Phylogenetic analysis of host–symbiont specificity and codivergence in bioluminescent symbioses
dc.contributor.author | Dunlap, Paul V. | en_US |
dc.contributor.author | Ast, Jennifer C. | en_US |
dc.contributor.author | Kimura, Seishi | en_US |
dc.contributor.author | Fukui, Atsushi | en_US |
dc.contributor.author | Yoshino, Tetsuo | en_US |
dc.contributor.author | Endo, Hiromitsu | en_US |
dc.date.accessioned | 2010-06-01T20:38:55Z | |
dc.date.available | 2010-06-01T20:38:55Z | |
dc.date.issued | 2007-10 | en_US |
dc.identifier.citation | Dunlap, Paul V.; Ast, Jennifer C.; Kimura, Seishi; Fukui, Atsushi; Yoshino, Tetsuo; Endo, Hiromitsu (2007). "Phylogenetic analysis of host–symbiont specificity and codivergence in bioluminescent symbioses." Cladistics 23(5): 507-532. <http://hdl.handle.net/2027.42/73754> | en_US |
dc.identifier.issn | 0748-3007 | en_US |
dc.identifier.issn | 1096-0031 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/73754 | |
dc.description.abstract | Several groups of marine fishes and squids form mutualistic bioluminescent symbioses with luminous bacteria. The dependence of the animal on its symbiont for light production, the animal's specialized anatomical adaptations for harboring bacteria and controlling light emission, and the host family bacterial species specificity characteristic of these associations suggest that bioluminescent symbioses are tightly coupled associations that might involve coevolutionary interactions. Consistent with this possibility, evidence of parallel cladogenesis has been reported for squid–bacterial associations. However, genetic adaptations in the bacteria necessary for and specific to symbiosis have not been identified, and unlike obligate endosymbiotic associations in which the bacteria are transferred vertically, bacterially bioluminescent hosts acquire their light-organ symbionts from the environment with each new host generation. These contrasting observations led us to test the hypotheses of species specificity and codivergence in bioluminescent symbioses, using an extensive sampling of naturally formed associations. Thirty-five species of fish in seven teleost families (Chlorophthalmidae, Macrouridae, Moridae, Trachichthyidae, Monocentridae, Acropomatidae, Leiognathidae) and their light-organ bacteria were examined. Phylogenetic analysis of a taxonomically broad sampling of associations was based on mitochondrial 16S rRNA and cytochrome oxidase I gene sequences for the fish and on recA , gyrB and luxA sequences for bacteria isolated from the light organs of these specimens. In a fine-scale test focused on Leiognathidae, phylogenetic analysis was based also on histone H3 subunit and 28S rRNA gene sequences for the fish and on gyrB , luxA , luxB , luxF and luxE sequences for the bacteria. Deep divergences were revealed among the fishes, and clear resolution was obtained between clades of the bacteria. In several associations, bacterial species identities contradicted strict host family bacterial species specificity. Furthermore, the fish and bacterial phylogenies exhibited no meaningful topological congruence; evolutionary divergence of host fishes was not matched by a similar pattern of diversification in the symbiotic bacteria. Re-analysis of data reported for squids and their luminous bacteria also revealed no convincing evidence of codivergence. These results refute the hypothesis of strict host family bacterial species specificity and the hypothesis of codivergence in bioluminescent symbioses. © The Willi Hennig Society 2007. | en_US |
