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Plant function and evolutionary biology
RESEARCH ARTICLE

Drought resistance or herbivory defense strategy? Oxalate druses function in a forage xeric species

D. F. Jaume https://orcid.org/0009-0007-0303-1127 A * , Y. I. Pelliza A , A. Nanni A and M. Tadey A
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A Grupo De Ecología De Ambientes Áridos – IdEAS, INIBIOMA-CONICET, San Carlos de Bariloche, Río Negro, Argentina.


Handling Editor: Nieves Fernandez-Garcia

Functional Plant Biology 52, FP24299 https://doi.org/10.1071/FP24299
Submitted: 20 November 2024  Accepted: 7 February 2025  Published: 27 February 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Oxalate druse synthesis in plants helps to reduce drought stress by maintaining osmotic balance and might also act as a defence against herbivory by reducing nutritional quality. This study experimentally investigated the role of druses in Atriplex lampa under drought and herbivory treatments. We propose that both stressors trigger druse synthesis. Furthermore, if druse production is an adaptation to stress, the allocation of resources to other physiological functions should not be affected. These hypotheses were experimentally tested under greenhouse and natural field conditions. Leaves of A. lampa were collected from eight rangelands in Monte Desert in Argentina, which shared similar environmental characteristics but differed in stocking rates. The manipulative experiment in the greenhouse consisted in applying drought and herbivory treatments to A. lampa seedlings. The highest druse abundance was observed at intermediate stocking rates, suggesting resource limitation for druse synthesis at extreme stocking rates. The adaptive advantage of druse synthesis was evident only for drought stress treatment, where higher druse abundance was correlated with improved growth rates. When both stressors were combined, there was no difference in druse abundance with respect to control treatment, indicating that herbivory negatively influenced the adaptive response to drought. Druse synthesis is an adaptation to drought that is susceptible to herbivory stress.

Keywords: Atriplex lampa, calcium oxalate druses, drought, druse abundance, dryland, herbivory, livestock grazing, natural selection, plant defenses, tolerance mechanisms.

References

Apóstolo NM (2005) Caracteres anatómicos de la vegetación costera del Río Salado (Noroeste de la provincia de Buenos Aires, Argentina). Boletín de la Sociedad Argentina de Botánica 40(3–4), 215-227 Available at https://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S1851-23722005000200008&lng=es&nrm=iso.
| Google Scholar |

Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221-235.
| Crossref | Google Scholar | PubMed |

Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proceedings of the National Academy of Sciences of the United States of America 97(26), 14412-14417.
| Crossref | Google Scholar |

Blumenthal DM, Mueller KE, Kray JA, Ocheltree TW, Augustine DJ, Wilcox KR (2020) Traits link drought resistance with herbivore defence and plant economics in semi-arid grasslands: the central roles of phenology and leaf dry matter content. Journal of Ecology 108(6), 2336-2351.
| Crossref | Google Scholar |

Busso CA, Bonvissuto GL (2009) Soil seed bank in and between vegetation patches in arid Patagonia, Argentina. Environmental and Experimental Botany 67(1), 188-195.
| Crossref | Google Scholar |

Busso CA, Fernández OA (2017) Arid and semi-arid rangelands: two thirds of Argentina. In ‘Climate variability impacts on land use and livelihoods in drylands’. (Eds MK Gaur, VR Squires) pp. 261–291. (Springer International Publishing: Cham)

Cabrera AL (1971) Fitogeografía de la República Argentina. Boletín de la Sociedad Argentina de Botánica XIV, 1-50.
| Google Scholar |

Ci HC, He XD, Li R, Wu W, Xue PP, Gao YB, Zhao HL (2010) Characteristics of plant calcium fractions for 25 species in Tengger Desert. Sciences in Cold and Arid Regions 2, 168-174.
| Google Scholar |

Cibils AF, Swift DM, McArthur ED (1998) Plant-herbivore interactions in Atriplex: current state of knowledge. USDA Forest Service – General Technical Report RMRS-GTR.

