Marine Biology

, Volume 161, Issue 12, pp 2897–2907 | Cite as

Host preference, site fidelity, and homing behavior of the symbiotically luminous cardinalfish, Siphamia tubifer (Perciformes: Apogonidae)

  • Alison L. GouldEmail author
  • Saki Harii
  • Paul V. Dunlap
Original Paper


The sea urchin cardinalfish, Siphamia tubifer (Perciformes: Apogonidae), is unusual among coral reef fishes for its use of bioluminescence, produced by symbiotic bacteria, while foraging at night. As a foundation for understanding the relationship between the symbiosis and the ecology of the fish, this study examined the diel behavior, host urchin preference, site fidelity, and homing of S. tubifer in June and July of 2012 and 2013 at reefs near Sesoko Island, Okinawa, Japan (26°38′N, 127°52′E). After foraging, S. tubifer aggregated in groups among the spines of the longspine sea urchin, Diadema setosum, and the banded sea urchin, Echinothrix calamaris. A preference for D. setosum was evident (P < 0.001), especially by larger individuals (>25 mm standard length, P < 0.01), and choice experiments demonstrated the ability of S. tubifer to recognize and orient to a host urchin and to conspecifics. Tagging studies revealed that S. tubifer exhibits daily fidelity to a host urchin; 43–50 and 26–37 % of tagged individuals were associated with the same urchin after 3 and 7 days. Tagged fish also returned to their site of origin after displacement; by day two, 23–43 and 27–33 % of tagged individuals returned from displacement distances of 1 and 2 km. These results suggest that S. tubifer uses various environmental cues for homing and site fidelity; similar behaviors and cues might be used by larvae for recruitment to settlement sites and for the acquisition of luminous symbiotic bacteria.


Standard Length Site Fidelity Coral Reef Fish Symbiotic Bacterium Reef Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank K. Dougan (University of Michigan) and S. Kadena (Sesoko Station) for technical assistance. This study is a contribution from Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus. Support was provided by the University of Michigan’s Rackham Graduate School and International Institute, and the Department of Ecology and Evolutionary Biology.


