Oecologia

, Volume 174, Issue 3, pp 921–930 | Cite as

Chenopod salt bladders deter insect herbivores

Plant-microbe-animal interactions - Original research

Abstract

Trichomes on leaves and stems of certain chenopods (Chenopodiaceae) are modified with a greatly enlarged apical cell (a salt bladder), containing a huge central vacuole. These structures may aid in the extreme salt tolerance of many species by concentrating salts in the vacuole. Bladders eventually burst, covering the leaf in residue of bladder membranes and solid precipitates. The presence of this system in non-halophytic species suggests additional functions. I tested the novel hypothesis that these bladders have a defensive function against insect herbivores using choice, no choice, and field tests. Generalist insect herbivores preferred to feed on leaves without salt bladders in choice tests. In no choice tests, herbivores consumed less leaf matter with bladders. In a field test, leaves from which I had removed bladders suffered greater herbivory than adjacent leaves with bladders. Solutions containing bladders added to otherwise preferred leaves deterred herbivores, suggesting a water-soluble chemical component to the defense. This bladder system has a defensive function in at least four genera of chenopods. Salt bladders may be a structural defense, like spines or domatia, but also have a chemical defense component.

Keywords

Plant–herbivore interaction Salt bladders Salt hairs Vesicular hairs Chenopodiaceae Chenopodium Atriplex 