Çinbilgel ˙I, Karadeniz A, Gökceoglu M (2007) Morphological and anatomical study on Endemic saponaria pamphylica Boiss. & Heldr. (Caryophyllaceae). Journal of Applied Biological Sciences 1(2), 19-25.
| Google Scholar |

Cleland EE, Goodale UM (2019) Co-limitation by nitrogen and water constrains allocation response to drought in deciduous and evergreen shrubs in a semi-arid ecosystem. Plant Ecology 220, 213-225.
| Crossref | Google Scholar |

Coughenour MB (1985) Graminoid responses to grazing by large herbivores: adaptations, exaptations, and interacting processes. Annals of the Missouri Botanical Garden 72(4), 852-863.
| Crossref | Google Scholar |

Cuadra VP, Cambi V (2017) Calcium oxalate crystals in halo-xerophytic species and their macropatterns trends. The importance of a multivariate analysis considering soil characteristics. Flora 234, 187-194.
| Crossref | Google Scholar |

Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences 72, 673-689.
| Crossref | Google Scholar | PubMed |

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In ‘Sustainable agriculture’. (Eds E Lichtfouse, M Navarrete, P Debaeke, S Véronique, C Alberola) pp. 153–188. (Springer: Dordrecht)

Farooq M, Hussain M, Wakeel A, Siddique KHM (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agronomy for Sustainable Development 35, 461-481.
| Crossref | Google Scholar |

Fernández ME (2020) Estrategias de tres especies arbustivas del Monte frente al estrés hídrico y su relevancia para la restauración. Ecología Austral 30(2), 175-330.
| Crossref | Google Scholar |

Franceschi V (2001) Calcium oxalate in plants. Trends in Plant Science 6(7), 331.
| Crossref | Google Scholar |

Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41-71.
| Crossref | Google Scholar |

Golluscio RA, Cavagnaro FP, Valenta MD (2011) Arbustos de la estepa patagónica: ¿adaptados a tolerar la sequía o el pastoreo? Ecologia Austral 21(1), 61-70.
| Google Scholar |

Gómez-Espinoza O, González-Ramírez D, Méndez-Gómez J, Guillén-Watson R, Medaglia-Mata A, Bravo LA (2021) Calcium oxalate crystals in leaves of the extremophile plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae). Plants 10(9), 1787.
| Google Scholar |

Guevara JC, Grünwaldt EG, Estevez OR, Bisigato AJ, Blanco LJ, Biurrun FN, Ferrando CA, Chirino CC, Morici E, Fernández B, Allegretti LI, Passera CB (2009) Range and livestock production in the Monte Desert, Argentina. Journal of Arid Environments 73(2), 228-237.
| Google Scholar |

Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8(4), 157-178.
| Crossref | Google Scholar |

Hothorn T, Bretz F, Westfall P (2017) Package ‘multcomp’ ‑ Simultaneous Inference in General Parametric Models. Available at https://cran.r-project.org/web/packages/multcomp/multcomp.pdf

Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant 7(8), 1267-1287.
| Crossref | Google Scholar | PubMed |

Jaume DF, Souto CP, Tadey M (2023) Herbivoría y sequía en el Monte: factores de estrés que afectan el crecimiento y el ataque de insectos en hojas y semillas de una especie forrajera. Ecología Austral 33(1), 074-088.
| Crossref | Google Scholar |

Jáuregui-Zuñiga D, Moreno Cárcamo A (2004) La biomineralización del oxalato de calcio en plantas: retos y potencial. Revista de Educación Bioquímica 23(1), 18-23.
| Google Scholar |

Kadereit G, Mavrodiev EV, Zacharias EH, Sukhorukov AP (2010) Molecular phylogeny of Atripliceae (Chenopodioideae, Chenopodiaceae): Implications for systematics, biogeography, flower and fruit evolution, and the origin of C4 photosynthesis. American Journal of Botany 97, 1664-1687.
| Crossref | Google Scholar |

Karabourniotis G, Horner HT, Bresta P, Nikolopoulos D, Liakopoulos G (2020) New insights into the functions of carbon–calcium inclusions in plants. New Phytologist 228(3), 845-854.
| Crossref | Google Scholar | PubMed |

