Aphids; Climate change; Honeydew; Mutualism; Sugars; Biochemistry; Ecology, Evolution, Behavior and Systematics; General Medicine
Abstract :
[en] Honeydew is the keystone of many interactions between aphids and their predators, parasitoids, and mutualistic partners. Despite the crucial importance of honeydew in aphid-ant mutualism, very few studies have investigated the potential impacts of climate change on its production and composition. Here, we quantified changes in sugar compounds and the amount of honeydew droplets released by Aphis fabae reared on Vicia faba plants under elevated temperature and/or CO2 conditions. Following the combined elevation of these two abiotic factors, we found a significant increase in the fructose content of A. fabae honeydew, accompanied by nonsignificant trends of increase in total honeydew production and melezitose content. The environmental conditions tested in this study did not significantly impact the other honeydew sugar contents. The observed changes may be related to changes in phloem composition under elevated CO2 conditions as well as to increases in aphid metabolism and sap ingestion under elevated temperatures. Although limited, such changes in aphid honeydew may concurrently reinforce ant attendance and mutualism under elevated temperature and CO2 conditions. Finally, we discuss the enhancing and counteracting effects of climate change on other biological agents (gut microorganisms, predators, and parasitoids) that interact with aphids in a complex multitrophic system.
Disciplines :
Entomology & pest control
Author, co-author :
Blanchard, S; Unit of Social Ecology, C.P. 231, Université Libre de Bruxelles, Avenue F.D. Roosevelt, 50, 1050, Bruxelles, Belgique ; Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, TERRA, Université de Liège, Avenue de la Faculté d'Agronomie 2B, 5030, Gembloux, Belgique
Verheggen, François ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Van De Vreken, Isabelle ; Université de Liège - ULiège > Département GxABT > Smart Technologies for Food and Biobased Products (SMARTECH)
Richel, Aurore ; Université de Liège - ULiège > TERRA Research Centre > Smart Technologies for Food and Biobased Products (SMARTECH)
Detrain, C ; Unit of Social Ecology, C.P. 231, Université Libre de Bruxelles, Avenue F.D. Roosevelt, 50, 1050, Bruxelles, Belgique. claire.detrain@ulb.be
Language :
English
Title :
Combined Elevation of Temperature and CO2 Impacts the Production and Sugar Composition of Aphid Honeydew.
Publication date :
29 September 2022
Journal title :
Journal of Chemical Ecology
ISSN :
0098-0331
eISSN :
1573-1561
Publisher :
Springer Science and Business Media LLC, United States
Abisgold JD, Simpson SJ, Douglas AE (1994) Nutrient regulation in the pea aphid Acyrthosiphon pisum – application of a novel geometric framework to sugar and amino-acid consumption. Physiol Entomol 19:95–102. 10.1111/j.1365-3032.1994.tb01081.x DOI: 10.1111/j.1365-3032.1994.tb01081.x
Ashford DA, Smith WA, Douglas AE (2000) Living on a high sugar diet: the fate of sucrose ingested by a phloem-feeding insect, the pea aphid Acyrthosiphon pisum J Insect Physiol 46(3):335–341. 10.1016/S0022-1910(99)00186-9 DOI: 10.1016/S0022-1910(99)00186-9
Auclair JL (1958) Honeydew excretion in the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera: Aphididae). J Insect Physiol 2(4):330–337. https://doi.org/10.1016/0022-1910(58)90018-0
Bacon JSD, Dickinson B (1957) The origin of melezitose: a biochemical relationship between the lime tree (Tilia spp.) and an aphis (Eucallipterus tiliae L.). Biochem J 66(2):289–299. 10.1042/bj0660289 DOI: 10.1042/bj0660289
Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge
Bishop KA, Lemonnier P, Quebedeaux JC, Montes CM, Leakey AD, Ainsworth EA (2018) Similar photosynthetic response to elevated carbon dioxide concentration in species with different phloem loading strategies. Photosynth Res 137(3):453–464. 10.1007/s11120-018-0524-x DOI: 10.1007/s11120-018-0524-x
Blanchard S, Lognay G, Verheggen F, Detrain C (2019) Today and tomorrow: Impact of climate change on aphid biology and potential consequences on their mutualism with ants. Physiol Entomol 44(2):77–86. 10.1111/phen.12275 DOI: 10.1111/phen.12275
Blüthgen N, Fiedler K (2004) Competition for composition. Lessons from nectar-feeding ant communities. Ecology 85:1479–1485. 10.1890/03-0430 DOI: 10.1890/03-0430
Boevé JL, Wäckers FL (2003) Gustatory perception and metabolic utilization of sugars by Myrmica rubra ant workers. Oecologia 136:508–514. 10.1007/s00442-003-1249-9 DOI: 10.1007/s00442-003-1249-9
Boullis A, Blanchard S, Francis F, Verheggen F (2018) Elevated CO2 concentrations impact the semiochemistry of aphid honeydew without having a cascade effect on an aphid predator. Insects 9(2):47. 10.3390/insects9020047 DOI: 10.3390/insects9020047
Breed MD, Fewel JH, Moore AJ, William KR (1987) Graded recruitment in a ponerine ant. Behav Ecol Sociobiol 20:407–411. 10.1007/BF00302983 DOI: 10.1007/BF00302983
Breed MD, Bowden RM, Garry MF, Weicker AL (1996) Giving-up time variation in response to differences in nectar volume and concentration in the giant tropical ant Paraponera clavata (Hymenoptera: Formicidae). J Insect Behav 9:659–672. 10.1007/BF02213547 DOI: 10.1007/BF02213547
Buckley R (1987) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Evol Syst 18:111–135 DOI: 10.1146/annurev.es.18.110187.000551
Detrain C, Deneubourg JL, Pasteels JM (1999) Decision-making in foraging by social insects. Information Processing in Social Insects. Birkhaüser Verlag, Basel, pp 331–354 DOI: 10.1007/978-3-0348-8739-7_18
Detrain C, Verheggen FJ, Diez L, Wathelet B, Haubruge E (2010) Aphid–ant mutualism: how honeydew sugars influence the behaviour of ant scouts. Physiol Entomol 35(2):168–174. 10.1111/j.1365-3032.2010.00730.x DOI: 10.1111/j.1365-3032.2010.00730.x
Detrain C, Prieur J (2014) Sensitivity and feeding efficiency of the black garden ant Lasius niger to sugar resources. J Insect Physiol 64:74–80. 10.1016/j.jinsphys.2014.03.010 DOI: 10.1016/j.jinsphys.2014.03.010
Docherty M, Wade F, Hurst D, Whittaker J, Lea P (1997) Responses of tree sap-feeding herbivores to elevated CO2. Glob Change Biol 3(1):51–59. 10.1046/j.1365-2486.1997.00096.x DOI: 10.1046/j.1365-2486.1997.00096.x
Dussutour A, Simpson SJ (2008) Carbohydrate regulation in relation to colony growth in ants. J Exp Biol 211:2224–2232. 10.1242/jeb.017509 DOI: 10.1242/jeb.017509
El-Ziady S, Kennedy JS (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli. Proc R Soc B 31:61–65
Engel V, Fischer MK, Wäckers FL, Völkl W (2001) Interactions between extrafloral nectaries, aphids and ants: are there competition effects between plant and homopteran sugar sources? Oecologia 129:577–584. 10.1007/s004420100765 DOI: 10.1007/s004420100765
Fischer M, Shingleton A (2001) Host plant and ants influence the honeydew sugar composition of aphids. Funct Ecol 15:544–550. 10.1046/j.0269-8463.2001.00550.x DOI: 10.1046/j.0269-8463.2001.00550.x
Fischer MK, Völkl W, Schopf R, Hoffmann KH (2002) Age-specific patterns in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant‐attendance. J Insect Physiol 48:319–326. 10.1016/S0022-1910(01)00179-2 DOI: 10.1016/S0022-1910(01)00179-2
Fischer MK, Völkl W, Hoffmann KH (2005) Honeydew production and honeydew sugar composition of polyphagous black bean aphid, Aphis fabae (Hemiptera: Aphididae) on various host plants and implications for ant-attendance. Eur J Entomol 102(2):155–160 DOI: 10.14411/eje.2005.025
