Response of extrafloral nectar production to elevated atmospheric carbon dioxide
Belinda Fabian A B , Brian J. Atwell A and Lesley Hughes AA Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia.
B Corresponding author. Email: belinda.fabian@mq.edu.au
Australian Journal of Botany 66(7) 479-488 https://doi.org/10.1071/BT18012
Submitted: 18 January 2018 Accepted: 14 September 2018 Published: 15 October 2018
Abstract
Extrafloral nectar attracts ants, whose presence provides protection for the plant against herbivores. Extrafloral nectar is thus a critical component of many plant–insect mutualisms worldwide, so environmental perturbations that alter extrafloral nectar production or composition could be disruptive. The carbon–nutrient balance hypothesis predicts that under elevated CO2 the total volume of extrafloral nectar will increase but the proportion of the foliar carbohydrate pool secreted as extrafloral nectar will decrease, without any change in the sugar composition of the extrafloral nectar. We investigated the impact of elevated atmospheric CO2 on extrafloral nectar in an Australian wild cotton species, Gossypium sturtianum J.H.Willis. Under elevated CO2 there was an increase in the proportion of leaves actively producing nectar and a decrease in the nectar volume per active leaf. Elevated CO2 did not affect the total volume or composition of extrafloral nectar, but there was a change in how the nectar was distributed within the leaf canopy, as well as evidence of increased turnover of leaves and earlier onset of flowering. By the end of the study, there was no difference in the total resources allocated to extrafloral nectar under elevated CO2, which contrasts with the predictions of the carbon-nutrient balance hypothesis. Developmental changes, however, could affect the timing of extrafloral nectar production which could, in turn, alter the foraging patterns of ants and their defence of plants.
Additional keywords: carbon dioxide, climate change and high CO2, extrafloral nectaries, Gossypium sturtianum, mutualism, plant defense.
References
Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell & Environment 30, 258–270.| The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions.Crossref | GoogleScholarGoogle Scholar |
Australian National Botanic Gardens (2012) Growing native plants: Gossypium sturtianum. Available at http://www.anbg.gov.au/gnp/interns-2002/gossypium-sturtianum.html [Verified 12 September 2014]
Baker HG, Opler PA, Baker I (1978) A comparison of the amino acid complements of floral and extrafloral nectars. Botanical Gazette 139, 322–332.
| A comparison of the amino acid complements of floral and extrafloral nectars.Crossref | GoogleScholarGoogle Scholar |
Bentley BL (1977a) The protective function of ants visiting the extrafloral nectaries of Bixa Orellana (Bixaceae). Journal of Ecology 65, 27–38.
| The protective function of ants visiting the extrafloral nectaries of Bixa Orellana (Bixaceae).Crossref | GoogleScholarGoogle Scholar |
Bentley BL (1977b) Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics 8, 407–427.
| Extrafloral nectaries and protection by pugnacious bodyguards.Crossref | GoogleScholarGoogle Scholar |
Bentley B, Elias TS (1983) ‘The biology of nectaries.’ (Columbia University Press: New York)
Bixenmann RJ, Coley PD, Kursar TA (2011) Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant–plant mutualism? Oecologia 165, 417–425.
| Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant–plant mutualism?Crossref | GoogleScholarGoogle Scholar |
Blüthgen N, Gottsberger G, Fiedler K (2004) Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecology 29, 418–429.
| Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest.Crossref | GoogleScholarGoogle Scholar |
Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368.
| Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Crossref | GoogleScholarGoogle Scholar |
Corbet SA (2003) Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34, 1–10.
| Nectar sugar content: estimating standing crop and secretion rate in the field.Crossref | GoogleScholarGoogle Scholar |
Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4, 43–54.
| Elevated CO2 reduces the nitrogen concentration of plant tissues.Crossref | GoogleScholarGoogle Scholar |
Dag A, Eisikowitch D (2000) The effect of carbon dioxide enrichment on nectar production in melons under greenhouse conditions. Journal of Apicultural Research 39, 88–89.
| The effect of carbon dioxide enrichment on nectar production in melons under greenhouse conditions.Crossref | GoogleScholarGoogle Scholar |
DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiology 160, 1677–1685.
| Climate change: resetting plant-insect interactions.Crossref | GoogleScholarGoogle Scholar |
Eamus D (1991) The interaction of rising CO2 and temperatures with water use efficiency. Plant, Cell & Environment 14, 843–852.
| The interaction of rising CO2 and temperatures with water use efficiency.Crossref | GoogleScholarGoogle Scholar |
Erhardt A, Rusterholz HP (1997) Effects of elevated CO2 on flowering phenology and nectar production. Acta Oecologica 18, 249–253.
