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Symbiosis

, Volume 54, Issue 3, pp 107–117 | Cite as

Symbioses between salamander embryos and green algae

  • Ryan KerneyEmail author
Article

Abstract

The symbiosis between Ambystoma maculatum (spotted salamander) embryos and green algae was initially described over 120 years ago. Algae populate the egg capsules that surround individual A. maculatum embryos, giving the intracapsular fluid a characteristic green hue. Early work established this symbiosis to be a mutualism, while subsequent studies sought to identify the material benefits of this association to both symbiont and host. These studies have shown that salamander embryos benefit from increased oxygen concentrations provided by their symbiotic algae. The algae, in turn, may benefit from ammonia excreted by the embryos. All of these early studies considered the association to be an ectosymbiotic mutualism. However our recent work has shown that algae invade both embryonic salamander cells and tissues during development. The unexpected invasion of algal cells into a salamander host changes our understanding of this symbiosis. This review will summarize the earlier research on this association in the context of these recent findings. It will also emphasize gaps in our understanding of this and other amphibian embryo-algal interactions and suggest various research avenues to address these unanswered questions.

Keywords

Salamanders Green algae Symbiosis Endosymbiosis Mutualism Ambystoma 

Notes

Acknowledgements

Thanks to Brian K. Hall for critically reading an earlier draft of this manuscript, and to Lars Crooks for providing the illustration of an adult spotted salamander. This work was funded by an NSERC grant to BKH, and an American Association of Anatomists Postdoctoral Fellowship to RK.

