D. S., Santos, J. N. D. S., Gomes, R. D. S., & Araújo, F. G. ( 2014 ). Ecomorphological relationships among four Characiformes fish species in a tropical reservoir in South-eastern Brazil. Zoologia (Curitiba), 31 ( 1 ), 28 – 34.
dc.identifier.citedreferenceSuzuki, R., & Shimodaira, H. ( 2006 ). Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540 – 1542.
dc.identifier.citedreferenceThompson, A. W., Betancur-R, R., López-Fernández, H., & Ortí, G. ( 2014 ). A time-calibrated, multi-locus phylogeny of piranhas and pacus (Characiformes: Serrasalmidae) and a comparison of species tree methods. Molecular Phylogenetics and Evolution, 81, 242 – 257.
dc.identifier.citedreferenceTripathi, P., & Mittal, A. K. ( 2010 ). Essence of keratin in lips and associated structures of a freshwater fish Puntius sophore in relation to its feeding ecology: Histochemistry and scanning electron microscope investigation. Tissue and Cell, 42, 223 – 233.
dc.identifier.citedreferenceVander Wall, S. B., Longland, W. S., Pyare, S., & Veech, J. A. ( 1997 ). Cheek pouch capacities and loading rates of heteromyid rodents. Oecologia, 113, 21 – 28.
dc.identifier.citedreferenceVieira, I., & Gery, J. ( 1979 ). Differential growth and nutrition in Catoprion mento (Characoidei). Scale-eating fish of Amazonia. Acta Amazonica, 9, 143 – 146.
dc.identifier.citedreferenceWang, S., Li, L., Sun, W., Wainwright, D., Wang, H., Zhao, W., Chen, B., Chen, Y., & Wen, L. ( 2020 ). Detachment of the remora suckerfish disc: Kinematics and a bio-inspired robotic model. Bioinspiration & Biomimetics, 15, 056018.
dc.identifier.citedreferenceWinemiller, K. O. ( 1989 ). Development of dermal lip protuberances for aquatic surface respiration in south American characid fishes. Copeia, 1989, 382 – 390.
dc.identifier.citedreferenceWitmer, L. M., Sampson, S. D., & Solounias, N. ( 1999 ). The proboscis of tapirs (Mammalia: Perissodactyla): A case study in novel narial anatomy. Journal of Zoology, 249, 249 – 267.
dc.identifier.citedreferenceAldous, S. E. ( 1941 ). Food habits of chipmunks. Journal of Mammalogy, 22 ( 1 ), 18 – 24.
dc.identifier.citedreferenceAlexander, R. M. ( 1964 ). Adaptation in the skulls and cranial muscles of south American characinoid fish. Zoological Journal of the Linnean Society, 45, 169 – 190.
dc.identifier.citedreferenceAlexander, R. McN. (1967). The functions and mechanisms of the protrusible upper jaws of some acanthopterygian fish. Journal of Zoology, 151 ( 1 ), 43 – 64. https://doi.org/10.1111/j.1469-7998.1967.tb02865.x
dc.identifier.citedreferenceAndrade, M. C., Jégu, M., & Giarrizzo, T. ( 2016 ). Tometes kranponhah and Tometes ancylorhynchus (Characiformes: Serrasalmidae), two new phytophagous serrasalmids, and the first Tometes species described from the Brazilian shield. Journal of Fish Biology, 89, 467 – 494.
dc.identifier.citedreferenceAndrade, M. C., Fitzgerald, D. B., Winemiller, K. O., Barbosa, P. S., & Giarrizzo, T. ( 2019 a). Trophic niche segregation among herbivorous serrasalmids from rapids of the lower Xingu River. Brazilian Amazon. Hydrobiologia, 829, 265 – 280.
dc.identifier.citedreferenceAndrade, M. C., Winemiller, K. O., Barbosa, P. S., Fortunati, A., Chelazzi, D., Cincinelli, A., & Giarrizzo, T. ( 2019 b). First account of plastic pollution impacting freshwater fishes in the Amazon: Ingestion of plastic debris by piranhas and other serrasalmids with diverse feeding habits. Environmental Pollution, 244, 766 – 773.