| Effects of elevated CO2 on flowering phenology and nectar production.Crossref | GoogleScholarGoogle Scholar |
Erhardt A, Rusterholz HP, Stocklin J (2005) Elevated carbon dioxide increases nectar production in Epilobium angustifolium L. Oecologia 146, 311–317.
| Elevated carbon dioxide increases nectar production in Epilobium angustifolium L.Crossref | GoogleScholarGoogle Scholar |
Escalante-Perez M, Jaborsky M, Lautner S, Fromm J, Muller T, Dittrich M, Kunert M, Boland W, Hedrich R, Ache P (2012) Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores. Plant Physiology 159, 1176–1191.
| Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores.Crossref | GoogleScholarGoogle Scholar |
González-Teuber M, Silva Bueno JC, Heil M, Boland W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLoS One 7, e46598
| Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service.Crossref | GoogleScholarGoogle Scholar |
Heil M (2011) Nectar: generation, regulation and ecological functions. Trends in Plant Science 16, 191–200.
| Nectar: generation, regulation and ecological functions.Crossref | GoogleScholarGoogle Scholar |
Heil M (2015) Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annual Review of Entomology 60, 213–232.
| Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs.Crossref | GoogleScholarGoogle Scholar |
Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology Evolution and Systematics 34, 425–453.
| Protective ant-plant interactions as model systems in ecological and evolutionary research.Crossref | GoogleScholarGoogle Scholar |
Heil M, Fiala B, Baumann B, Linsenmair KE (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology 14, 749–757.
| Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius.Crossref | GoogleScholarGoogle Scholar |
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology 67, 283–335.
| The dilemma of plants: to grow or defend.Crossref | GoogleScholarGoogle Scholar |
Hirschmüller H (1953) Physical properties of sucrose. In ‘Principles of sugar technology’. (Ed. P Honig) pp. 18–74. (Elsevier Science: Amsterdam, The Netherlands)
Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249–275.
| Coevolution of mutualism between ants and acacias in Central America.Crossref | GoogleScholarGoogle Scholar |
Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Functional Ecology 25, 348–357.
| The multiple faces of indirect defences and their agents of natural selection.Crossref | GoogleScholarGoogle Scholar |
Koptur S, Palacios-Rios M, Díaz-Castelazo C, Mackay WP, Rico-Gray V (2013) Nectar secretion on fern fronds associated with lower levels of herbivore damage: field experiments with a widespread epiphyte of Mexican cloud forest remnants. Annals of Botany 111, 1277–1283.
| Nectar secretion on fern fronds associated with lower levels of herbivore damage: field experiments with a widespread epiphyte of Mexican cloud forest remnants.Crossref | GoogleScholarGoogle Scholar |
Kwok KE, Laird RA (2012) Plant age and the inducibility of extrafloral nectaries in Vicia faba. Plant Ecology 213, 1823–1832.
| Plant age and the inducibility of extrafloral nectaries in Vicia faba.Crossref | GoogleScholarGoogle Scholar |
Lake JC, Hughes L (1999) Nectar production and floral characteristics of Tropaeolum majus L. grown in ambient and elevated carbon dioxide. Annals of Botany 84, 535–541.
| Nectar production and floral characteristics of Tropaeolum majus L. grown in ambient and elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Le Quéré C, Andrew RM, Canadell JG, Sitch S, Korsbakken JI, Peters GP, Manning AC, Boden TA, Tans PP, Houghton RA, et al. (2016) Global carbon budget 2016. Earth System Science Data 8, 605–649.
| Global carbon budget 2016.Crossref | GoogleScholarGoogle Scholar |
Leakey ADB, Ainsworth EA, Bernacchi CJ, Zhu X, Long SP, Ort DR (2012) Photosynthesis in a CO2-rich atmosphere. In ‘Photosynthesis: plastid biology, energy conversion and carbon assimilation’. (Eds JJ Eaton-Rye, BC Tripathy, TD Sharkey) pp. 733–768. (Springer: Dordrecht, The Netherlands)
Marazzi B, Bronstein JL, Koptur S (2013) The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Annals of Botany 111, 1243–1250.
| The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges.Crossref | GoogleScholarGoogle Scholar |
Marov G, Dowling J (1990) Sugar in beverages. In ‘Sugar: user’s guide to sucrose’. (Eds NL Pennington, CW Baker) pp. 198–211. (Van Nostrand Reinhold: New York)
Mayer VE, Frederickson ME, McKey D, Blatrix R (2014) Current issues in the evolutionary ecology of ant–plant symbioses. New Phytologist 202, 749–764.
| Current issues in the evolutionary ecology of ant–plant symbioses.Crossref | GoogleScholarGoogle Scholar |
McCluney KE, Belnap J, Collins SL, González AL, Hagen EM, Nathaniel Holland J, Kotler BP, Maestre FT, Smith SD, Wolf BO (2012) Shifting species interactions in terrestrial dryland ecosystems under altered water availability and climate change. Biological Reviews of the Cambridge Philosophical Society 87, 563–582.
