Abstract
Herbivore injury has a direct effect on the growth and performance of host plants through photosynthetic suppression. However, changes in plant photosynthesis affected by ant tending of hemipteran sap feeders remain poorly understood. We investigated the effects of an invasive mealybug (Phenacoccus solenopsis) tended by native ants (Paratrechina longicornis) on the chlorophyll content and chlorophyll fluorescence characteristics of cotton (Gossypium hirsutum) leaves under greenhouse conditions. The results showed that the relative chlorophyll content of the infested cotton leaves significantly decreased after 10 days, and the chlorophyll contents were reduced by 26.4 and 34.9 % after 20 days in the without and with ant treatments compared to the control, respectively. In addition, the light utilization efficiency and maximum relative electron transport rate were reduced by 53.0 and 51.3 % compared to the control, respectively. However, no significant differences in these factors were found between the without and with ant treatments. The light saturation coefficient, describing the capacity of a sample to resist glare, exhibited no significant difference among treatments. The number of tending P. longicornis ants increased with P. solenopsis numbers, and the P. solenopsis numbers decreased after 20 days compared to the without ant treatment. We suggest that the tending ants may enhance the feeding ability of individual mealybugs in spite of the decreased number of mealybugs in this situation. Additionally, P. longicornis decrease the relative chlorophyll content of infested cotton leaves and may accelerate the damage caused by P. solenopsis to plants over time.
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References
Aldea M, Hamilton JG, Resti JP, Zangerl AR, Berenbaum MR, Frank TD, Delucia EH (2006) Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings. Oecologia 149:221–232
Bach CE (1991) Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87(2):233–239
Bounfour M, Tanigoshi LK, Chen C, Cameron SJ, Klauer S (2002) Chlorophyll content and chlorophyll fluorescence in red raspberry leaves infested with Tetranychus urticae and Eotetranychus carpini borealis (Acari: Tetranychidae). Environ Entomol 31:215–220
Burd JD, Elliott NC (1996) Changes in chlorophyll a fluorescence induction kinetics in cereals infested with Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 89:1332–1337
Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecol Entomol 32:583–596
Delaney KJ, Haile FJ, Peterson RKD, Higley LG (2008) Impairment of leaf photosynthesis after insect herbivory or mechanical injury on common milkweed, Asclepias syriaca. Ecol Entomol 37:1332–1343
Diaz R, Knutson A, Bernal JS (2004) Effect of the red imported fire ant on cotton aphid population density and predation of bollworm and beet armyworm eggs. J Econ Entomol 97:222–229
Eubanks MD (2001) Estimates of the direct and indirect effects of red imported fire ants on biological control. Biol Control 21(1):35–43
Fand BB, Suroshe SS (2015) The invasive mealybug Phenacoccus solenopsis Tinsley, a threat to tropical and subtropical agricultural and horticultural production systems: a review. Crop Prot 69:34–43
Feng DD, Michaud JP, Li P, Zhou ZS, Xu ZF (2015) The native ant, Tapinoma melanocephalum, improves the survival of an invasive mealybug, Phenacoccus solenopsis, by defending it from parasitoids. Sci Rep-UK 5:15691. doi:10.1038/srep15691
Gaigher R, Samways MJ, Henwood J, Jolliffe K (2011) Impact of a mutualism between an invasive ant and honeydew-producing insects on a functionally important tree on a tropical island. Biol Invasions 13:1717–1721
Harmon JP, Andow DA (2007) Behavioral mechanisms underlying ants’ density-dependent deterrence of aphid-eating predators. Oikos 116:1030–1036
Helms KR, Vinson SB (2003) Apparent facilitation of an invasive mealybug by an invasive ant. Insect Soc 50:403–404
Heng-Moss T, Macedo T, Franzen L, Baxendale F, Higley L, Sarath G (2006) Physiological responses of resistant and susceptible buffalograsses to Blissus Occiduus (Hemiptera: Blissidae) feeding. J Econ Entomol 99:222–228
Huang J, Zhang J, Wei HX, Li MJ (2012) Effects of a native ant, Pristomyrmex pungens Mayr (Hymenoptera: Formicidae) on the population dynamics and spatial distribution of invasive mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). Sociobiology 59(3):719–729
Huang J, Zhang PJ, Zhang J, Lu YB, Huang F, Li MJ (2013) Chlorophyll content and chlorophyll fluorescence in tomato leaves infested with an invasive mealybug, Phenacoccus solenopsis (Hemiptera: Pseudococcidae). Environ Entomol 42(5):973–979
Iatrou G, Cook CM, Stamou G, Lanaras T (1995) Chlorophyll fluorescence and leaf chlorophyll content of bean leaves injured by spider mites (Acari: Tetranychidae). Exp Appl Acarol 19:581–591