dc.format.extent | 3223442 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.rights | 2007 The Willi Hennig Society | en_US |
dc.title | Phylogenetic analysis of host–symbiont specificity and codivergence in bioluminescent symbioses | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA | en_US |
dc.contributor.affiliationother | Fisheries Research Laboratory, Mie University, Shima, Mie, Japan | en_US |
dc.contributor.affiliationother | School of Fisheries and Marine Technology, Tokai University, Shimizu-Orido, Shizuoka, Japan | en_US |
dc.contributor.affiliationother | Department of Marine Sciences, University of the Ryukyus, Nishihara, Okinawa, Japan | en_US |
dc.contributor.affiliationother | Laboratory of Marine Biology, Kochi University, Kochi, Japan | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/73754/1/j.1096-0031.2007.00157.x.pdf | |
dc.identifier.doi | 10.1111/j.1096-0031.2007.00157.x | en_US |
dc.identifier.source | Cladistics | en_US |
dc.identifier.citedreference | Ast, J.C., Dunlap, P.V., 2004. Phylogenetic analysis of the lux operon distinguishes two evolutionarily distinct clades of Photobacterium leiognathi. Arch. Microbiol. 181, 352 – 361. | en_US |
dc.identifier.citedreference | Ast, J.C., Dunlap, P.V., 2005. Phylogenetic resolution and habitat specificity of members of the Photobacterium phosphoreum species group. Environ. Microbiol. 7, 1641 – 1654. | en_US |
dc.identifier.citedreference | Bardey, V., Vallet, C., Robas, N., Charpentier, B., Thouvenot, B., Mougin, A., Hajnsdorf, E., Regnier, P., Springer, M., Branlant, C., 2005. Characterization of the molecular mechanisms involved in the differential production of erythrose-4-phosphate dehydrogenase, 3-phosphoglycerate kinase and class II fructose-1,6-bisphosphate aldolase in Escherichia coli. Mol. Microbiol. 57, 1265 – 1287. | en_US |
dc.identifier.citedreference | Baumann, P., Baumann, L., 1981. The marine Gram-negative eubacteria: genera Photobacterium, Beneckea, Alteromonas, Pseudomonas, and Alcaligenes. In: M.P. Starr, H. Stolp, H.G. TrÜper, A. Balows, H.G. Schlegel (Eds.), The Prokaryotes: a Handbook on Habitats, Isolation, and Identification of Bacteria. Springer-Verlag, Berlin, pp. 1302 – 1331. | en_US |
dc.identifier.citedreference | Baumann, P., Baumann, L., Lai, C.-Y., Rouhbakhsh, 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49, 55 – 94. | en_US |
dc.identifier.citedreference | Boisvert, H., Chatelain, R., Bassot, J.M., 1967. Étude d'un Photobacterium isolÉ de l'organe lumineux des poissons Leiognathidae. Ann. Inst. Pasteur (Paris), 112, 520 – 524. | en_US |
dc.identifier.citedreference | Boschi-Muller, S., Azza, S., Pollastro, D., Corbier, C., Branlant, G., 1997. Comparative enzymatic properties of GapB-encoded erythrose-4-phosphate dehydrogenase of Escherichia coli and phosphorylating glyceraldehyde-3-phsosphate dehydrogenase. J. Biol. Chem. 272, 15106 – 15112. | en_US |
dc.identifier.citedreference | Cary, S.C., Giovanonni, S.J., 1993. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl Acad. Sci USA. 90, 5695 – 5699. | en_US |
dc.identifier.citedreference | Charleston, M.A., 1998. Jungles: a new solution to the host-parasite phylogeny reconciliation problem. Math. Biosci. 149, 191 – 223. | en_US |
dc.identifier.citedreference | Charleston, M.A., Page, R.D.M., 2002. Treemap, Version 2.0. Available from the authors at: http://taxonomy.zoology.gla.ac.uk/∼mac/treemap/index.html | en_US |