References

  1. Anderson J, Hassinger D, Dalrymple G (1971) Natural mortality of eggs and larvae of Ambystoma t. tigrinum. Ecology 52:1107–1112CrossRefGoogle Scholar
  2. Archetti M, Ubeda F, Fudenberg D, Green J, Pierce NE, Yu DW (2011) Let the right one in: a microeconomic approach to partner choice in mutualisms. Am Nat 177:75–85PubMedCrossRefGoogle Scholar
  3. Bachmann M, Carlton R, Burkholder J, Wetzel R (1985) Symbiosis between salamander eggs and green algae: microelectrode measurements inside eggs demonstrate effect of photosynthesis on oxygen concentration. Can J Zool 64:1586–1588CrossRefGoogle Scholar
  4. Banta AM, Gortner RA (1914) A milky white amphibian egg jelly. Biol Bull 27:259–261CrossRefGoogle Scholar
  5. Barsanti L, Coltelli P, Evangelista V, Frassanito AM, Passarelli V, Vesentini N, Gualtieri P (2008) Oddities and curiosities of the algal world. In: Evangelista V, Barsanti L, Frassanito AM, Passarelli V, Gualtieri P (eds) Algal Toxins: Nature, Occurrence, Effect and Detection. Springer Science, pp 353–391.Google Scholar
  6. Bhavsar AP, Guttman JA, Finlay BB (2007) Manipulation of host-cell pathways by bacterial pathogens. Nature 449:827–834PubMedCrossRefGoogle Scholar
  7. Biebel P (1969) Use of physiological and biochemical characteristics in distinguishing chlamydonomad algae associated with amphibian egg membranes. Int Bot Cong Abstr 11:15Google Scholar
  8. Bishop S (1941) Salamanders of New York. N Y State Mus Bull 324:1–365Google Scholar
  9. Blaustein AR, Kiesecker JM, Chivers DM, Anthony RG (1997) Ambient UV-B radiation causes deformities in amphibian embryos. Proc Natl Acad Sci U S A 94:13735–13737PubMedCrossRefGoogle Scholar
  10. Branch LC, Taylor DH (1977) Physiological and behavioral responses of larval spotted salamanders (Ambystoma maculatum) to various concentrations of oxygen. Comp Biochem Physiol 58A:269–274CrossRefGoogle Scholar
  11. Breder R (1927) The courtship of the spotted salamander. Bull New York Zool Soc 30:51–56Google Scholar
  12. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microb 8:218–230CrossRefGoogle Scholar
  13. Brodman R (1995) Annual variation in breeding sucess of two syntopic species of Ambystoma salamanders. J Herpetol 29:111–113CrossRefGoogle Scholar
  14. Brucker R, Harris R, Schwantes C, Gallaher T, Flaherty D, Lam B, Minbiole K (2008) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34:1422–1429PubMedCrossRefGoogle Scholar
  15. Buckland-Nicks J, Chia FS, Behrens S (1973) Oviposition and development of two intertidal snails, Littorina sitkana and Littorina scutulata. Can J Zool 51:359–365CrossRefGoogle Scholar
  16. Burggren WW (1985) Gas, exchange, metabolism, and ‘ventilation’ in gelatinous frog egg masses. Physiol Zool 58:503–514Google Scholar
  17. Carl GC, Cowan IM (1945) Notes on the salamanders of British Columbia. Copeia 1945:43–44CrossRefGoogle Scholar
  18. DeMartini E (1978) Spatial aspects of reproduction in buffalo sculpin, Enophrys bison. Env Biol Fish 3:331–336CrossRefGoogle Scholar
  19. Douglas A (2010) The symbiotic habit. Princeton University Press, PrincetonGoogle Scholar
  20. Epel D, Gilbert SF (2008) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, SunderlandGoogle Scholar
  21. Ettl H (1961) Zwei neue Chlamydomonaden. Arch Protistenk Bd 105:273–284Google Scholar
  22. Felsenstein J (2004) Inferring Phylogenies. Sinauer Associates, SunderlandGoogle Scholar
  23. Gatz J (1973) Algal entry into the eggs of Ambystoma maculatum. J Herpetol 7:137–138CrossRefGoogle Scholar
  24. Gilbert PW (1942) Observations on the eggs of Ambystoma maculatum with especial reference to the green algae found within the egg envelopes. Ecology 23:215–227CrossRefGoogle Scholar
  25. Gilbert PW (1944) The alga-egg relationship in Ambystoma maculatum, a case of symbiosis. Ecology 25:366–369CrossRefGoogle Scholar
  26. Gilhen J (1984) Amphibians and reptiles of Nova Scotia. Nova Scotia Museum, HalifaxGoogle Scholar
  27. Goff L, Stein J (1976) Preliminary studies on the green alga Oophila in salamander egg masses. J Phycol 12(suppl):23Google Scholar
  28. Goff L, Stein JR (1978) Ammonia: basis for algal symbiosis in salamander egg masses. Life Sci 22:1463–1468PubMedCrossRefGoogle Scholar
  29. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  30. Graham L, Graham J, Wilcox L (2009) Algae, 2nd Edition. Benjamin Cummings (Pearson), San FranciscoGoogle Scholar
  31. Gregg JR, Ballentine R (1946) Nitrogen metabolism of Rana pipiens during embryonic development. J Exp Zool 103:143–168PubMedCrossRefGoogle Scholar
  32. Greven H (2003) Oviduct and egg-jelly. In: Sever D (ed) Reproductive biology and phylogeny of the Urodela. Science Publishers Inc., Enfield, pp 151–181Google Scholar
  33. Hammen C, Hutchison V (1962) Carbon dioxide assimilation in the symbiosis of the salamander Ambystoma maculatum and the algae Oophila amblystomatis. Life Sci 1:527–532CrossRefGoogle Scholar
  34. Hardy LM, Lucas C (1991) A crystalline protein is responsible for dimorphic egg jellies in the spotted salamander, Ambystoma maculatum (Shaw) (Caudata Ambystomatidae). Comp Biochem Physiol 100A:653–660CrossRefGoogle Scholar
  35. Harrison R (1969) Harrison stages and description of normal development of the spotted salamander, Ambystoma punctatum (Linn). In: Wilens S (ed) Organization and development of the embryo. Yale University Press, New Haven, pp 44–66Google Scholar
  36. Hayes TB, Khoury V, Narayan A, Nazir M, Park A, Brown T, Adame L, Chan E, Buchholz D, Stueve T, Gallipeau S (2010) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc Natl Acad Sci U S A 107:4612–4617PubMedCrossRefGoogle Scholar
  37. Henry WV, Twitty VC (1940) Contributions to the life histories of Dicamptodon ensatus and Ambystoma gracile. Copeia 1940:247–250CrossRefGoogle Scholar
  38. Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc R Soc Lond B 271:509–515CrossRefGoogle Scholar
  39. Hutchison V (1971) On the Ambystoma egg-alga relationship. Herp Rev 3:82Google Scholar
