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Ecomorphology and evolution of the pharyngeal apparatus of benthic damselfishes (Pomacentridae, subfamily Stegastinae)

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Abstract

Coral and rocky reefs are productive and complex habitats that favor niche partitioning, the appearance of functional and morphological uniqueness in their inhabitants, and diversification. Members of the damselfish (Pomacentridae) subfamily Stegastinae, with 8 genera and 66 species, are among the most common inhabitants of reefs. Feeding behavior tends to be similar for most members of this subfamily, as they are benthic species that aggressively protects their feeding areas. Their main food sources are algae and invertebrates, but they also feed opportunistically on a wider range of resources. In this study, I analyzed the morphology of the pharyngeal jaw apparatus in an ecological and phylogenetic context to understand the role of these structures in promoting functional capacity and/or diversification. I found variation in the number and morphology of teeth, particularly in the lower pharyngeal jaw. The presence or absence of hard-shelled items in the diet appears to be a factor shaping the evolution of the pharyngeal jaw apparatus. Finally, the pharyngeal plates in the subfamily Stegastinae are highly diverse, reflecting specialization in processing particular prey items.

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References

  • Aguilar-Medrano R, Barber P (2016) Ecomorphological diversification in reef fish of the genus Abudefduf (Percifomes, Pomacentridae). Zoomorphology 135:103–114

    Article  Google Scholar 

  • Aguilar-Medrano R, Frédérich B, De Luna E, Balart EF (2011) Patterns of morphological evolution of the cephalic region in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Biol J Linn Soc 102:593–613

    Article  Google Scholar 

  • Aguilar-Medrano R, Frédérich B, Balart EF, De Luna E (2013) Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Zoomorphology 132:197–213

    Article  Google Scholar 

  • Aguilar-Medrano R, Kobelkowsky A, Balart EF (2015) Anatomical description of the Cortés damselfish Stegastes rectifraenum (Perciformes:Pomacentridae). Key structures for omnivore feeding. Rev Mex Biodivers 86:934–946

    Article  Google Scholar 

  • Allen GR (1991) Damselfishes of the world. Aquariums Systems, Mentor

    Google Scholar 

  • Allen GR, Robertson DR (1994) Fishes of the Tropical Eastern Pacific. University of Hawaii Press, Honolulu

    Google Scholar 

  • Allen GR, Woods LP (1980) A review of the damselfish genus Stegastes from the Eastern Pacific with description of a new species. Rec Aus Mus 8:171–198

    Google Scholar 

  • Angel A, Ojeda PF (2001) Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Mar Ecol Prog Series 217:81–91

    Article  Google Scholar 

  • Barneche DR, Floeter SR, Ceccarelli DM, Frensel DMB, Dinslaken DF, Mário HFS (2009) Feeding macroecology of territorial damselfishes (Perciformes: Pomacentridae). Mar Biol 156:289–299

    Article  Google Scholar 

  • Baum DA, Allan L (1991) Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Syst Biol 40(1):1–18

    Article  Google Scholar 

  • Bazzaz FA (1975) Plant species diversity in old-field successional ecosystems in southern Illinois. Ecology 56(2):485–488

    Article  Google Scholar 

  • Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fish 28(1):189–214

    Article  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. University Press, Cambridge

    Google Scholar 

  • Burress ED, Duarte A, Serra WS, Loureiro M (2015) Rates of piscivory predict pharyngeal jaw morphology in a piscivorous lineage of cichlid fishes. Ecol Freshw Fish. doi:10.1111/eff.12236

    Google Scholar 

  • Casciotta JR, Arratia G (1993) Jaws and teeth of American cichlids (Pisces: Labroidei). J Morphol 217:1–36

    Article  Google Scholar 

  • Cervigón F (1993) Los peces marinos de Venezuela, vol 2. Fundación Científica Los Roques, Caracas, Venezuela

    Google Scholar 

  • Choat JH, Bellwood DR (1998) Wrasses and parrotfishes. In: Paxton JR, Eschmeyer WN (eds) Encyclopedia of animals:fishes. Academic Press, San Diego, pp 209–213

    Google Scholar 

  • Ciardelli A (1967) The anatomy of the feeding mechanism and the food habits of Microspathodon chrysurus (Pisces: Pomacentridae). Bull Mar Sci 17:843–883