References

  1. Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190. doi:10.1046/j.1469-8137.1998.00111.x CrossRefGoogle Scholar
  2. Adolf VI, Jacobsen SE, Shabala S (2013) Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.). Environ Exp Bot 92:43–54. doi:10.1016/j.envexpbot.2012.07.004 CrossRefGoogle Scholar
  3. Baldwin BG, Goldman DH, Keil DJ, Patterson R, Rosatti TJ, Wilken DH (2012) The Jepson manual: vascular plants of California, 2nd edn. University of California Press, BerkeleyGoogle Scholar
  4. Bassett IJ, Crompton CW (1978) The biology of Canadian weeds. 32. Chenopodium album L. Can J Plant Sci 58:1061–1072Google Scholar
  5. Black RF (1954) The leaf anatomy of Australian members of the genus Atriplex. I. Atriplex vesicaria Heward and A. nummularia Lindl. Aust J Bot 2:269–286CrossRefGoogle Scholar
  6. Black RF (1958) Effect of sodium chloride on leaf succulence and area of Atriplex hastata L. Aust J Bot 6:306–321CrossRefGoogle Scholar
  7. Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. doi:10.1007/s11104-007-9240-6 CrossRefGoogle Scholar
  8. Chu GL, Stutz HC, Sanderson SC (1991) Morphology and taxonomic position of Suckleya suckleyana (Chenopodiaceae). Am J Bot 78:63–68. doi:10.2307/2445228 CrossRefGoogle Scholar
  9. Cooper SM, Ginnett TF (1998) Spines protect plants against browsing by small climbing mammals. Oecologia 113:219–221. doi:10.1007/s004420050371 CrossRefGoogle Scholar
  10. Del Rı́o M, Font R, Almela C, Vélez D, Montoro R, De Haro-Bailón A (2002) Heavy metals and arsenic uptake by wild vegetation in the Guadiamar river area after the toxic spill of the Aznalcóllar mine. J Biotechnol 98:125–137. doi:10.1016/S0168-1656(02)00091-3
  11. Del Río-Celestino M, Font R, Moreno-Rojas R, De Haro-Bailón A (2006) Uptake of lead and zinc by wild plants growing on contaminated soils. Ind Crops Prod 3:230–237. doi:10.1016/j.indcrop.2006.06.013 CrossRefGoogle Scholar
  12. Ehleringer JR, Mooney HA (1978) Leaf hairs: effects on physiological activity and adaptive value to a desert shrub. Oecologia 37:183–200. doi:10.1007/BF00344990 CrossRefGoogle Scholar
  13. Fuentes-Bazan S, Mansion G, Borsch T (2012a) Towards a species level tree of the globally diverse genus Chenopodium (Chenopodiaceae). Mol Phylogenet Evol 62:359–374. doi:10.1016/j.ympev.2011.10.006 PubMedCrossRefGoogle Scholar
  14. Fuentes-Bazan S, Uotila P, Borsch T (2012b) A novel phylogeny-based generic classification for Chenopodium sensu lato, and a tribal rearrangement of Chenopodioideae (Chenopodiaceae). Willdenowia 42:5–24. doi:10.3372/wi42.42101 CrossRefGoogle Scholar
  15. Hemminga MA, Van Soelen J (1988) Estuarine gradients and the growth and development of Agapanthia villosoviridescens (Coleoptera), a stem-borer of the salt marsh halophyte Aster tripolium. Oecologia 77:307–312. doi:10.1007/BF00378035 CrossRefGoogle Scholar
  16. Hemminga MA, Van Soelen J (1992) The performance of the leaf mining microlepidopteran Bucculatrix maritima (Stt.) on the salt marsh halophyte Aster tripolium (L.) exposed to different salinity conditions. Oecologia 89:422–427. doi:10.1007/BF00317421 Google Scholar
  17. Jou Y, Wang YL, Yen HE (2007) Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum. Funct Plant Biol 34:353–359. doi:10.1071/FP06269 CrossRefGoogle Scholar
  18. Karban R, Karban C, Huntzinger M, Pearse I, Crutsinger G (2010) Diet mixing enhances the performance of a generalist caterpillar, Platyprepia virginalis. Ecol Entomol 35:92–99. doi:10.1111/j.1365-2311.2009.01162.x CrossRefGoogle Scholar
  19. Karimi SH, Ungar IA (1989) Development of epidermal salt hairs in Atriplex triangularis Willd. in response to salinity, light intensity, and aeration. Bot Gaz 150:68–71. doi:10.1086/337749 CrossRefGoogle Scholar
  20. Kenagy GJ (1972) Saltbush leaves: excision of hypersaline tissue by a kangaroo rat. Science 178:1094–1096. doi:10.1126/science.178 4065.1094PubMedCrossRefGoogle Scholar
  21. Kenagy GJ (1973) Adaptations for leaf eating in the Great Basin kangaroo rat, Dipodomys microps. Oecologia 12:383–412. doi:10.1007/BF00345050 CrossRefGoogle Scholar
  22. Krimmel WA, Pearse IS (2013) Sticky plant traps insects to enhance indirect defense. Ecol Lett 16:219–224. doi:10.1111/ele.12032 PubMedCrossRefGoogle Scholar
  23. Leuck DB, Wiseman BR, McMillian WW (1974) Nutritional plant sprays: effect on fall armyworm feeding preferences. J Econ Entomol 67:58–60Google Scholar
  24. Liphschitz N, Waisel Y (1982) Adaptation of plants to saline environments: salt excretion and glandular structure. In: Sen DN, Rajpurohit KN (eds) Contributions to the ecology of halophytes. Junk, The Hague, pp 197–214CrossRefGoogle Scholar
  25. MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquat Bot 68:45–59. doi:10.1016/S0304-3770(00)00105-4 CrossRefGoogle Scholar
  26. Mares MA, Ojeda RA, Borghi CE, Giannoni SM, DmHaz GB, Braun JK (1997) How desert rodents overcome halophytic plant defenses. BioScience 47:699–704Google Scholar
  27. Martel J (1998) Plant-mediated effects of soil salinity on a gall-inducing caterpillar Epiblema scudderiana (Lepidoptera: Tortrieidae) and the influence of feeding guild. Eur J Entomol 95:545–557Google Scholar
  28. Martens SN, Boyd RS (1994) The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 98:379–384. doi:10.1007/BF00324227 CrossRefGoogle Scholar
  29. Molano-Flores B (2001) Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot 88:387–391CrossRefGoogle Scholar
  30. Moogouei R, Borghei M, Arjmandi R (2011) Phytoremediation of stable Cs from solutions by Calendula alata, Amaranthus chlorostachys and Chenopodium album. Ecotoxicol Environ Saf 74:2036–2039. doi:10.1016/j.ecoenv.2011.07.019 PubMedCrossRefGoogle Scholar
  31. Mozafar A, Goodin JR (1970) Vesiculated hairs: a mechanism for salt tolerance in Atriplex halimus L. Plant Physiol 45:62–65. doi:10.1104/pp.45.1.62 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Niveyro SL, Mortensen AG, Fomsgaard IS, Salvo A (2012) Differences among five amaranth varieties (Amaranthus spp.) regarding secondary metabolites and foliar herbivory by chewing insects in the field. Arthropod–Plant Interact 7:235–245. doi:10.1007/s11829-012-9219-y CrossRefGoogle Scholar
  33. Opel MR (2005) Leaf anatomy of Conophytum NE Br. (Aizoaceae). Haseltonia 11:27–52CrossRefGoogle Scholar
  34. Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Carrasco KBR, Martinez EA, Alnayef M, Marotti I, Bosi S (2011) Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol 38:818–831. doi:10.1071/FP11088 CrossRefGoogle Scholar
  35. Osmond CB, Lüttge U, West KR, Pallaghy CK, Shacher-Hill B (1969) Ion absorption in Atriplex leaf tissue II. Secretion of ions to epidermal bladders. Aust J Biol Sci 22:797–814. doi:10.1071/BI9690797 Google Scholar
  36. Rand TA (2002) Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution. Oecologia 132:549–558. doi:10.1007/s00442-002-0989-2 CrossRefGoogle Scholar
  37. Schirmer U, Breckle SW (1982) The role of bladders for salt removal in some Chenopodiaceae (mainly Atriplex species). In: Sen DN, Rajpurohit KN (eds) Contributions to the ecology of halophytes. Junk, The Hague, pp 215–231CrossRefGoogle Scholar
  38. Sokal RR, Rohlf FJ (1969) Biometry. Freeman, San FranciscoGoogle Scholar
  39. Vasconcelos HL (1991) Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295–298. doi:10.1007/BF00325269 CrossRefGoogle Scholar
  40. Waisel Y (1970) Biology of halophytes. Academic, New YorkGoogle Scholar
  41. Walker DJ, Clemente R, Bernal MP (2004) Contrasting effects of manure and compost on soil pH, heavy metal availability and growth of Chenopodium album L. in a soil contaminated by pyritic mine waste. Chemosphere 57:215–224. doi:10.1016/j.chemosphere.2004.05.020 PubMedCrossRefGoogle Scholar
  42. Wang GH, Mopper S (2008) Separate and interacting effects of deer florivory and salinity stress on iris herbivores. Oikos 117:564–570CrossRefGoogle Scholar
  43. Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J Chem Ecol 23:333–346. doi:10.1023/B:JOEC.0000006363.34360.9d CrossRefGoogle Scholar
  44. Weis JS, Weis P (2004) Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environ Int 30:685–700. doi:10.1016/j.envint.2003.11.002 PubMedCrossRefGoogle Scholar
  45. Yábar E, Gianoli E, Echegaray ER (2002) Insect pests and natural enemies in two varieties of quinua (Chenopodium quinoa) at Cusco, Peru. J Appl Entomol 126:275–280. doi:10.1046/j.1439-0418.2002.00664.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Entomology, Graduate Group in Ecology, Center for Population BiologyUniversity of California-DavisDavisUSA

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