dc.identifier.citedreferenceAnker, G. C. ( 1974 ). Morphology and kinetics of the head of the stickleback, Gasterosteus aculeatus. Transactions of the Zoological Society of London, 32, 311 – 416.
dc.identifier.citedreferenceBarlow, G. W., & Munsey, J. W. ( 1976 ). The Red Devil-Midas-Arrow Cichlid Species Complex in Nicaragua. In: Thorson TV, (Ed.), Investigations of the icthyofauna of Nicaraguan lakes. Lincoln, NB: School of Life Science, Univesity of Nebraska. 359–369.
dc.identifier.citedreferenceBaumgarten, L., Machado-Schiaffino, G., Henning, F., & Meyer, A. ( 2015 ). What big lips are good for: On the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes. Biological Journal of the Linnean Society, 115, 448 – 455.
dc.identifier.citedreferenceBelovsky, G. E., & Schmitz, O. J. ( 1994 ). Plant defenses and optimal foraging by mammalian herbivores. Journal of Mammalogy, 75, 816 – 832.
dc.identifier.citedreferenceBenjamin, M. ( 1986 ). The oral sucker of Gyrinocheilus aymonieri (Teleostei: Cypriniformes). Journal of Zoology, 1 ( 2 ), 211 – 254.
dc.identifier.citedreferenceBerkovitz, B. K. B. ( 1975 ). Observations on tooth replacement in piranhas (Characidae). Archives of Oral Biology, 20, 53 – IN7.
dc.identifier.citedreferenceBetancur, R. R., Arcila, D., Vari, R. P., Hughes, L. C., Oliveira, C., Sabaj, M. H., & Ortí, G. ( 2019 ). Phylogenomic incongruence, hypothesis testing, and taxonomic sampling: The monophyly of characiform fishes. Evolution, 73, 329 – 345.
dc.identifier.citedreferenceBurress, E. D. ( 2015 ). Cichlid fishes as models of ecological diversification: Patterns, mechanisms, and consequences. Hydrobiologia, 748, 7 – 27.
dc.identifier.citedreferenceBuser, T. J., Boyd, O. F., Cortés, Á., Donatelli, C. M., Kolmann, M. A., Luparell, J. L., Pfeiffenberger, J. A., Sidlauskas, B. L., & Summers, A. P. ( 2020 ). The natural historian’s guide to the CT galaxy: Step-by-step instructions for preparing and analyzing computed tomographic (CT) data using cross-platform, open access software. Integrative Organismal Biology, 2, obaa009.
dc.identifier.citedreferenceCarvalho, L. N., dos Santos Júnior, J. B., & Correa, S. B. ( 2021 ). Uncovering mechanisms of seed predation by fish. Biotropica, 202, 1460 – 1464.
dc.identifier.citedreferenceChristy, R. M., & Maie, T. ( 2019 ). Adhesive force and endurance during waterfall climbing in an amphidromous gobiid, Sicyopterus japonicus (Teleostei: Gobiidae): Ontogenetic scaling of novel locomotor performance. Zoology, 133, 10 – 16.
dc.identifier.citedreferenceCohen, K. E., Crawford, C. H., Hernandez, L. P., Beckert, M., Nadler, J. H., & Flammang, B. E. ( 2020 ). Sucker with a fat lip: The soft tissues underlying the viscoelastic grip of remora adhesion. Journal of Anatomy, 237, 643 – 654.
dc.identifier.citedreferenceCorrea, S. B., Araujo, J. K., Penha, J. M., da Cunha, C. N., Stevenson, P. R., & Anderson, J. T. ( 2015 ). Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands. Biological Conservation, 191, 159 – 167.
dc.identifier.citedreferenceCorrea, S. B., & Winemiller, K. O. ( 2014 ). Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology, 95, 210 – 224.
dc.identifier.citedreferenceCorrea, S. B., Winemiller, K. O., Lopez-Fernandez, H., & Galetti, M. ( 2007 ). Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience, 57, 748 – 756.
dc.identifier.citedreferenceCullen, J. A., Maie, T., Schoenfuss, H. L., & Blob, R. W. ( 2013 ). Evolutionary novelty versus exaptation: Oral kinematics in feeding versus climbing in the waterfall-climbing Hawaiian goby Sicyopterus stimpsoni. PLoS One, 8, e53274.