dc.identifier.citedreference | Charleston, M.A., Perkins, S.L., 2006. Traversing the tangle: algorithms and applications for cophylogenetic studies. J. Biomed. Informat. 39, 62 – 71. | en_US |
dc.identifier.citedreference | Claes, M.F., Dunlap, P.V., 2000. Aposymbiotic culture of the sepiolid squid Euprymna scolopes: role of the symbiotic bacterium Vibrio fischeri in host animal growth, development, and light organ morphogenesis. J. Exp. Zool. 286, 280 – 296. | en_US |
dc.identifier.citedreference | Dunlap, P.V., 1984. Physiological and morphological state of the symbiotic bacteria from light organs of ponyfish. Biol. Bull. 167, 410 – 425. | en_US |
dc.identifier.citedreference | Dunlap, P.V., 1985. Physiological and morphological state of the symbiotic bacteria from light organs of ponyfish. Biol. Bull. 167, 410 – 425. | en_US |
dc.identifier.citedreference | Dunlap, P.V., Ast, J.C., 2005. Genomic and phylogenetic characterization of the luminous bacteria symbiotic with the deep-sea fish Chlorophthalmus albatrossis (Aulopiformes: Chlorophthalmidae). Appl. Environ. Microbiol. 71, 930 – 939. | en_US |
dc.identifier.citedreference | Dunlap, P.V., Jiemjit, A., Ast, J.C., Pearce, M.M., Marques, R.R., Lavilla-Pitogo, C.R., 2004. Genomic polymorphism in symbiotic populations of Photobacterium leiognathi. Environ. Microbiol. 6, 145 – 158. | en_US |
dc.identifier.citedreference | Dunlap, P.V., Kita-Tsukamoto, K., 2006. Luminous bacteria. In: M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.), The Prokaryotes, a Handbook on the Biology of Bacteria, 3rd edn, Vol. 2. Springer, New York, pp. 863 – 892. | en_US |
dc.identifier.citedreference | Fidopiastis, P.M., von Boletzky, S., Ruby, E.G., 1998. A new niche for Vibrio logei, the predominant light organ symbiont of squids in the genus Sepiola. J. Bacteriol. 180, 59 – 64. | en_US |
dc.identifier.citedreference | Froese, R., Pauly, D. (Eds.), 2004. FishBase, Ver. 04. Published online. http://www.fishbase.org. | en_US |
dc.identifier.citedreference | Fukasawa, S., Dunlap, P.V., 1986. Identification of luminous bacteria isolated from the light organs of the squid, Doryteuthis kensaki. Agri. Biol. Chem. 50, 1645 – 1646. | en_US |
dc.identifier.citedreference | Goloboff, P.A., Farris, J.S., Nixon, K.C., 2005. TNT: Tree Analysis Using New Technology, Version 1.0. Distributed by the authors. | en_US |
dc.identifier.citedreference | Graf, J., Ruby, E.G., 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl Acad. Sci. USA. 95, 1818 – 1822. | en_US |
dc.identifier.citedreference | Hastings, J.W., 1971. Light to hide by: ventral luminescence to camouflage the silhouette. Science, 173, 1016 – 1017. | en_US |
dc.identifier.citedreference | Hastings, J.W., Makemson, J., Dunlap, P.V., 1987. How are growth and luminescence regulated independently in light organ symbionts? Symbiosis, 4, 3 – 24. | en_US |
dc.identifier.citedreference | Hastings, J.W., Nealson, K.H., 1981. The symbiotic luminous bacteria. In: M.P. Starr, H. Stolp, H.G. TrÜper, A. Balows, H.G. Schlegel (Eds.), The Prokaryotes: a Handbook on Habitats, Isolation, and Identification of Bacteria. Springer-Verlag, Berlin, pp. 1332 – 1345. | en_US |
dc.identifier.citedreference | Haygood, M.G., 1993. Light organ symbioses in fishes. Crit. Rev. Microbiol. 19, 191 – 216. | en_US |