Fischer CY, Lognay GC, Detrain C, Heil M, Grigorescu A, Sabri A et al (2015) Bacteria may enhance species association in an ant–aphid mutualistic relationship. Chemoecology 25(5):223–232. 10.1007/s00049-015-0188-3 DOI: 10.1007/s00049-015-0188-3
Fu X, Ye L, Kang L, Ge F (2010) Elevated CO2 shifts the focus of tobacco plant defenses from cucumber mosaic virus to the green peach aphid. Plant Cell Environ 33(12):2056–2064. 10.1111/j.1365-3040.2010.02205.x DOI: 10.1111/j.1365-3040.2010.02205.x
Hendrix DL, Wei YA, Leggett JE (1992) Homopteran honeydew sugar composition is determined by both the insect and plant species. Comp Biochem Physiol B Biochem Mol Biol 101:23–27. 10.1016/0305-0491(92)90153-I DOI: 10.1016/0305-0491(92)90153-I
Hewer A, Will T, van Bel AJ (2010) Plant cues for aphid navigation in vascular tissues. J Exp Biol 213(23):4030–4042. 10.1242/jeb.046326 DOI: 10.1242/jeb.046326
Hodge S, Ward JL, Beale MH et al (2013) Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237:1057–1064. 10.1007/s00425-012-1826-4 DOI: 10.1007/s00425-012-1826-4
Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge DOI: 10.1007/978-3-662-10306-7
IPCC (2019) Summary for policymakers. In: Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems [P.R. Shukla, J. Skea, E. Calvo Buendia, V. Masson-Delmotte, H.- O. Pörtner, D. C. Roberts, P. Zhai, R. Slade, S. Connors, R. van Diemen, M. Ferrat, E. Haughey, S. Luz, S. Neogi, M. Pathak, J. Petzold, J. Portugal Pereira, P. Vyas, E. Huntley, K. Kissick, M. Belkacemi, J. Malley, (eds.)]
Kiss A (1981) Melezitose, aphids and ants. Oikos 37:382 DOI: 10.2307/3544132
Kremer JM, Nooten SS, Cook JM, Ryalls JM, Barton CV, Johnson SN (2018) Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids. J Anim Ecol 87(5):1475–1483. 10.1111/1365-2656.12842 DOI: 10.1111/1365-2656.12842
Krumbein A, Kläring HP, Schonhof I, Schreiner M (2010) Atmospheric carbon dioxide changes photochemical activity, soluble sugars and volatile levels in broccoli (Brassica oleracea var. italica). J Agric Food Chem 58(6):3747–3752. 10.1021/jf903280w DOI: 10.1021/jf903280w
Leroy PD, Wathelet B, Sabri A, Francis F, Verheggen FJ, Capella Q et al (2011) Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition? Arthropod Plant Interact 5(3):193–199. 10.1007/s11829-011-9128-5 DOI: 10.1007/s11829-011-9128-5
Mailleux AC, Deneubourg JL, Detrain C (2000) How do ants assess food volume? Anim Behav 59:1061–1069. 10.1006/anbe.2000.1396 DOI: 10.1006/anbe.2000.1396
Mailleux AC, Deneubourg JL, Detrain C (2003) Regulation of ants’ foraging to resource productivity. Proc. R Soc B 270:1609–1616. 10.1098/rspb.2003.2398
Mooney E, Davidson B, Den Uyl J, Mullins M, Medina E, Nguyen P, Owens J (2019) Elevated temperatures alter an ant-aphid mutualism. Entomol Exp et Appl 167(10):891–905. 10.1111/eea.12839 DOI: 10.1111/eea.12839
Moreno-Delafuente A, Morales I, Garzo E, Fereres A, Viñuela E, Medina P (2021) Changes in melon plant phytochemistry impair Aphis gossypii growth and weight under elevated CO2. Sci Rep 11(1):1–12 DOI: 10.1038/s41598-021-81167-x
Newman JA, Gibson DJ, Parsons AJ, Thornley JHM (2003) How predictable are aphid population responses to elevated CO2 J Anim Ecol 72:556–566. 10.1046/j.1365-2656.2003.00725.x DOI: 10.1046/j.1365-2656.2003.00725.x
Oehme V, Högy P, Zebitz CP, Fangmeier A (2013) Effects of elevated atmospheric CO2 concentrations on phloem sap composition of spring crops and aphid performance. J Plant Interact 8(1):74–84 DOI: 10.1080/17429145.2012.736200
Petry WK, Perry KI, Mooney KA (2012) Influence of macronutrient imbalance on native ant foraging and interspecific interactions in the field. Ecol Entomol 37(3):175–183. 10.1111/j.1365-2311.2012.01349.x DOI: 10.1111/j.1365-2311.2012.01349.x