| Shifting species interactions in terrestrial dryland ecosystems under altered water availability and climate change.Crossref | GoogleScholarGoogle Scholar |
Minitab Inc. (2015) Minitab statistical software 17. Available at www.minitab.com [Verified 15 September 2016]
Ness JH (2003) Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia 134, 210–218.
| Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards.Crossref | GoogleScholarGoogle Scholar |
Nicolson SW, Nepi M, Pacini E (2007) ‘Nectaries and nectar.’ (Springer: Dordrecht, The Netherlands)
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences of the United States of America 107, 19368–19373.
| CO2 enhancement of forest productivity constrained by limited nitrogen availability.Crossref | GoogleScholarGoogle Scholar |
O’Dowd DJ (1979) Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale. Oecologia 43, 233–248.
| Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale.Crossref | GoogleScholarGoogle Scholar |
O’Dowd DJ (1980) Pearl bodies of a neotropical tree, Ochroma pyramidale: ecological implications. American Journal of Botany 67, 543–549.
| Pearl bodies of a neotropical tree, Ochroma pyramidale: ecological implications.Crossref | GoogleScholarGoogle Scholar |
Osborne J, Awmack C, Clark S, Williams I, Mills V (1997) Nectar and flower production in Vicia faba L (field bean) at ambient and elevated carbon dioxide. Apidologie 28, 43–55.
| Nectar and flower production in Vicia faba L (field bean) at ambient and elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Pacini E, Nepi M, Vesprini JL (2003) Nectar biodiversity: a short review. Plant Systematics and Evolution 238, 7–21.
| Nectar biodiversity: a short review.Crossref | GoogleScholarGoogle Scholar |
Rafferty NE, CaraDonna PJ, Bronstein JL (2015) Phenological shifts and the fate of mutualisms. Oikos 124, 14–21.
| Phenological shifts and the fate of mutualisms.Crossref | GoogleScholarGoogle Scholar |
Rathcke B (1992) Effects of elevated CO2 on flowering phenology and nectar production of morning glory (Ipomoea purpurea). In ‘Proceedings of the 77th ESA meeting’. (Ecological Society of America: Columbus, OH, USA)
Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytologist 194, 321–336.
| A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables.Crossref | GoogleScholarGoogle Scholar |
Root T, Hughes L (2006) Changes in phenology and ecological interactions. In ‘Climate change and biodiversity’. (Eds TE Lovejoy, L Hannah) pp. 61–69. (Yale University Press: New Havenm, CT, USA)
Rudgers JA, Gardener MC (2004) Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85, 1495–1502.
| Extrafloral nectar as a resource mediating multispecies interactions.Crossref | GoogleScholarGoogle Scholar |
Rusterholz HP, Erhardt A (1998) Effects of elevated CO2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands. Oecologia 113, 341–349.
| Effects of elevated CO2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands.Crossref | GoogleScholarGoogle Scholar |
Rutter MT, Rausher MD (2004) Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait. Evolution 58, 2657–2668.
| Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait.Crossref | GoogleScholarGoogle Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar |
Smith NG, Dukes JS (2013) Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2. Global Change Biology 19, 45–63.
| Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2.Crossref | GoogleScholarGoogle Scholar |
Stamp N (2003) Out of the quagmire of plant defense hypotheses. The Quarterly Review of Biology 78, 23–55.
| Out of the quagmire of plant defense hypotheses.Crossref | GoogleScholarGoogle Scholar |
Weber MG, Keeler KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Annals of Botany 111, 1251–1261.
| The phylogenetic distribution of extrafloral nectaries in plants.Crossref | GoogleScholarGoogle Scholar |
Wilder SM, Eubanks MD (2010) Extrafloral nectar content alters foraging preferences of a predatory ant. Biology Letters 6, 177–179.
| Extrafloral nectar content alters foraging preferences of a predatory ant.Crossref | GoogleScholarGoogle Scholar |
Yamawo A, Tagawa J, Suzuki N (2014) Two Mallotus species of different life histories adopt different defense strategies in relation to leaf age. Plant Species Biology 29, 152–158.
| Two Mallotus species of different life histories adopt different defense strategies in relation to leaf age.Crossref | GoogleScholarGoogle Scholar |
Zavala JA, Gog L, Giacometti R (2017) Anthropogenic increase in carbon dioxide modifies plant-insect interactions. Annals of Applied Biology 170, 68–77.
| Anthropogenic increase in carbon dioxide modifies plant-insect interactions.Crossref | GoogleScholarGoogle Scholar |