Abstract
An experimental assessment of the defence hypothesis of nickel (Ni) hyperaccumulation in Alyssum was lacking. Also, to date no study had investigated the effects of hyperaccumulator litter on a detritivore species. We performed several experiments with model arthropods representatives of two trophic levels: Tribolium castaneum (herbivore) and Porcellio dilatatus (detritivore). In no-choice trials using artificial food disks with different Ni concentrations, T. castaneum fed significantly less as Ni concentration increased and totally rejected disks with the highest Ni concentration. In choice tests, insects preferred disks without Ni. In the no-choice experiment, mortality was low and did not differ significantly among treatments. Hence, this suggested a deterrent effect of high Ni diet. Experiments with P. dilatatus showed that isopods fed A. pintodasilvae litter showed significantly greater mortality (83%) than isopods fed litter from the non-hyperaccumulator species Iberis procumbens (8%), Micromeria juliana (no mortality) or Alnus glutinosa (no mortality). Also, isopods consumed significantly greater amounts of litter from the non-hyperaccumulator plant species. The behaviour of isopods fed A. pintodasilvae litter suggested an antifeedant effect of Ni, possibly due to post-ingestive toxic effects. Our results support the view that Ni defends the Portuguese serpentine hyperaccumulator A. pintodasilvae against herbivores, indicating that Ni can account both for feeding deterrence and toxic effects. The effects of hyperaccumulator litter on the detritivore P. dilatatus suggest that the activity of these important organisms may be significantly impaired with potential consequences on the decomposition processes.
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Alonso-Amelot ME, Avila JL, Otero LD, Mora F, Wolff B (1994) A new bioassay for testing-plant extracts and pure compounds using red flour beetle Tribolium castaneum Herbst. J Chem Ecol 20:1161–1177
Behmer ST, Lloyd CM, Raubenheimer D, Stewart-Clark J, Knight J, Leighton RS, Harper FA, Smith JAC (2005) Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Funct Ecol 19:55–66
Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567
Boyd RS, Davis MA, Wall MA, Balkwill K (2002) Nickel defends the South African hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mollusca: Pulmonidae). Chemoecology 12:91–97
Boyd RS, Jhee EM (2005) A test of elemental defence against slugs by Ni in hyperaccumulator and non-hyperaccumulator Streptanthus species. Chemoecology 15:179–185
Boyd RS, Martens SN (1994) Nickel hyperaccumulated by Thlaspi montanum var montanum is acutely toxic to an insect herbivore. Oikos 70:21–25
Boyd RS, Martens SN (1992) The raison d’être for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd, Andover, pp 279–289
Boyd RS, Martens SN (1998) The significance of metal hyperaccumulation for biotic interactions. Chemoecology 8:1–7
Boyd RS, Moar WJ (1999) The defensive function of Ni in plants: response of the polyphagous herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae). Oecologia 118:218–224
Boyd RS, Shaw JJ, Martens SN (1994) Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81:294–300
Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57
Brooks RR, Radford CC (1978) Nickel accumulation by European species of genus Alyssum. P Roy Soc Lond B Bio 200:217–224
Caseiro I, Santos S, Sousa JP, Nogueira AJA, Soares AMVM (2000) Optimization of culture conditions of Porcellio dilatatus (Crustacea: Isopoda) for laboratory test development. Ecotox Environ Safe 47:285–291
Coleman CM, Boyd RS, Eubanks MD (2005) Extending the elemental defence hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. J Chem Ecol 31:1669–1681
Dudley TR (1986) A new nickelophilous species of Alyssum (Cruciferae) from Portugal, Alyssum pintodasilvae T. R. Dudley. Feddes Repert 97:135–138
Ghaderian YSM, Lyon AJE, Baker AJM (2000) Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp. New Phytol 146:219–224
Hanson B, Garifullina GF, Lindblom SD, Wangeline A, Ackley A, Kramer K, Norton A P, Lawrence CB, Pilon-Smits EAH (2003) Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol 159:461–469
Hanson B, Lindblom SD, Loeffler ML, Pilon-Smits EAH (2004) Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity. New Phytol 162:655–662