    Google Scholar 

  • Cooper WJ, Smith LL, Weastneat MW (2009) Exploring the radiation of a diverse reef fish family: phylogenetics of the damselfishes (Pomacentridae), with new classifications based on molecular analyses of all genera. Mol Phyl Evol 52:1–16

    Article  Google Scholar 

  • Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63(6):1802–1813

    Article  Google Scholar 

  • Davis JC (1986) Statistics and data analysis in geology. Wiley, New York

    Google Scholar 

  • Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:209–221

    Google Scholar 

  • Dromard CR, Bouchon-Navaroa Y, Cordonniera S, Fontaineb M-F, Verlaqueb M, Harmelin-Vivienb M, Bouchona C (2013) Resource use of two damselfishes, Stegastes planifrons and Stegastes adustus, on Guadeloupean reefs (Lesser Antilles): inference from stomach content and stable isotope analysis. J Exp Mar Biol Ecol 440:116–125

    Article  Google Scholar 

  • Emery AR (1973) Comparative ecology and functional osteology of fourteen species of damselfish (Pisces: Pomacentridae) at Alligator Reef, Florida Keys. Bull Mar Sci 23:649–770

    Google Scholar 

  • Eschmeyer WN, Fricke R, van der Laan R (2016) Catalog of fishes: genera, species, references. (http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Accessed Jun 2016

  • Espinoza M, Salas E (2005) Estructura de las comunidades de peces de arrecife en las Islas Catalinas y Playa Ocotal, Pacífico Norte de Costa Rica. Rev Biol Trop 53:523–536

    Article  Google Scholar 

  • Fraser RH, Currie DJ (1996) The species richness-energy hypothesis in a system where historical factors are thought to prevail: coral reefs. Am Nat 148(1):138–159

    Article  Google Scholar 

  • Frédérich B, Pilet A, Parmentier E, Vandewalle P (2008) Comparative trophic morphology in eight species of damselfishes (Pomacentridae). J Morphol 269:175–188

    Article  Google Scholar 

  • Frédérich B, Fabri G, Lepoint G, Vandewalle P, Parmentier E (2009) Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Recif of Toliara, Madagascar. Ichthyol Res 56:10–17

    Article  Google Scholar 

  • Frédérich B, Sorenson L, Santini F, Slater GJ, Alfaro ME (2013) Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). Am Nat 181:94–113

    Article  Google Scholar 

  • Frédérich B, Cooper WJ, Aguilar-Medrano R (2016) Ecomorphology and iterative ecological radiation of damselfishes. In: Frédérich B, Parmentier E (eds) Biology of damselfishes. CRC Press, Florida, pp 184–203

    Chapter  Google Scholar 

  • Froese R, Pauly D (2016) FishBase: concepts, design and data sources. ICLARM, Los Baños, Laguna. http://www.fishbase.org. Accessed May 2016

  • Galis F (2001) Key innovations and radiations. In: Wagner GP (ed) The character concept in evolutionary biology. Academic Press, San Diego, pp 581–605

    Chapter  Google Scholar 

  • Galis F, Drucker EG (1996) Pharyngeal biting mechanics in centrarchid and cichlid fishes: insights into a key evolutionary innovation. J Evol Biol 9:641–670

    Article  Google Scholar 

  • Gluckmann I, Vandewalle P (1998) Morphofunctional analysis of the feeding apparatus in four Pomacentridae species: Dascyllus aruanus, Chromis retrofasciata, Chrysiptera biocellata and C. unimaculata. Ital J Zool 65:421–424

    Article  Google Scholar 

  • Grove JG, Lavenberg RJ (1997) The fishes of the Galapagos Islands. Stanford University Press, Stanford, California

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: palentological statistics software package for education and data analysis. Palaeontolia Electronica 4(1):9. http://folk.uio.no/ahammer/past

  • Hellig CJ, Kerschbaumer M, Sefc KM, Koblmüller S (2010) Allometric shape change of the lower pharyngeal jaw correlates with a dietary shift to piscivory in a cichlid fish. Naturwissenschaften 97(7):663–672

    Article  CAS  Google Scholar 

  • Hixon MA (1981) An experimental analysis of territoriality in the California reef fish Embiotoca jacksoni (Embiotocidae). Copeia 1981:653–665