dc.identifier.citedreferenceDary, E. P., Ferreira, E., Zuanon, J., & Röpke, C. P. ( 2017 ). Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotropical Ichthyology, 15, e160173.
dc.identifier.citedreferenceDatovo, A., & Castro, R. M. ( 2012 ). Anatomy and evolution of the mandibular, hyopalatine, and opercular muscles in characiform fishes (Teleostei: Ostariophysi). Zoology, 115, 84 – 116.
dc.identifier.citedreferenceDatovo, A., & Vari, R. P. ( 2014 ). The jaw adductor muscle complex in teleostean fishes: Evolution, homologies and revised nomenclature (Osteichthyes: Actinopterygii). PLoS One, 8, e60846.
dc.identifier.citedreferenceDe Meyer, J., & Geerinckx, T. ( 2014 ). Using the whole body as a sucker: Combining respiration and feeding with an attached lifestyle in hill stream loaches (Balitoridae, Cypriniformes). Journal of Morphology, 275, 1066 – 1079.
dc.identifier.citedreferenceDean, M. N., Wilga, C. D., & Summers, A. P. ( 2005 ). Eating without hands or tongue: Specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes. Biology Letters, 1, 357 – 361.
dc.identifier.citedreferenceDoosey, M. H., & Bart, H. L., Jr. ( 2011 ). Morphological variation of the palatal organ and chewing pad of catostomidae (Teleostei: Cypriniformes). Journal of Morphology, 272, 1092 – 1108.
dc.identifier.citedreferenceFerreira, F. S., Vicentin, W., Costa, F. E. D. S., & Súarez, Y. R. ( 2014 ). Trophic ecology of two piranha species, Pygocentrus nattereri and Serrasalmus marginatus (Characiformes, Characidae), in the floodplain of the Negro River, Pantanal. Acta Limnologica Brasiliensia, 26, 381 – 391.
dc.identifier.citedreferenceFeilich, K. L., Laurence-Chasen, J. D., Orsbon, C., Gidmark, N. J., & Ross, C. F. ( 2021 ). Twistand chew: three-dimensional tonguekinematics during chewing in macaqueprimates. Biology Letters, 17, 20210431.
dc.identifier.citedreferenceFratzl, P. ( 2008 ). Collagen: Structure and mechanics, an introduction. In P. Fratzl (Ed.), Collagen: Structure and mechanics (pp. 1 – 13 ) Springer US.
dc.identifier.citedreferenceFroese, R. & Pauly, D. ( 2014 ). Fish Base. World Wide Web Electronic Publication. http://www.fishbase.org
dc.identifier.citedreferenceGeerinckx, T., Brunain, M., Herrel, A., Aerts, P., & Adriaens, D. ( 2007 ). A head with a suckermouth: A functional-morphological study of the head of the suckermouth armoured catfish Ancistrus cf. triradiatus (Loricariidae, Siluriformes). Belgian Journal of Zoology, 137, 47.
dc.identifier.citedreferenceGintof, C., Konow, N., Ross, C. F., & Sanford, C. P. ( 2010 ). Rhythmic chewing with oral jaws in teleost fishes: A comparison with amniotes. Journal of Experimental Biology, 213, 1868 – 1875.
dc.identifier.citedreferenceGonzález, N., & Vispo, C. ( 2003 ). Aspects of the diet and feeding ecologies of fish from nine floodplain lakes of the lower Caura, Venezuelan Guayana. Scientia Guaianae, 12, 329 – 323.
dc.identifier.citedreferenceGosline, W. A. ( 1986 ). Jaw muscle configuration in some higher teleostean fishes. Copeia, 1986, 705 – 713.
dc.identifier.citedreferenceGoulding, M. ( 1980 ). The fishes and the forest: Explorations in Amazonian natural history. University of California Press.
dc.identifier.citedreferenceGoulding, M., & Carvalho, M. L. ( 1982 ). Life history and management of the tambaqui ( Colossoma macropomum, Characidae): An important Amazonian food fish. Revista Brasileira de Zoologia, 1, 107 – 133.