Pritchard J, Griffiths B, Hunt EJ (2007) Can the plant-mediated impacts on aphids of elevated CO2 and drought be predicted? Glob. Change Biol 13:1616–1629. 10.1111/j.1365-2486.2007.01401.x DOI: 10.1111/j.1365-2486.2007.01401.x
Pringle EG, Novo A, Ableson I, Barbehenn RV, Vannette RL (2014) Plant-derived differences in the composition of aphid honeydew and their effects on colonies of aphid‐tending ants. Ecol Evol 4(21):4065–4079. 10.1002/ece3.1277 DOI: 10.1002/ece3.1277
Renoz F, Pons I, Hance T (2019) Evolutionary responses of mutualistic insect–bacterial symbioses in a world of fluctuating temperatures. Curr Opin Insect Sci 35:20–26. 10.1016/j.cois.2019.06.006 DOI: 10.1016/j.cois.2019.06.006
Ryan GD, Sylvester EV, Shelp BJ, Newman JA (2015) Towards an understanding of how phloem amino acid composition shapes elevated CO2-induced changes in aphid population dynamics. Ecol Entomol 40(3):247–257. 10.1111/een.12181 DOI: 10.1111/een.12181
Stadler B, Dixon AFG (2005) Ecology and evolution of aphid–ant interactions, Annu. Rev Ecol Evol Syst 36:345–372. 10.1146/annurev.ecolsys.36.091704.175531 DOI: 10.1146/annurev.ecolsys.36.091704.175531
Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob Change Biol 13:1823–2842. 10.1111/j.1365-2486.2007.01392.x DOI: 10.1111/j.1365-2486.2007.01392.x
Sudderth EA, Stinson KA, Bazzaz FA (2005) Host-specific aphid population responses to elevated CO2 and increased N availability. Glob Change Biol 11:1997–2008. 10.1111/j.1365-2486.2005.01006.x DOI: 10.1111/j.1365-2486.2005.01006.x
Sun YC, Jing BB, Ge F (2009) Response of amino-acid changes in Aphis gossypii (Glover) to elevated CO2 levels. J Appl Entomol 133(3):189–197. 10.1111/j.1439-0418.2008.01341.x DOI: 10.1111/j.1439-0418.2008.01341.x
Sun Y, Ge F (2011) How do aphids respond to elevated CO2? J. Asia-Pac Entomol 14:217–220. 10.1016/j.aspen.2010.08.001 DOI: 10.1016/j.aspen.2010.08.001
Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57(4):739–745. 10.1093/jxb/erj088 DOI: 10.1093/jxb/erj088
Vantaux A, Van den Ende W, Billen J, Wenseleers T (2011) Large interclone differences in melezitose secretion in the facultatively ant-tended black bean aphid Aphis fabae J Insect Physiol 57(12):1614–1621. 10.1016/j.jinsphys.2011.08.014 DOI: 10.1016/j.jinsphys.2011.08.014
Vassiliadis S, Plummer KM, Powell KS, Trębicki P, Luck JE, Rochfort SJ (2016) The effect of elevated CO2 and virus infection on the primary metabolism of wheat. Funct Plant Bio 43(9):892–902. 10.1071/FP15242 DOI: 10.1071/FP15242
Völkl W, Woodring J, Fischer M, Lorenz MW, Hoffmann KH (1999) Ant–aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 118:483–491. 10.1007/s004420050751 DOI: 10.1007/s004420050751
Wäckers FL (2000) Do oligosaccharides reduce the suitability of honeydew for predators and parasitoids? A further facet to the function of insect-synthesized honeydew sugars. Oikos 90:197–202 DOI: 10.1034/j.1600-0706.2000.900124.x
Wäckers FL (2001) A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoids Cotesia glomerata J Insect Physiol 47:1077–1084. 10.1016/S0022-1910(01)00088-9 DOI: 10.1016/S0022-1910(01)00088-9
Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344 DOI: 10.1146/annurev.en.08.010163.001515
Woodring J, Wiedemann R, Fischer MK et al (2004) Honeydew amino-acids in relation to sugars and their role in the establishment of ant attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiol Entomol 29:311–319. 10.1111/j.0307-6962.2004.00386.x DOI: 10.1111/j.0307-6962.2004.00386.x
Yao I, Shibao H, Akimoto SI (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola Oikos 89:3–10. 10.1034/j.1600-0706.2000.890101.x DOI: 10.1034/j.1600-0706.2000.890101.x
Yao I, Akimoto SI (2001) Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola Oecologia 128(1):36–43. 10.1007/s004420100633 DOI: 10.1007/s004420100633