    Article  Google Scholar 

  • Hobson ES (1965) Diurnal-nocturnal activity of some inshore fishes in the Gulf of California. Copeia 1965:291–302

    Article  Google Scholar 

  • Hoogerhoud RJC (1986) The adverse effects of shell ingestion for molluscivorous cichlids, a constructional morphological approach. Neth J Zool 37(3):277–300

    Article  Google Scholar 

  • Hulsey CD (2006) Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw. Proc R Soc B 273:669–675

    Article  Google Scholar 

  • Huysseune A (1995) Phenotypic plasticity in the lower pharyngeal jaw dentition of Astatoreochromis alluaudi (teleostei: cichlidae). Arch Oral Biol 40(11):1005–1014

    Article  CAS  Google Scholar 

  • Kaufman LS, Liem KF (1982) Fishes of the suborder Labroidei (Pisces: Perciformes): phylogeny, ecology and evolutionary significance. Breviora 472:1–19

    Google Scholar 

  • Kuo SR, Shao KT (1991) Feeding habits of damselfish (Pomacentridae) from the southern part of Taiwan. J Fish Soc Taiwan 18(3):165–176

    Google Scholar 

  • Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Zool 22:425–441

    Article  Google Scholar 

  • Liem KF (1980) Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am Zool 20:295–314

    Article  Google Scholar 

  • Liem KF, Sanderson SL (1986) The pharyngeal jaw apparatus of labrid fishes: a functional morphological perspective. J Morphol 187:143–158

    Article  Google Scholar 

  • Losos JB (2010) Adaptive radiation, ecological opportunity and evolutionary determinism. Am Nat 175(6):623–639

    Article  Google Scholar 

  • MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42(3):594–598

    Article  Google Scholar 

  • McGee MD, Borstein SR, Neches RY, Buescher HH, Seehausen O, Wainwright PC (2015) A pharyngeal jaw evolutionary innovation facilitated extinction in Lake Victoria cichlids. Science 350(6264):1077–1079

    Article  CAS  Google Scholar 

  • Montgomery WL (1980) Comparative feeding ecology of two herbivorous damselfishes (Pomacentridae: Teleostei) from the Gulf of California, Mexico. J Exp MarBiol Ecol 47:9–24

    Article  Google Scholar 

  • Moreno-Sánchez XG, Abitia-Cárdenas LA, Escobar-Sánchez O, Palacios-Salgado DS (2011) Diet of the Cortez damselfish Stegastes rectifraenum (Teleostei: Pomacentridae) from the rocky reef at Los Frailes, Baja California Sur, Mexico. Mar Biodivers Rec 4:e98. doi:10.1017/S1755267211000996

    Article  Google Scholar 

  • Muschick M, Barluenga M, Salburger W, Meyer A (2011) Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol Biol 11:116

    Article  Google Scholar 

  • Pauly D, Froese R, Sa-a PS, Palomares ML, Christensen V, Rius J (2000) Trophlab manual. ICLARM, Manila

    Google Scholar 

  • Petersen CW, Marchetti K (1989) Filial cannibalism in the Cortez Damselfish Stegastes rectifraenum. Evolution 43:58–168

    Article  Google Scholar 

  • Poisot T, Thrall PH, Hochberg ME (2012) Trophic network structure emerges through antagonistic coevolution in temporally varying environments. Proc R Soc B 279:299–308

    Article  Google Scholar 

  • Price NN, Hamilton SL, Smith JE, Tootell JS (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440:67–78

    Article  CAS  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. See http://R-project.org/

  • Randall JE (1996) Shore fishes of Hawai‘i. University of Hawai‘i Press, Honolulu

  • Reidenbach MA, Koseff JR, Koehl MAR (2009) Hydrodynamic forces on larvae affect their settlement on coral reefs in turbulent, wave-driven flow. Limnol Oceanogr 54(1):318–330

    Article  Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Revell LJ (2013) Two new graphical methods for mapping trait evolution on phylogenies. Methods Ecol Evol 4:754–759

    Article  Google Scholar 

  • Robertson DR, Allen GR (2008) Shorefishes of the Tropical Eastern Pacific online information system, Version 1.0. Smithsonian Tropical Research Institute, Balboa, Panamá. http://www.neotropicalfishes.org/sftep. http://www.stri.org/sftep

