Abstract
Calcium oxalate (CaOx) crystals have challenged human curiosity since the advent of microscopy. These crystals are linked to the control of calcium levels in plant cells, but they have also been attributed several other functions, including protection against herbivory. However, the protection offered by CaOx crystals against herbivory may be overstated, as claims have been mainly based on their shapes and hard and indigestible nature rather than on experimental evidence. I contend that it is improbable that a constitutive defense, present since very early in the evolution of plants, has not been superseded by herbivores, especially insects. Here, I present arguments and evidence that suggest that these crystals have low efficiency in protecting plants against herbivores. First, I argue that insects with chewing mouthparts possess a semipermeable structure that protects their midgut, minimizing damage from crystals. Second, the action of CaOx crystals is purely mechanical and similar to other inert materials such as sand. Therefore, CaOx crystals only provide effective protection from herbivory in very particular cases and should not be considered an effective defense without supporting experimental evidence.
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References
Arditti J, Rodriguez E (1982) Dieffenbachia: uses, abuses and toxic constituents: a review. J Ethnopharmacol 5:293–302. https://doi.org/10.1016/0378-8741(82)90015-0
Bauer P, Elbaum R, Weiss IM (2011) Calcium and silicon mineralization in land plants: transport, structure and function. Plant Sci 180:746–756. https://doi.org/10.1016/j.plantsci.2011.01.019
Bernays EA, Chapman R (1987) The evolution of deterrent responses in plant-feeding insects. In: Chapman RF, Bernays EA, Stoffolano JG (eds) Perspectives in chemoreception and behavior. Springer-Verlag, New York, pp 159–173. https://doi.org/10.1007/978-1-4612-4644-2_10
Cortinovis C, Caloni F (2013) Epidemiology of intoxication of domestic animals by plants in Europe. Vet J 197:163–168. https://doi.org/10.1016/j.tvjl.2013.03.007
Dethier VG, Browne LB, Smith CN (1960) The designation of chemical in terms of the responses they ilicit from insects. J Econ Entomol 53:134–136. https://doi.org/10.1093/jee/53.1.134
Doege SJ (2003) The role of natural calcium oxalate crystals in plant defense against chewing insects. Inquiry: The University of Arkansas Undergraduate Research Journal, 4: Article 15. Available at: http://scholarworks.uark.edu/inquiry/vol4/iss1/15
Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427. https://doi.org/10.1007/BF02860532
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Ann Rev Plant Biol 56:41–71. https://doi.org/10.1146/annurev.arplant.56.032604.144106
Gardner DG (1994) Injury to the oral mucous membranes caused by the common houseplant, Dieffenbachia: a review. Or Surg or Med or Pathol 78:631–633. https://doi.org/10.1016/0030-4220(94)90177-5
Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169. https://doi.org/10.1046/j.1469-8137.2002.00519.x
Herbert DA (1924) Stinging crystals in plants. Science 60:204–205. https://doi.org/10.1126/science.60.1548.204-a
Hirata T, Cabrero P, Berkholz DS, Bondeson DP, Ritman EL, Thompson JR, Dow JAT, Romero MF (2012) In vivo Drosophila genetic model for calcium oxalate nephrolithiasis. Am J Physiol Renal Physiology 303:F1555–F1562. https://doi.org/10.1152/ajprenal.00074.2012
Hudgins JW, Krekling T, Franceschi VR (2003) Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism? New Phytol 159:677–690. https://doi.org/10.1046/j.1469-8137.2003.00839.x
Janzen DH (1980) When is it coevolution? Evolution 34:611–612
Karabourniotis G, Horner HT, Bresta P, Nikolopoulos D, Liakopoulos G (2020) New insights on the functions of carbon-calcium-inclusions in plants. New Phytol 228:845–854. https://doi.org/10.1111/nph.16763
Konno K, Inoue TA, Nakamura M (2014) Synergistic defensive function of raphides and protease through the needle effect. PLoS ONE 9(3):e91341. https://doi.org/10.1371/journal.pone.0091341
Korth KL, Doege SJ, Park S-H, Goggin FL, Wang Q, Gomez SK, Liu G, Jia L, Nakata PA (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195. https://doi.org/10.1104/pp.106.076737
Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28:593–599. https://doi.org/10.1007/s10529-006-0022-7
Le Coz CJ, Ducombs G (2006) Plants and plant products. In: Frosch PJ, Menne T, Leppoittevin JP (eds) Contact dermatitis, 4th edn. Springer, Berlin, pp 751–800
Leeuwenhoek A (1675) Microscopical observations. Philos Trans R Soc Lond 10:380–385
Lopresti EF, Grof-Tisza P, Robinson M, Godfrey J (2018) Entrapped sand as a plant defence: effects on herbivore performance and preference. Ecol Entomol 43:154–161. https://doi.org/10.1111/een.12483
Lopresti EF, Karban R (2016) Chewing sandpaper: grit, plant apparency, and plant defense in sand-entrapping plants. Ecology 97:826–833. https://doi.org/10.1890/15-1696.1
Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291. https://doi.org/10.1111/j.1365-2656.2008.01472.x
Mello MO, Silva-Filho MC (2002) Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms. Braz J Plant Physiol 14:71–81. https://doi.org/10.1590/S1677-04202002000200001
Mohan S, Ma PWK, Pechan T, Bassford ER, Williams WP, Luthe DS (2006) Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28. https://doi.org/10.1016/j.jinsphys.2005.08.011
Nagaoka S, Katayama H, Fujibayashi Y, Sugimura Y (2010) Calcium oxalate crystals in mulberry leaves: no negative effect on feeding the silkworm, Bombyx mori. J Insect Biotech Sericol 79:71–74. https://doi.org/10.11416/jibs.79.2_071
Nakata PA (2003) Advances in our understanding of calcium oxalate crystal formation and function in plants. Plant Sci 164:901–909. https://doi.org/10.1016/S0168-9452(03)00120-1
Nelson LS, Shih RD, Balick MJ (2007) Handbook of poisonous and injurious plants. Springer-Verlag, Berlin
Paiva EAS (2019) Are calcium oxalate crystals a dynamic calcium store in plants? New Phytol 223:1707–1711. https://doi.org/10.1111/nph.15912
Park S, Doege SJ, Nakata PA, Korth KL (2009) Medicago truncatula-derived calcium oxalate crystals have a negative impact on chewing insect performance via their physical properties. Entomol Exp Appl 131:208–215. https://doi.org/10.1111/j.1570-7458.2009.00846.x
Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defence protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci USA 99:13319–13323. https://doi.org/10.1073/pnas.202224899
Perera CO, Hallett IC, Nguyen TT, Charles JC (1990) Calcium oxalate crystals: the irritant factor in kiwifruit. J Food Sci 55:1066–1069. https://doi.org/10.1111/j.1365-2621.1990.tb01599.x
Peschiutta ML, Bucci SJ, Goldstein G, Scholz FG (2020) Leaf herbivory and calcium oxalate crystal production in Prunus avium. Arthropod-Plant Inte 14:727–732. https://doi.org/10.1007/s11829-020-09781-6
Rahman MM, Abdullah RB, Wan Khadijah WE (2013) A review of oxalate poisoning in domestic animals: tolerance and performance aspects. J Anim Physiol an Nutr 97:605–614. https://doi.org/10.1111/j.1439-0396.2012.01309.x
Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864. https://doi.org/10.1038/35081193
Ruiz N, Ward D, Saltz D (2002) Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defence? Funct Ecol 16:99–105. https://doi.org/10.1046/j.0269-8463.2001.00594.x
Sanz PMD, Reig RMD (1992) Clinical and pathological findings in fatal plant oxalosis - a review. Am J Foren Med Path 13:342–345
Showler AT (2002) Effects of kaolin-based particle film application on boll weevil (Coleoptera: Curculionidae) injury to cotton. J Econ Entomol 95:754–762. https://doi.org/10.1603/0022-0493-95.4.754
Stout MJ (2013) Re-evaluating the conceptual framework for applied research on host-plant resistance. Insect Sci 20:263–272. https://doi.org/10.1111/1744-7917.12011
Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem 47:47–51. https://doi.org/10.1002/arch.1036
Wang P, Granados RR (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem 47:110–118. https://doi.org/10.1002/arch.1041
War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Plant defence against herbivory and insect adaptations. AoB PLANTS 10:ply037; https://doi.org/10.1093/aobpla/ply037
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 2:333–346. https://doi.org/10.1023/B:JOEC.0000006363.34360.9d
Yoshida M, Cowgill SE, Wightman JA (1995) Mechanism of resistance to Helicoverpa armigera (Lepidoptera, Noctuidae) in chickpea: role of oxalic acid in leaf exudate as an antibiotic factor. J Econ Entomol 88:1783–1786. https://doi.org/10.1093/jee/88.6.1783
Yoshihara T, Sogawa K, Pathak MD, Juliano BO, Sakamura S (1980) Oxalic acid as a sucking inhibitor of the brown planthopper in rice (Delphacidae, Homoptera). Entomol Exp Appl 27:149–155. https://doi.org/10.1111/j.1570-7458.1980.tb02959.x
Acknowledgements
I thank Dr. Clemens Schlindwein, Dr. Denise M. T. Oliveira, and Dr. Alberto Teixido for their helpful comments and suggestions. I am also indebted to Paula Roig, Dr. Harry Horner, and an anonymous reviewer for improving the article with valuable suggestions and comments. This work is dedicated to the memory of my greatest master, Olimpio Vieira de Paiva, whom I have always taken as a model.
Funding
This study was funded in part by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil, process 305638/2018‒1).
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Communicated by: Lukasz Stepien and Paula Roig-Boixeda
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Paiva, É.A.S. Do calcium oxalate crystals protect against herbivory?. Sci Nat 108, 24 (2021). https://doi.org/10.1007/s00114-021-01735-z
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DOI: https://doi.org/10.1007/s00114-021-01735-z