  1. Allen GR (1972) Observations on a commensal relationship between Siphamia fuscolineata (Apogonidae) and the crown-of-thorns starfish, Acanthaster planci. Copeia 1972(3):595–597CrossRefGoogle Scholar
  2. Allen GR (1993) Cardinalfishes (Apogonidae) of Madang Province, Papua New Guinea, with descriptions of three new species. Revue Française d’aquariologie 20(1):9–20Google Scholar
  3. Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention, and orientation to reefs. Mar Ecol Prog Ser 241:151–160. doi: 10.3354/meps241151 CrossRefGoogle Scholar
  4. Bellwood DR (1995) Carbonate transport and within-reef patterns of bioerosion and sediment release by parrotfishes (family Scaridae) on the Great Barrier Reef. Mar Ecol Prog Ser 117:127–136. doi: 10.3354/meps117127 CrossRefGoogle Scholar
  5. Bellwood DR (1996) The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblage. Coral Reefs 15:11–19. doi: 10.1007/BF01626074
  6. Breder CM Jr, Rosen DE (1966) Modes of Reproduction in Fishes. Natural History Press, Garden CityGoogle Scholar
  7. Brown GE, Dreier VM (2002) Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Anim Behav 63:1175–1181. doi: 10.1006/anbe.2002.3024 CrossRefGoogle Scholar
  8. Chesson J (1978) Measuring preference in selective predation. Ecology 211–215. doi: 10.2307/1936364
  9. Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 1297–1304. doi: 10.2307/1937838
  10. Chrystal PJ, Potter IC, Loneragan NR, Holt CP (1985) Age structure, growth rates, movement patterns and feeding in an estuarine population of the cardinalfish Apogon rueppellii. Mar Biol 85:185–197. doi: 10.1007/BF00397437 CrossRefGoogle Scholar
  11. Døving KB, Stabell OB, Östlund-Nilsson S, Fisher R (2006) Site fidelity and homing in tropical coral reef cardinalfish: are they using olfactory cues? Chem Senses 31:265–272. doi: 10.1093/chemse/bjj028 CrossRefGoogle Scholar
  12. Dunlap PV, Nakamura M (2011) Functional morphology of the luminescence system of Siphamia versicolor (Perciformes: Apogonidae), a bacterially luminous coral reef fish. J Morphol 272:897–909. doi: 10.1002/jmor.10956 CrossRefGoogle Scholar
  13. Dunlap PV, Kojima Y, Nakamura S, Nakamura M (2009) Inception of formation and early morphogenesis of the bacterial light organ of the sea urchin cardinalfish, Siphamia versicolor (Perciformes, Apogonidae). Mar Biol 156:2011–2020. doi: 10.1007/s00227-009-1232-z CrossRefGoogle Scholar
  14. Dunlap PV, Gould AL, Wittenrich ML, Nakamura M (2012) Symbiosis initiation in the bacterially luminous sea urchin cardinalfish Siphamia versicolor. J Fish Biol 81:1340–1356. doi: 10.1111/j.1095-8649.2012.03415.x CrossRefGoogle Scholar
  15. Eibl-Eibesfeldt I (1961) Eine Symbiose zwischen Fischen (Siphamia versicolor) und Seeigeln. Zeitschrift fur Tierpsychologie 18:56–59Google Scholar
  16. Gardiner NM, Jones GP (2005) Habitat specialization and overlap in a guild of coral reef cardinalfishes (Apogonidae). Mar Ecol Prog Ser 305:163–175. doi: 10.3354/meps305163 CrossRefGoogle Scholar
  17. Gardiner NM, Jones GP (2010) Synergistic effects of habitat preference and gregarious behaviour on habitat use in coral reef cardinalfish. Coral Reefs 29:845–856. doi: 10.1007/s00338-010-0642-1 CrossRefGoogle Scholar
  18. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. PNAS 3(104):858–863. doi: 10.1073/pnas.0606777104 CrossRefGoogle Scholar
  19. Gon O, Allen GR (2012) Revision of the Indo-Pacific cardinalfish genus Siphamia (Perciformes: Apogonidae). Zootaxa 3294:1–84Google Scholar
  20. Greenfield DW, Johnson RK (1990) Heterogeneity in habitat choice in cardinalfish community structure. Copeia 4:1107–1114CrossRefGoogle Scholar
  21. Hohenegger J, Yordanova E, Nakano Y, Tatzreiter F (1999) Habitats of larger foraminifera on the upper reef slope of Sesoko Island, Okinawa, Japan. Mar Micropaleontol 36(2):109–168CrossRefGoogle Scholar
  22. Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83(10):2855–2868. doi: 10.2307/3072021 CrossRefGoogle Scholar
  23. Kaeding AJ, Ast JC, Pearce MM, Urbanczyk H, Kimura S, Endo H, Nakamura M, Dunlap PV (2007) Phylogenetic diversity and cosymbiosis in the bioluminescent symbioses of Photobacterium mandapamensis. Appl Environ Microbiol 73(10):3173–3182. doi: 10.1128/AEM.02212-06 CrossRefGoogle Scholar
  24. Kingsford MJ, Finn MD, O’Callaghan MD, Atema J, Gerlach G (2014) Planktonic larval duration, age and growth of Ostorhinchus doederleini (Pisces: Apogonidae) on the southern Great Barrier Reef, Australia. Mar Biol 161(2):245–259. doi: 10.1007/s00227-013-2331-4 CrossRefGoogle Scholar
  25. Kolm N, Hoffman EA, Olsson J, Berglund A, Jones AG (2005) Group stability and homing behavior but no kin group structures in a coral reef fish. Behav Ecol 16:521–527. doi: 10.1093/beheco/ari022 CrossRefGoogle Scholar
  26. Kuwamura T (1985) Social and reproductive behaviour of three mouthbrooding cardinalfishes, Apogon doederlini, A. niger and A. notatus. Environ Biol Fishes 13:17–24CrossRefGoogle Scholar
  27. Lachner EA (1955) Inquilinism and a new record for Paramia bipunctata, a new cardinal fish from the Red Sea. Copeia 1955:53–55CrossRefGoogle Scholar
  28. Leis JM, Bullock S (1986) The luminous cardinalfish Siphamia (Pisces, Apogonidae), development of larvae and the luminous organ. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-pacific fish biology: proceedings of the second international conference on Indo-pacific fish. Japanese Ichthyol Soc, Toyko, pp 703–714Google Scholar