dc.identifier.citedreference | Haygood, M.G., Distel, D.L., 1993. Bioluminescent symbionts of flashlight fishes and deep-sea anglerfishes form unique lineages related to the genus Vibrio. Nature 363, 154 – 156. | en_US |
dc.identifier.citedreference | Haygood, M.G., Distel, D.L., Herring, P.J., 1992. Polymerase chain reaction and 16S rRNA gene sequences from the luminous bacterial symbionts of two deep-sea anglerfishes. J. Mar. Biol. Assoc. UK, 71, 149 – 159. | en_US |
dc.identifier.citedreference | Haygood, M.G., Tebo, B.M., Nealson, K.H., 1984. Luminous bacteria of a monocentrid fish ( Monocentris japonicus ) and two anomalopid fishes ( Photoblepharon palpebratus and Kryptophaneron alfredi ): population sizes and growth within the light organs, and rates of release into the seawater. Mar. Biol. 78, 249 – 254. | en_US |
dc.identifier.citedreference | Herring, P.J., Morin, J.G., 1978. Bioluminescence in fishes. In: P.J. Herring (Ed.), Bioluminescence in Action. Academic Press, London, pp. 273 – 329. | en_US |
dc.identifier.citedreference | Hosokawa, T., Kikuchi, Y., Nikoh, N., Shimada, M., Fukatsu, T., 2006. Strict host–symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4, e337. | en_US |
dc.identifier.citedreference | Jackson, A.P., 2004. A reconciliation analysis of host switching in plant-fungal symbioses. Evolution 58, 1909 – 1923. | en_US |
dc.identifier.citedreference | Jones, B.W., Lopez, J.E., Huttenburg, J., Nishiguchi, M.K., 2006. Population structure between environmentally transmitted vibrios and bobtail squids using nested clade analysis. Mol. Ecol. 15, 4317 – 4329. | en_US |
dc.identifier.citedreference | Jones, B.W., Nishiguchi, M.K., 2004. Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar. Biol. 144, 1151 – 1155. | en_US |
dc.identifier.citedreference | Kaeding, A.J., Ast, J.C., Pearce, M.M., Urbanczyk, H., Kimura, S., Endo, H., Nakamura, M., Dunlap, P.V., 2007. Phylogenetic specificity and diversity in the bioluminescent symbioses of Photobacterium mandapamensis. Appl. Environ. Microbiol. 73, 3173 – 3182. | en_US |
dc.identifier.citedreference | Kimura, S., Dunlap, P.V., Peristiwady, T., Lavilla-Pitogo, C.R., 2003. The Leiognathus aureus complex (Perciformes: Leiognathidae), with the description of a new species. Ichthyol. Res. 50, 221 – 232. | en_US |
dc.identifier.citedreference | Lo, N., Bandi, C., Watanabe, H., Nalepa, C., Beninati, C., 2003. Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20, 907 – 913. | en_US |
dc.identifier.citedreference | Maddison, D.R., Maddison, W.P., 2005. Macclade4: Analysis of Phylogeny and Character Evolution, Version 4.08. Sinauer Associates, Sunderland, MA. | en_US |
dc.identifier.citedreference | McFall-Ngai, M.J., 1991. Luminous bacterial symbiosis in fish evolution: adaptive radiation among the leiognathid fishes. In: L. Margulis, R. Fester (Eds.), Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis, 2nd edn. MIT Press, Cambridge, MA, pp. 381 – 409. | en_US |
dc.identifier.citedreference | McFall-Ngai, M.J., Dunlap, P.V., 1983. Three new modes of luminescence in the leiognathid fish Gazza minuta: discrete projected luminescence, ventral body flash, and buccal luminescence. Mar. Biol. 73, 227 – 237. | en_US |
dc.identifier.citedreference | McFall-Ngai, M.J., Morin, J.G., 1991. Camouflage by disruptive illumination in leiognathids, a family of shallow-water, bioluminescent fishes. J. Exp. Biol. 156, 119 – 137. | en_US |
dc.identifier.citedreference | McFall-Ngai, M.J., Ruby, E.G., 1991. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science, 254, 1491 – 1494. | en_US |