  • Rohlf FJ (1993) Relative warps analysis and an example of its application to mosquito wings. Contributions to morphometrics. In: Marcus LF, Bello E, Garcia-Valdecasas A (eds) Monografías del Museo Nacional de Ciencias Naturales. CSIC, Madrid, pp 139–151

    Google Scholar 

  • Rohlf FJ. 2016. Tps series. Suny stonny brook. http://life.bio.sunysb.edu/morph/

  • Rohlf FJ, Slice D (1990) Extension of the Procrustes method for the optimal superposition of landmarks. Syst Zool 39:40–59

    Article  Google Scholar 

  • Schluter D (2000) Ecological character displacement in adaptive radiation. Am Nat 156:S4–S16

    Article  Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185(4145):27–39

    Article  CAS  Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Article  Google Scholar 

  • Stiassny MLJ, Jensen JS (1987) Labroid intrarelationships revisited: morphological complexity, key innovations and the study of comparative diversity. Bull Mus Comp Zool 151:269–319

    Google Scholar 

  • Thompson DA (1917) On growth and form. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Trapani J (2004) A morphometric analysis of polymorphism in the pharyngeal dentition of Cichlasoma minckleyi (Teleostei: Cichlidae). Arch Oral Biol 49(10):825–835

    Article  Google Scholar 

  • Vermeij GJ (1987) Evolution and escalation: an ecological history of life. Princeton University Press, Princeton

    Google Scholar 

  • Vermeij GJ, Covich AP (1978) Coevolution of freshwater gastropods and their predators. Am Nat 112:833–843

    Article  Google Scholar 

  • Wainwright PC (1987) Biomechanical limits to ecological performance: mollusc crushing by the Caribbean hogfish, Lachnolaimus maximus (Labridae). J Zool Lond 213:283–298

    Article  Google Scholar 

  • Wainwright PC (1991) Ecomorphology: experimental functional anatomy for ecological problems. Am Zool 31:680–693

    Article  Google Scholar 

  • Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 33–55

    Chapter  Google Scholar 

  • Wainwright PC, Smith WL, Price SA, Tang KL, Sparks JS, Ferry LA, Kuhn KL, Eytan RI, Near TJ (2012) The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Syst Biol 61(6):1001–1027

    Article  Google Scholar 

  • Wilson S, Bellwood DR (1997) Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Mar Ecol Prog Ser 153:299–310

    Article  CAS  Google Scholar 

  • Winemiller KO (1989) Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan ilanos. Environ Biol Fish 26:177–199

    Article  Google Scholar 

  • Yashpal M, Kumari U, Mittal S, Mittal AK (2006) Surface architecture of the mouth cavity of a carnivorous fish Rita rita (Hamilton, 1822) (Siluriformes, Bagridae). Belg J Zool 136(2):155–162

    Google Scholar 

  • Yoder JB, Clancey E, Des Roches S, Eastman JM, Gentry L, Godsoe W, Hagey TJ, Jochimsen D, Oswald BP, Robertson J, Sarver BAJ, Schenk JJ, Spear SF, Harmon LJ (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23(8):1420–9101

    Article  Google Scholar 

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Acknowledgements

I wish to thank the Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico, and the University of California Institute for Mexico and the United States (UC MEXUS), USA, which funded my postdoctoral research, and the Universidad Autónoma de Tamaulipas (Project PFI2015-06) for support of this project. Kevin McKeegan and Winnie Wu from the Department of Earth, Planetary and Space Sciences of University of California, Los Angeles, helped with the scanning electron microscopy. Lucia Campos (CIBNOR), H.J. Walker (SIO), Phil Hastings (SIO) and Rick Feeney (LACM) assisted in the fish collections. Edward Burress provided his data on cichlids. Three reviewers provided comments and revisions which greatly improved this manuscript.

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Correspondence to Rosalía Aguilar-Medrano.

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Aguilar-Medrano, R. Ecomorphology and evolution of the pharyngeal apparatus of benthic damselfishes (Pomacentridae, subfamily Stegastinae). Mar Biol 164, 21 (2017). https://doi.org/10.1007/s00227-016-3051-3

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