Huitson SB, Macnair MR (2003) Does zinc protect the zinc hyperaccumulator Arabidopsis halleri from herbivory by snails? New Phytol. 159:453–459
Jhee EM, Boyd RS, Eubanks MD, Davis MA (2006) Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Plutella xylostella (Lepidoptera : Plutellidae). Plant Ecol 183:91–104
Jhee EM, Dandridge KL, Christy AM, Pollard AJ (1999) Selective herbivory on low-zinc phenotypes of the hyperaccumulator Thlaspi caerulescens (Brassicaceae). Chemoecology 9:93–95
Jiang RF, Ma DY, Zhao FJ, McGrath SP (2005) Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol 167:805–813
Martens SN, Boyd RS (2002) The defensive role of Ni hyperaccumulation by plants: a field experiment. Am J Bot 89:998–1003
Martens SN, Boyd RS (1994) The ecological significance of nickel hyperaccumulation - a plant-chemical defense. Oecologia 98:379–384
Menezes de Sequeira E, Pinto da Silva A R (1992) The ecology of serpentinized areas of north-east Portugal. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks. A world view. Kluwer Academic Publishers, Dordrecht, pp 169–197
Noret N, Meerts P, Tolrà R, Poschenrieder C, Barceló J, Escarre J (2005) Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytol 165:763–772
Ó Ceallacháin DP, Ryan MF (1977) Production and perception of pheromones by beetle Tribolium confusum. J Insect Physiol 23:1303–1309
Peterson LR, Trivett V, Baker AJM, Aguiar C, Pollard AJ (2003) Spread of metals through an invertebrate food chain as influenced by a plant that hyperaccumulates nickel. Chemoecology 13:103–108
Pinto da Silva AR (1970) A flora e a vegetação das áreas ultrabásicas do nordeste transmontano. Agronomia Lusit 30:175–364
Pollard AJ (2000) Metal hyperaccumulation: a model system for coevolutionary studies. New Phytol 146:179–181
Pollard AJ, Baker AJM (1997) Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens (Brassicaceae). New Phytol 135:655–658
Raessler M, Rothe J, Hilke I (2005) Accurate determination of Cd, Cr, Cu and Ni in woodlice and their skins - is moulting a means of detoxification? Sci Total Environ 337:83–90
Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley & Sons, New York, pp 193–229
Ribeiro S, Guilhermino L, Sousa JP, Soares AMVM (1999) A novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods. Ecotox Environ Safe 44:287–293
Ribeiro S, Sousa JP, Nogueira AJA, Soares AMVM (2001) Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotox Environ Safe 49:131–138
Sousa JP, Vingada JV, Loureiro S, Gama MM, Soares AMVM (1998) Effects of introduced exotic tree species on growth, consumption and assimilation rates of the soil detritivore Porcellio dilatatus (Crustacea: Isopoda). Appl Soil Ecol 9:399–403
SPSS 2005 SPSS for Windows, Release 14.0, Chicago, IL, USA
Swain T, Hillis WE (1959) The phenolic constituents of Prunus domestica. I. The quantitative analysis of phenolic constituents. J Sci Food Agr 10:63–68
Szlávecz K, Pobozsny M (1995) Coprophagy in isopods and diplopods: a case for indirect intercation. Acta Zool Fennica 196:124–128
Van Wensem J, Verhoef HA, Van Straalen NM (1993) Litter degradation stage as a prime factor for isopod interaction with mineralization processes. Soil Biol Biochem 25:1175–1183
Whiting SN, Neumann PM, Baker AJM (2003) Nickel and zinc hyperaccumulation by Alyssum murale and Thlaspi caerulescens (Brassicaceae) do not enhance survival and whole-plant growth under drought stress. Plant Cell Environ 6:351–360
Zar JH (1996) Biostatistical Analysis. Prentice Hall International, Upper Saddle River, 662 pp
Zhang L, Angle JS, Delorme T, Chaney RL (2005) Degradation of Alyssum murale biomass in soil. Int J Phytorem 7:169–176
Zidar P, Bozic J, Strus J (2005) Behavioral response in the terrestrial isopod Porcellio scaber (Crustacea) offered a choice of uncontaminated and cadmium-contaminated food. Ecotoxicology 14:493–502
Zidar P, Drobne D, Strus J, Van Gestel CAM, Donker M (2004) Food selection as a means of Cu intake reduction in the terrestrial isopod Porcellio scaber (Crustacea, Isopoda). Appl Soil Ecol 25:257–265
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Gonçalves, M.T., Gonçalves, S.C., Portugal, A. et al. Effects of nickel hyperaccumulation in Alyssum pintodasilvae on model arthropods representatives of two trophic levels. Plant Soil 293, 177–188 (2007). https://doi.org/10.1007/s11104-006-9174-4
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DOI: https://doi.org/10.1007/s11104-006-9174-4