dc.identifier.citedreference | Miya, M., Kawaguchi, A., Nishida, M., 2001. Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences. Mol. Biol. Evol. 18, 1993 – 2009. | en_US |
dc.identifier.citedreference | Miya, M., Takeshima, H., Endo, H., Ishiguro, N.B., Inoue, J.G., Mukai, T., Satoh, T.P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K., Shirai, S.M., Nishida, M., 2003. Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol. Phylogenet. Evol. 26, 121 – 138. | en_US |
dc.identifier.citedreference | Morin, J.G., Harrington, A., Nealson, K., Krieger, N., Baldwin, T.O., Hastings, J.W., 1975. Light for all reasons: versatility in the behavioral repertoire of the flashlight fish. Science, 190, 74 – 76. | en_US |
dc.identifier.citedreference | Nakabo, T. (Ed.), 2002. Fishes of Japan with Pictoral Keys to the Species. Tokai University Press, Tokyo, Japan. | en_US |
dc.identifier.citedreference | Nealson, K.H., 1978. Isolation, identification and manipulation of luminous bacteria. Methods Enzymol. 57, 153 – 166. | en_US |
dc.identifier.citedreference | Nealson, K.H., 1979. Alternative strategies of symbiosis of marine luminous fishes harboring light-emitting bacteria. Trends Biochem. Sci. 4, 105 – 110. | en_US |
dc.identifier.citedreference | Nealson, K., Cohn, D., Leisman, G., Tebo, B., 1981. Coevolution of luminous bacteria and their eukaryotic hosts. Ann. New York Acad. Sci. 361, 76 – 91. | en_US |
dc.identifier.citedreference | Nealson, K.H., Haygood, M.G., Tebo, B.M., Roman, M., Miller, E., McCosker, J.E., 1984. Contribution of symbiotically luminous fishes to the occurrence and bioluminescence of luminous bacteria in seawater. Microb. Ecol. 10, 69 – 77. | en_US |
dc.identifier.citedreference | Nelson, J.S., 2006. Fishes of the World, 4th edn. John Wiley and Sons, New York. | en_US |
dc.identifier.citedreference | Nishiguchi, M., 2000. Temperature affects species distribution in symbiotic populations of Vibrio spp. Appl. Environ. Microbiol. 66, 3550 – 3555. | en_US |
dc.identifier.citedreference | Nishiguchi, M.K., Lopez, J.E., von Boletzky, S., 2004. Enlightenment of old ideas from new investigations: the evolution of bacteriogenic light organs in squids. Evol. Dev. 6, 41 – 49. | en_US |
dc.identifier.citedreference | Nishiguchi, M., Nair, V.S., 2003. Evolution of symbiosis in the Vibrionaceae: a combined approach using molecules and physiology. Int. J. System. Evol. Microbiol. 53, 2019 – 2026. | en_US |
dc.identifier.citedreference | Nishiguchi, M., Ruby, E.G., McFall-Ngai, M.J., 1998. Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel cladogenesis in sepiolid squid- Vibrio symbioses. Appl. Environ. Microbiol. 64, 3209 – 3213. | en_US |
dc.identifier.citedreference | Page, R.D.M., 1994. Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics 10, 155 – 173. | en_US |
dc.identifier.citedreference | Page, R.D.M., Charleston, M.A., 1998. Trees within trees: phylogeny and historical associations. Trends Ecol. Evol. 13, 356 – 359. | en_US |
dc.identifier.citedreference | Peek, A.S., Feldman, R.A., Lutz, R.A., Vrijenhoek, R.C., 1998. Cospeciation of bacteria and deep sea clams. Proc. Natl Acad. Sci. USA. 95, 9962 – 9966. | en_US |
dc.identifier.citedreference | Reichelt, J.L., Nealson, K., Hastings, J.W., 1977. The specificity of symbiosis: Ponyfish and luminous bacteria. Arch. Microbiol. 112, 157 – 161. | en_US |