dc.identifier.citedreferenceGrubich, J. R., Huskey, S., Crofts, S., Ortí, G., & Porto, J. ( 2012 ). Mega-bites: Extreme jaw forces of living and extinct piranhas (Serrasalmidae). Scientific Reports, 2, 1009.
dc.identifier.citedreferenceHanley, M. E., Lamont, B. B., Fairbanks, M. M., & Rafferty, C. M. ( 2007 ). Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics, 27, 157 – 178.
dc.identifier.citedreferenceHeinsohn, G. E., & Spain, A. V. ( 1974 ). Effects of a tropical cyclone on littoral and sub-littoral biotic communities and on a population of Dugongs (Dugong dugon (Müller)). Biological Conservation, 6, 43 – 152.
dc.identifier.citedreferenceHiiemae, K. M., & Palmer, J. B. ( 2003 ). Tongue movements in feeding and speech. Critical Reviews in Oral Biology & Medicine, 14, 413 – 429.
dc.identifier.citedreferenceHonda, E. M. S. ( 1974 ). Contribuicão ao conhecimento da biologia de peixesdo Amazonas: II. Alimentacão do tambaqui, Colossoma bidens. Acta Amazonica, 4, 47 – 53.
dc.identifier.citedreferenceHuertas, V., & Bellwood, D. R. ( 2017 ). Mucus-secreting lips offer protection to suction-feeding corallivorous fishes. Current Biology, 27, R406 – R407.
dc.identifier.citedreferenceHuie, J. M., Summers, A. P., & Kolmann, M. A. ( 2019 ). Body shape separates guilds of rheophilic herbivores (Myleinae: Serrasalmidae) better than feeding morphology. Proceedings of the Academy of Natural Sciences of Philadelphia, 166, 1 – 15.
dc.identifier.citedreferenceIrish, F. J. ( 1987 ). Analysis of design in the feeding apparatus of snakes and fishes. [Doctoral dissertation, Harvard University, Cambridge Massachusetts]. ProQuest Dissertations Publishing.
dc.identifier.citedreferenceKier, W. M., & Smith, K. ( 1985 ). Tongues, tentacles and trunks: The biomechanics of movement in muscular-hydrostats. Zoological journal of the Linnean Society, 83, 307 – 324.
dc.identifier.citedreferenceKolmann, M. A., Cohen, K. E., Bemis, K. E., Summers, A. P., Irish, F. J., & Hernandez, L. P. ( 2019 ). Tooth and consequences: Heterodonty and dental replacement in piranhas and pacus (Serrasalmidae). Evolution & Development, 20, e12306.
dc.identifier.citedreferenceKolmann, M. A., Hughes, L. C., Hernandez, L. P., Arcila, D., Betancur-R, R., Sabaj, M. H., López-Fernández, H., & Ortí, G. ( 2021 ). Phylogenomics of piranhas and pacus (Serrasalmidae) uncovers how dietary convergence and parallelism obfuscate traditional morphological taxonomy. Systematic Biology, 70, 576 – 592.
dc.identifier.citedreferenceKolmann, M. A., Huie, J. M., Evans, K., & Summers, A. P. ( 2018 ). Specialized specialists and the narrow niche fallacy: A tale of scale-feeding fishes. Royal Society Open Science, 5, 171581.
dc.identifier.citedreferenceKolmann, M. A., Welch, K. C., Summers, A. P., & Lovejoy, N. R. ( 2016 ). Always chew your food: Freshwater stingrays use mastication to process tough insect prey. Proceedings of the Royal Society B: Biological Sciences, 283 ( 1838 ), 20161392. https://doi.org/10.1098/rspb.2016.1392
dc.identifier.citedreferenceLegendre, P., & Anderson, M. J. ( 1999 ). Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments. Ecological Monographs, 69, 1 – 24.
dc.identifier.citedreferenceLeite, R. G., & Jégu, M. ( 1990 ). Food habits of two species of Acnodon (Characiformes, Serrasalmidae) and scale-eating habits of Acnodon normani. Cybium, 14, 353 – 360.
dc.identifier.citedreferenceLeuthold, W. ( 1977 ). African ungulates: A comparative review of their ethology and behavioral ecology. Springer, Springer-Verlag.