Karban R, Agrawal AA, Mangel M (1997) The benefits of induced defenses against herbivores. Ecology 78(5), 1351-1355.
| Crossref | Google Scholar |

Karimi SH, Ungar IA (1986) Oxalate and inorganic ion concentrations in Atriplex triangularis Willd. Organs in response to salinity, light level, and aeration. Botanical Gazette 147(1), 65-70.
| Crossref | Google Scholar |

Khan MI, Pandith SA, Shah MA, Reshi ZA (2023) Calcium oxalate crystals, the plant ‘Gemstones’: insights into their synthesis and physiological implications in plants. Plant and Cell Physiology 64(10), 1124-1138.
| Crossref | Google Scholar | PubMed |

Kolyva F, Nikolopoulos D, Bresta P, Liakopoulos G, Karabourniotis G, Rhizopoulou S (2023) Acclimation of the Grapevine Vitis vinifera L. cv. Assyrtiko to water deficit: coordination of structural and functional leaf traits and the dynamic of calcium oxalate crystals. Plants 12(23), 3992.
| Crossref | Google Scholar | PubMed |

Le Rudulier D, Strom AR, Dandekar AM, Smith LT, Valentine RC (1984) Molecular biology of osmoregulation. Science 224(4653), 1064-1068.
| Crossref | Google Scholar | PubMed |

Loeser MRR, Sisk TD, Crews TE (2007) Impact of grazing intensity during drought in an Arizona grassland. Conservation Biology 21(1), 87-97.
| Crossref | Google Scholar | PubMed |

Mazen AMA (2004) Calcium oxalate deposits in leaves of Corchorus olitorius as related to accumulation of toxic metals. Russian Journal of Plant Physiology 51, 281-285.
| Crossref | Google Scholar |

McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40(3), 329-336.
| Crossref | Google Scholar |

Milchunas DG, Sala OE, Lauenroth WK (1988) A generalized model of the effects of grazing by large hHerbivores on grassland community structure. The American Naturalist 132(1), 87-106.
| Google Scholar |

Nguyen D, Rieu I, Mariani C, van Dam NM (2016) How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Molecular Biology 91, 727-740.
| Crossref | Google Scholar | PubMed |

Oesterheld M, Aguiar MR, Paruelo JM (1998) Ecosistemas patagónicos. Ecología Austral 8, 75-84.
| Google Scholar |

Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167, 1-9.
| Crossref | Google Scholar | PubMed |

Ounaissia K, Ailane L, Laredj H, Bennadja S, Smati D (2019) Anatomical Study of Atriplex halimus L. (Guettaf) growing under the climatic conditions of Biskra – Algeria. International Journal of Innovative Approaches in Agricultural Research 3(4), 698-705.
| Crossref | Google Scholar |

Paiva EAS (2019) Are calcium oxalate crystals a dynamic calcium store in plants? New Phytologist 223(4), 1707-1711.
| Crossref | Google Scholar | PubMed |

Paruelo JM, Jobbágy EG, Sala OE (1998) Biozones of patagonia (Argentina). Ecología Austral 8(2), 145-153.
| Google Scholar |

Peguero-Pina JJ, Vilagrosa A, Alonso-Forn D, Ferrio JP, Sancho-Knapik D, Gil-Pelegrín E (2020) Living in drylands: functional adaptations of trees and shrubs to cope with high temperatures and water scarcity. Forests 11(10), 1028.
| Crossref | Google Scholar |

Pelliza YI, Souto CP, Tadey M (2022) How does domestic livestock affect plant biomass and fecundity of different successional types of species in Patagonian Monte? Ecología Austral 32, 453-468.
| Google Scholar |

Peschiutta ML, Bucci SJ, Scholz FG, Goldstein G (2016) Compensatory responses in plant-herbivore interactions: Impacts of insects on leaf water relations. Acta Oecologica 73, 71-79.
| Crossref | Google Scholar |