  29. Leis JM, Carson-Ewart BM, Hay AC, Cato DH (2003) Coral reef sounds enable nocturnal navigation by some reef-fish larvae in some places and at some times. J Fish Biol 63:724–737. doi: 10.1046/j.1095-8649.2003.00182.x CrossRefGoogle Scholar
  30. Magnus DB (1967) Ecological and ethological studies and experiments on the echinoderms of the Red Sea. Stud Trop Oceanogr 5:635–664Google Scholar
  31. Manly BFJ, Miller P, Cook LM (1972) Analysis of a selective predation experiment. Am Nat 719–736Google Scholar
  32. Marnane MJ (2000) Site fidelity and homing behaviour in coral reef cardinalfishes. J Fish Biol 57:1590–1600. doi: 10.1111/j.1095-8649.2000.tb02234.x CrossRefGoogle Scholar
  33. Marnane MJ, Bellwood DR (2002) Diet and nocturnal foraging in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef, Australia. Mar Ecol Prog Ser 231:261–268. doi: 10.3354/meps231261 CrossRefGoogle Scholar
  34. Meyer JL, Shultz ET, Helfman GS (1983) Fish schools: an asset to corals. Science 220:1047–1049CrossRefGoogle Scholar
  35. Michael SW (2013) Lionfish: risky but rewarding. Lionfish are beautiful, but stay away from their sting. Accessed 22 April 2014
  36. Noda M, Gushima K, Kakuda S (1994) Local prey search based on spatial memory and expectation in the planktivorous reef fish, Chromis chrysurus (Pomacentridae). Anim Behav 47:1413–1422. doi: 10.1006/anbe.1994.1188
  37. Okuda N, Yanagisawa Y (1996) Filial cannibalism by mouthbrooding males of the cardinalfish, Apogon doederlini, in relation to their physical condition. Environ Biol Fish 45:397–404CrossRefGoogle Scholar
  38. R Development Core Team (2012) R: a language and environment for statistical computing. R 2.15.1 edn. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  39. Radcliffe L (1911) Notes on some fishes of the genus Amia, family of Cheilodipteridae, with descriptions of four new species from the Philippine Islands. Proc US Natl Mus 41(1853):245–261CrossRefGoogle Scholar
  40. Radford CA, Jeffs AG, Tindle CT, Montgomery JC (2008) Resonating sea urchin skeletons create coastal choruses. Mar Ecol Prog Ser 362:37–43. doi: 10.3354/meps07444 CrossRefGoogle Scholar
  41. Radford CA, Stanley JA, Tindle CT, Montgomery JC, Jeffs AG (2010) Localised coastal habitats have distinct underwater sound signatures. Mar Ecol Prog Ser 401:21–29. doi: 10.3354/meps08451 CrossRefGoogle Scholar
  42. Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Travolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 131–149CrossRefGoogle Scholar
  43. Sale PF (1978a) Reef fishes and other vertebrates: a comparison of social structures. In: Reese ES, Lichter FJ (eds) Contrasts in behaviour: adaptations in the aquatic and terrestrial environments. Wiley, New York, pp 313–346Google Scholar
  44. Sale PF (1978b) Coexistence of coral reef fishes: a lottery for living space. Environ Biol Fish 3:85–102. doi: 10.1007/BF00006310 CrossRefGoogle Scholar
  45. Shapiro DY (1986) Intra-group home ranges in a female-biased group of sex changing fish. Anim Behav 34:865–870. doi: 10.1016/S0003-3472(86)80072-0 CrossRefGoogle Scholar
  46. Shima JS (2001) Recruitment of a coral reef fish: roles of settlement, habitat, and postsettlement losses. Ecology 82:2190–2199. doi: 10.2307/2680225 CrossRefGoogle Scholar
  47. Shima JS, McNaughtan D, Geange SW, Wilkinson S (2012) Ontogenetic variation in site fidelity and homing behaviour of a temperate reef fish. J Exp Mar Biol Ecol 416:162–167. doi: 10.1016/j.jembe.2012.02.020 CrossRefGoogle Scholar
  48. Simpson SD, Meekan MG, McCauley RD, Jeffs A (2004) Attraction of settlement-stage coral reef fishes to reef noise. Mar Ecol Prog Ser 276:263–268. doi: 10.3354/meps276263 CrossRefGoogle Scholar
  49. Simpson SD, Meekan MG, Montgomery JC, McCauley RD, Jeffs AG (2005) Homeward sound. Science 308(5719):221. doi: 10.1126/science.1107406 CrossRefGoogle Scholar
  50. Stier AC, Steele MA, Brooks AJ (2009) Coral reef fishes use crown-of-thorns seastar as habitat. Coral Reefs 28(1):227. doi: 10.1007/s00338-008-0445-9 CrossRefGoogle Scholar
  51. Strasburg DW (1966) Observations on the ecology of four apogonid fishes. Pacific Sci 20:338–341Google Scholar
  52. Tamura R (1982) Experimental observations on the association between the cardinalfish (Siphamia versicolor) and the sea urchin (Diadema setosum). Galaxea 1:1–10Google Scholar
  53. Thresher RE (1984) Reproduction in reef fishes. TFH Publications, Neptune City, p 399Google Scholar
  54. Tominaga Y (1964) Notes on the fishes of the genus Siphamia (Apogonidae), with a record of S. versicolor from the Ryukyu Islands. Jpn J Ichthyol 12:10–17Google Scholar
  55. Urbanczyk H, Ogura Y, Hendry TA, Gould AL, Kiwaki N, Atkinson JT, Hayashi T, Dunlap PV (2011) Genome sequence of Photobacterium mandapamensis strain svers. 1.1, the bioluminescent symbiont of the cardinal fish Siphamia versicolor. J Bacteriol 193(12):3144–3145. doi: 10.1128/JB.00370-11 CrossRefGoogle Scholar
  56. Weber M (1909) Diagnosen neuer Fische der Siboga-Expedition. Notes Leyden Museum 31:143–169Google Scholar
  57. White GE, Brown C (2013) Site fidelity and homing behaviour in intertidal fishes. Mar Biol 160:1365–1372. doi: 10.1007/s00227-013-2188-6 CrossRefGoogle Scholar
  58. Yoshiyama RM, Gaylord KB, Philippart MT, Moore TR, Jordan JR, Coon CC, Schalk LL, Valpey CJ, Tosques I (1992) Homing behavior and site fidelity in intertidal sculpins (Pisces: Cottidae). J Exp Mar Biol Ecol 160:115–130. doi: 10.1016/0022-0981(92)90114-P CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Sesoko Station, Tropical Biosphere Research CenterUniversity of the RyukyusMotobuJapan

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