Kaplan I, Eubanks MD (2002) Disruption of cotton aphid (Homoptera: Aphididae)-natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ Entomol 31(6):1175–1183
Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 35:441–453
Lawlor DW (2009) Musings about the effects of environment on photosynthesis. Ann Bot 103:543–549
Macedo TB, Bastos CS, Higley LG, Ostile KR, Madhavan S (2003) Photosynthetic responses of soybean to soybean aphid (Homoptera: Aphididae) injury. J Econ Entomol 96(1):188–193
Meyer GA, Whitlow TH (1992) Effects of leaf and sap feeding insects on photosynthetic rates of goldenrod. Oecologia 92:480–489
Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663
Nowak RS, Caldwell MM (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61:311–318
Paris CI, Espadaler X (2009) Honeydew collection by the invasive garden ant Lasius neglectus versus the native ant L. grandis. Arthropod-Plant Interact 3:75–85
Paris CI, Llusia J, Peñuelas J (2010) Changes in monoterpene emission rates of Quercus ilex infested by aphids tended by native or invasive Lasius ant species. J Chem Ecol 36:689–698
Paris CI, Llusia J, Peñuelas J (2011) Indirect effects of tending ants on holm oak volatiles and acorn quality. Plant Signal Behav 6(4):547–550
Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701
Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237
Ralph PJ, Gademann R, Larkum AWD, Kuhl M (2002) Spatial heterogeneity in active fluorescence and PSII activity of coral tissues. Mar Biol 141:539–646
Rauch G, Simon JC, Chaubet B, Haack L, Flatt T, Weisser WW (2002) The influence of ant attendance on aphid behaviour investigated with the electrical penetration graph technique. Entomol Exp Applic 102:13–20
Retuerto R, Fernandez-Lema B, Rodriguez-Roiloa Obeso JR (2004) Increased photosynthetic performanc in holly trees infested by scale insects. Funct Ecol 18:664–669
Samsone I, Andersone U, Ievinsh G (2012) Variable effect of arthropod-induced galls on photochemistry of photosynthesis, oxidative enzyme activity and ethylene production in tree leaf tissues. Environ Exp Biol 10:15–26
Schroeder R, Forstreuter M, Hilker M (2005) A plant notices insect egg deposition and changes its rate of photosynthesis. Plant Physiol 138:470–477
Stadler B, Dixon AFG (2005) Ecology and evolution of aphid–ant interactions. Ann Rev Ecol Syst 36:345–372
Stanley MC, Nathan HW, Phillips LK, Knight SJ, Galbraith JA, Winks CJ, Ward DF (2013) Invasive interactions: can Argentine ants indirectly increase the reproductive output of a weed? Arthropod-Plant Interact 7:59–67
Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc Lond B Biol 274:151–164
Thomson VP, Cunningham SA, Ball MC, Nicotra AB (2003) Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia 134:167–175
Watanabe T, Kitagawa H (2001) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). J Econ Entomol 93(4):1192–1198
Way MJ (1963) Mutualism between ants and honeydew producing Homoptera. Ann Rev Entomol 8:307–344
Welter SC (1989) Arthropod impact on plant gas exchange. In: Bernays EA (ed) Insect–plant interactions. CRC Press, Boca Raton, pp 135–151
Whittaker J (1991) Effects of ants on temperate woodland trees. In: Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford University Press, Oxford, England, pp 67–79
Yao I, Akimoto S (2001) Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus querciola. Oecologia 128:36–43
Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, de Lucial EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091
Zhou AM, Liang GW, Lu YY, Zeng L, Xu YJ (2014) Interspecific competition between the red imported fire ant, Solenopsis invicta Buren and ghost ant, Tapinoma melanocephalum Fabricius for honeydew resources produced by an invasive mealybug, Phenacoccus solenopsis Tinsiley. Arthropod-Plant Interact 8:469–474
Acknowledgments
We gratefully acknowledge the assistance of Zheng Shi-Yu and Shan Dan (Animal and Plant Quarantine Department, Plant Protection Institute, Anhui Agricultural University) for helping with the measurements of chlorophyll fluorescence. This work was supported in part by the Zhejiang Provincial Natural Science Foundation of China (Grant Nos. LQ14C140004 and LQ16C140004) and the Youth Foundation of Zhejiang Academy of Agricultural Sciences (Grant No. 2015CX23).
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Handling Editor: Heikki Hokkanen.
Juan Zhang contributed equally with Jun Huang and is a co-first author of this paper.
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Huang, J., Zhang, J. Changes in the photosynthetic characteristics of cotton leaves infested by invasive mealybugs tended by native ant species. Arthropod-Plant Interactions 10, 161–169 (2016). https://doi.org/10.1007/s11829-016-9418-z
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DOI: https://doi.org/10.1007/s11829-016-9418-z