  40. Hutchison V, Hammen C (1958) Oxygen utilization in the symbiosis of embryos of the salamander, Ambystoma maculatum and the alga, Oophila amblystomatis. Biol Bull Mar Biol Lab Woods Hole 115:483–489CrossRefGoogle Scholar
  41. Jones TR, Kluge AG, Wolf AJ (1993) When theories and methodologies clash: a phylogenetic reanalysis of the North American ambystomatid salamanders (Caudata: Ambystomatidae). Syst Biol 42:92–102Google Scholar
  42. Kerney R, Kim E, Hangarter RP, Heiss AA, Bishop CD, Hall BK (2011) Intracellular invasion of green algae in a salamander host. Proc Natl Acad Sci U S A 108:6497–6502PubMedCrossRefGoogle Scholar
  43. Kuzmin V, Tkach V, Snyder S (2001) Rhabdias ambystomae sp. n. (Nematoda: Rhabdiasidae) from the North American spotted salamander Ambystoma maculatum (Ambystomatidae). Comp Parasit 68:228–235Google Scholar
  44. Lauer A, Simon M, Banning J, André E, Duncan K, Harris R (2007) Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007:630–640CrossRefGoogle Scholar
  45. Lee W, Lagios M, Leonards R (1975) Wound infection by Prototheca wickerhamii, a saprophytic alga pathogenic for man. J Clin Microbiol 2:62–66PubMedGoogle Scholar
  46. Lewin RA, Robinson PT (1979) The greening of polar bears in zoos. Nature 278:445–447PubMedCrossRefGoogle Scholar
  47. Ling R, Wener J (1988) Mortality in Ambystoma maculatum larvae due to Tetrahymena infection. Herp Rev 19:26–27Google Scholar
  48. Marco A, Blaustein A (2000) Symbiosis with green algae affects survival and growth of Northwestern salamander embryos. J Herpetol 34:617–621CrossRefGoogle Scholar
  49. Miller D, Geibel J (1973) Summary of blue rockfish and lingcod life histories; a reef ecology study; and giant kelp, Macrocystis pyrifera, experiments in Monterey Bay, California. Fish Bull 158:51–77Google Scholar
  50. Mills NE, Barnhart MC (1999) Effects of hypoxia on embryonic development in two Ambystoma and two Rana species. Physiol Biochem Zool 72:178–188CrossRefGoogle Scholar
  51. Olivier HM, Moon BR (2010) The effects of atrazine on spotted salamander embryos and their symbiotic alga. Ecotoxicology 19:654–661PubMedCrossRefGoogle Scholar
  52. Orr H (1888) Note on the development of amphibians, chiefly concerning the central nervous system; with additional observations on the hypophysis, mouth, and the appendages and skeleton of the head. Quart J Micro Sci N S 115:483–489Google Scholar
  53. Patch CL (1922) Some amphibians and reptiles from British Columbia. Copeia 1922:74–79CrossRefGoogle Scholar
  54. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, WashingtonGoogle Scholar
  55. Peyton K, Hanisak M, Lin J (2004) Marine algal symbionts benefit benthic invertebrate embryos deposited in gelatinous egg masses. J Exp Mar Biol Ecol 307:139–164CrossRefGoogle Scholar
  56. Pinder A, Friet S (1994) Oxygen transport in egg masses of the amphibians Rana sylvatica and Ambystoma maculatum: convection, diffusion and oxygen production by algae. J Exp Biol 197:17–30PubMedGoogle Scholar
  57. Printz H (1928) Chlorophyceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, vol 3. W. Engelmannl 1924-, Leipzig, pp 1–463.Google Scholar
  58. Rankin J (1937) An ecological study of the parasites of some North Carolina salamanders. Evol Monogr 7:169–269CrossRefGoogle Scholar
  59. Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD (2004) Multiple stressors and salamanders: effects of an herbicide, food limitation, and hydroperiod. Ecol App 14:1028–1040CrossRefGoogle Scholar
  60. Ruth B, Dunson W, Rowe C, Hedges S (1993) A molecular and functional evaluation of the egg mass color polymorphism of the spotted salamander: Ambystoma maculatum. J Herpetol 27:306–314CrossRefGoogle Scholar
  61. Sacerdote AB, King RB (2009) Dissolved oxygen requirements for hatching sucess of two ambystomatid salamanders in restored ephemeral ponds. Wetlands 29:1202–1213CrossRefGoogle Scholar
  62. Salthe S (1963) The egg capsules in the amphibia. J Morphol 113:161–171PubMedCrossRefGoogle Scholar
  63. Selosse M-A (2000) Un exemple de symbiose algue-invertébré à Belle-Isle-en-Mer: la planaire Convoluta roscoffensis et la prasinophycée Tetraselmis convolutae. Acta Bot Gall 147:323–331Google Scholar
  64. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707PubMedCrossRefGoogle Scholar
  65. Seymour R, Roberts J (1991) Embryonic respiration and oxygen distribution in foamy and nonfoamy egg masses of the frog Limnodynastes tasmaniensis. Physiol Zool 64:1322–1340Google Scholar
  66. Seymour RS, Bradford DF (1995) Respiration of amphibian eggs. Physiol Zool 68:1–25Google Scholar
  67. Shaffer HB, Clark JM, Kraus F (1991) When molecules and morphology clash: a phylogenetic analysis of the North American ambystomatid salamanders (Caudata: Ambystomatidae). Syst Zool 40:284–303CrossRefGoogle Scholar
  68. Shudert E (2003) Nonmotile coccoid and colonial green algae. In: Wehr TD, Sheath RG (eds) Freshwater Algae of North America. Academic, New York, pp 253–307Google Scholar
  69. Storer TI (1925) A synopsis of the amphibia of California. Univ Cal Pub Zool 27:1–342Google Scholar
  70. Tattersall G, Spiegelaar N (2008) Embryonic motility and hatching success of Ambystoma maculatum are influenced by a symbiotic alga. Can J Zool 86:1289–1298CrossRefGoogle Scholar
  71. Valls JH, Mills NE (2007) Intermittent hypoxia in eggs of Ambystoma maculatum: embryonic development and egg capsule conductance. J Exp Biol 210:2430–2435PubMedCrossRefGoogle Scholar
  72. Venn A, Loram J, Douglas A (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080PubMedCrossRefGoogle Scholar
  73. Ward D, Sexton O (1981) Anti-predator role of salamander egg membranes. Copeia 1981:724–726CrossRefGoogle Scholar
  74. Woods HA, Podolsky RD (2007) Photosynthesis drives oxygen levels in macrophyte-associated gastropod egg masses. Biol Bull 213:88–94PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Biology DepartmentDalhousie UniversityHalifaxCanada

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