dc.identifier.citedreferenceLomax, J. J., & Brainerd, E. L. ( 2020 Mar). Comparative Skeletal Kinematics of Overbite-Shearing and Compressive Chewing Cycles in a Pacu Fish, Piaractus brachypomus. In Integrative and comparative biology (Vol. 60, pp. E143 – E143 ).
dc.identifier.citedreferenceLucas, C. M. ( 2008 ). Within Flood Season Variation in Fruit Consumption and Seed Dispersal by Two Characin Fishes of the Amazon. Biotropica, 40 ( 5 ), 581 – 589. https://doi.org/10.1111/j.1744-7429.2008.00415.x
dc.identifier.citedreferenceLucas, P. W., Turner, I. M., Dominy, N. J., & Yamashita, N. ( 2000 ). Mechanical defences to herbivory. Annals of Botany, 86, 913 – 920.
dc.identifier.citedreferenceLujan, N. K., & Armbruster, J. W. ( 2012 ). Morphological and functional diversity of the mandible in suckermouth armored catfishes (Siluriformes: Loricariidae). Journal of Morphology, 273, 24 – 39.
dc.identifier.citedreferenceLumsden, A. G. S., & Osborn, J. W. ( 1977 ). The evolution of chewing: A dentist’s view of palaeontology. Journal of Dentistry, 5, 269 – 287.
dc.identifier.citedreferenceMachado-Allison, A. ( 1985 ). Studies on the subfamily Serrasalminae, part III. On the generic status and phylogenetic relationships of the genera Pygopristis, Pygocentrus, Pristobrycon, and Serrasalmus (Teleostei-Characidae-Serrasalminae). Acta Biologica Venezuela, 12, 19 – 42.
dc.identifier.citedreferenceMachado-Schiaffino, G., Henning, F., & Meyer, A. ( 2014 ). Species-specific differences in adaptive phenotypic plasticity in an ecologically relevant trophic trait: Hypertrophic lips in Midas cichlid fishes. Evolution, 68, 2086 – 2091.
dc.identifier.citedreferenceMaie, T., Meister, A. B., Leonard, G. L., Schrank, G. D., Blob, R. W., & Schoenfuss, H. L. ( 2011 ). Jaw muscle fiber type distribution in Hawaiian gobioid stream fishes: Histochemical correlations with feeding ecology and behavior. Zoology, 114, 340 – 347.
dc.identifier.citedreferenceMateussi, N. T., Melo, B. F., Ota, R. P., Roxo, F. F., Ochoa, L. E., Foresti, F., & Oliveira, C. ( 2020 ). Phylogenomics of the Neotropical fish family Serrasalmidae with a novel intrafamilial classification (Teleostei: Characiformes). Molecular Phylogenetics and Evolution, 153, 106945.
dc.identifier.citedreferenceMérona, B., Santos, G., & Almeida, R. ( 2001 ). Short term effects of Tucuruí Dam (Amazonia, Brazil) on the trophic organization of fish communities. Environmental Biology of Fishes, 60, 375 – 392. https://doi.org/10.1023/A:1011033025706
dc.identifier.citedreferenceMurtagh, F., & Legendre, P. ( 2014 ). Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? Journal of Classification, 31 ( 3 ), 274 – 295.
dc.identifier.citedreferenceNico LG. 1991. Trophic ecology of piranhas (Characidae: Serrasalminae) from savanna and forest regions in the Orinoco River basin of Venezuela. Ph.D. dissertation, Univ. of Florida, Gainesville.
dc.identifier.citedreferenceNico, L. G., & Taphorn, D. C. ( 1988 ). Food habits of piranhas in the low llanos of Venezuela. Biotropica, 20, 311 – 321.
dc.identifier.citedreferenceOlson, R. A., Montuelle, S. J., Chadwell, B. A., Curtis, H., & Williams, S. H. ( 2021 ). Jaw kinematics and tongue protraction–retraction during chewing and drinking in the pig. Journal of Experimental Biology, 224, 724 – 734.
dc.identifier.citedreferenceOsse, J. W. M. ( 1969 ). Functional morphology of the head of the perch ( Perca fluviatilis L.): An electromyographic study. Netherlands Journal of Zoology, 19, 289 – 392.
dc.working.doiNOen
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.