R Development Core Team (2018) R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/

Roig-Juñent S, Flores G, Claver S, Debandi G, Marvaldi A (2001) Monte Desert (Argentina): insect biodiversity and natural areas. Journal of Arid Environments 47(1), 77-94.
| Crossref | Google Scholar |

Sankaran M, Augustine DJ (2004) Large herbivores suppress decomposer abumdance in a semiarid grazing ecosystem. Ecology 85, 1052-1061.
| Crossref | Google Scholar |

Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: An open platform for biomedical image analysis. Molecular Reproduction & Development 82, 518-529.
| Crossref | Google Scholar |

Solans M, Pelliza YI, Tadey M (2022) Inoculation with native actinobacteria may improve desert plant growth and survival with potential use for restoration practices. Microbial Ecology 83, 380-392.
| Crossref | Google Scholar | PubMed |

Souto CP, Tadey M (2018) Livestock effects on genetic variation of creosote bushes in patagonian rangelands. Environmental Conservation 46, 59-66.
| Crossref | Google Scholar |

StatSoft (2002) STATISTICA (data analysis software system), version 10. StatSoft, Inc. Available at www.statsoft.com

Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annual Review of Ecology, Evolution, and Systematics 31, 565-595.
| Crossref | Google Scholar |

Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution 14(5), 179-185.
| Crossref | Google Scholar | PubMed |

Tadey M (2006) Grazing without grasses: effects of introduced livestock on plant community composition in an arid environment in northern Patagonia. Applied Vegetation Science 9(1), 109-116.
| Crossref | Google Scholar |

Tadey M (2020) Reshaping phenology: Grazing has stronger effects than climate on flowering and fruiting phenology in desert plants. Perspectives in Plant Ecology, Evolution and Systematics 42, 125501.
| Crossref | Google Scholar |

Tadey M (2023) Cascading effects of livestock grazing on insect functional groups associated to flowers in arid lands. Agricultural and Forest Entomology 25(3), 375-390.
| Crossref | Google Scholar |

Tadey M, Farji-Brener AG (2007) Indirect effects of exotic grazers: livestock decreases the nutrient content of refuse dumps of leaf-cutting ants through vegetation impoverishment. Journal of Applied Ecology 44(6), 1209-1218.
| Crossref | Google Scholar |

Thakur A, Sharma V, Thakur A (2019) An overview of anti-nutritional factors in food. International Journal of Chemical Studies 7, 2472-2479.
| Google Scholar |

Tooulakou G, Giannopoulos A, Nikolopoulos D, Bresta P, Dotsika E, Orkoula MG, Kontoyannis CG, Fasseas C, Liakopoulos G, Klapa MI, Karabourniotis G (2016) Reevaluation of the plant “gemstones”: Calcium oxalate crystals sustain photosynthesis under drought conditions. Plant Signaling & Behavior 11(9), e1215793.
| Crossref | Google Scholar |

Trione SO, Passera CB (1993) Growth and nitrogen status of Atriplex lampa seedlings under different water regimes. Journal of Arid Environments 25(3), 331-341.
| Crossref | Google Scholar |

Valladares F, Vilagrosa A, Peñuelas J, Ogaya R, Camarero JJ, Corcuera L, Sisó S, Gil-Pelegrín E (2004) Estrés hídrico: ecofisiología y escalas de la sequía. In ‘Ecología del bosque mediterráneo en un mundo cambiante, Vol. 2’. pp. 165–192. (Ministerio de Medio Ambiente Madrid)

Vallentine JF (2001) ‘Grazing management.’ (Elservier)

Villagra PE, Giordano C, Alvarez JA, Cavagnaro JB, Guevara A, Sartor C, Passera CB, Greco S (2011) Ser planta en el desierto: estrategias de uso de agua y resistencia al estrés hídrico en el Monte Central de Argentina. Ecologia Austral 21, 29-42.
| Google Scholar |

Wilkinson DM (1999) The disturbing history of intermediate disturbance. Oikos 84, 145-147.
| Crossref | Google Scholar |