dc.identifier.citedreference | Ruby, E.G., Asato, L.M., 1993. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch. Microbiol. 159, 160 – 167. | en_US |
dc.identifier.citedreference | Ruby, E.G., Morin, J.G., 1978. Specificity of symbiosis between deep-sea fish and psychrotrophic luminous bacteria. Deep-Sea Res. 25, 161 – 171. | en_US |
dc.identifier.citedreference | Saffo, M.B., 2002. Themes from variation: probing the commonalities of symbiotic associations. Integr. Comp. Biol. 42, 291 – 294. | en_US |
dc.identifier.citedreference | Sasaki, A., Ikejima, K., Aoki, S., Azuma, N., Kashimura, N., Wada, M., 2003. Field evidence for bioluminescent signaling in the pony fish, Leiognathus elongatus. Environ. Biol. Fishes, 66, 307 – 311. | en_US |
dc.identifier.citedreference | Shimizu, T., 1997. Beryciformes. In: O. Okamura, K. Amaoka (Eds.), Sea Fishes of Japan. Yama-Kei Publishers Co., Ltd, Tokyo, pp. 156 – 167. | en_US |
dc.identifier.citedreference | Sparks, J.S., Dunlap, P.V., Smith, W.L., 2005. Evolution and diversification of a sexually dimorphic luminescent system in ponyfishes (Teleostei: Leiognathidae), including diagnoses for two new genera. Cladistics 21, 305 – 327. | en_US |
dc.identifier.citedreference | Swofford, D.L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0B10. Sinauer Associates, Sunderland, MA. | en_US |
dc.identifier.citedreference | Thompson, J.N., 2005. The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, IL. | en_US |
dc.identifier.citedreference | Vydryakova, G.A., Kuznetsov, A.M., Primakova, G.A., Chugaeva, Y.V., Fish, A.M., 1995. Luminescent bacterial symbionts and commensals of luminescent and nonluminescent animals of the Indian Ocean. Mikrobiologiya 64, 589 – 592. | en_US |
dc.identifier.citedreference | Wada, M., Azuma, N., Mizuno, N., Kurokura, H., 1999. Transfer of symbiotic luminous bacteria from parental Leiognathus nuchalis to offspring. Mar. Biol. 135, 683 – 687. | en_US |
dc.identifier.citedreference | Wada, M., Kamiya, A., Uchiyama, N., Yoshizawa, S., Kita-Tsukamoto, K., Ikejima, K., Yu, R., Imada, C., Karatani, H., Mizuno, N., Suzuki, Y., Nishida, M., Kogure, K., 2006. Lux A gene of light organ symbionts of the bioluminescent fish Acropoma japonicum (Acropomatidae) and Siphamia versicolor (Apogonidae) forms a lineage closely related to that of Photobacterium leiognathi ssp. mandapamensis. FEMS Microbiol. Lett. 260, 186 – 192. | en_US |
dc.identifier.citedreference | Wei, S.L., Young, R.E., 1989. Development of symbiotic bacterial bioluminescence in a nearshore cephalopod, Euyprmna scolopes. Mar. Biol. 103, 541 – 546. | en_US |
dc.identifier.citedreference | Wheeler, W., Gladstein, D., De Laet, J., 2003. POY, Phylogeny Reconstruction Via Optimization of DNA and Other Data, Version 3.0.11 ( American Museum of Natural History, New York), available by anonymous ftp from ftp://ftp.amnh.org/pub/people/wheeler/poy/version3-current/poy.3.0.11.pdf. | en_US |
dc.identifier.citedreference | Wolfe, C.J., Haygood, M.G., 1991. Restriction fragment length polymorphism analysis reveals high levels of genetic divergence among the light organ symbionts of flashlight fish. Biol. Bull. 181, 135 – 143. | en_US |
dc.identifier.citedreference | Woodland, D.J., Cabanban, A.S., Taylor, V.M., Taylor, R.J., 2002. A synchronized rhythmic flashing light display by schooling Leiognathus splendens (Leiognathidae: Perciformes). Mar. Freshwater Res. 53, 159 – 162. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
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.