Plasticity in within-plant distribution patterns allows aphids to optimize their fitness under contrasting interactions with protective ants and predatory ladybugs

doi:10.1016/j.jia.2025.06.009

Journal of Integrative Agriculture

2026, Vol. 25

Issue (5): 2003-2013 DOI: 10.1016/j.jia.2025.06.009

Plant Protection

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Plasticity in within-plant distribution patterns allows aphids to optimize their fitness under contrasting interactions with protective ants and predatory ladybugs

Tian Xu^1,^2,³^*, Yao Chen¹^*, Meng Xu³, Xinyi Li¹, Ted C. J. Turlings^4,^5,⁶^#, Li Chen^1,³^#

¹College of Life Sciences/Hebei Basic Science Center for Biotic Interaction, Hebei University, Baoding 071002, China

²Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China

³State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

⁴State Key Laboratory of Crop Stress Adaptation and Improvement/State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, School of Life Sciences, Henan University, Kaifeng 475006, China

⁵Laboratory of Fundamental and Applied Research in Chemical Ecology (FARCE), University of Neuchâtel, Neuenburg 2000, Switzerland

⁶Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA

Highlights

● Phenotypic plasticity is the ability of organisms to adapt to environmental changes. Many aphids have evolved facultative mutualistic relationships with ants, but the colonies must often cope without ants.

● Attendance by red imported fire ants, Solenopsis invicta, increased the proportions of cotton aphids (Aphis gossypii) distributed on the nutritive parts of cotton seedlings (stem, petioles, and sprouts (SPS)). However, in the absence of tending ants, the aphids on SPS suffered higher predation risk than on leaves. But the aphids can rapidly shift to leaves to reduce the proportions on SPS when the predatory ladybug or its signals were present.

● Aphid distribution patterns have adaptive plasticity which allows aphid colonies to optimize their fitness by responding to the presence of mutualistic ants or predatory threats with flexibility.

Abstract
References

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摘要

表型可塑性是生物的一种重要适应策略，有助于生物对环境变化作出响应。许多蚜虫进化出了与蚂蚁的共生关系，蚜虫提供蜜露以换取蚂蚁的保护。蚜-蚁共生关系通常是兼性的，因此蚜虫常需要在没有蚂蚁保护的情况下生存。本研究表明，红火蚁（Solenopsis invicta）的共生改变了棉蚜（Aphis gossypii）在棉苗上的空间分布。与无蚂蚁共生的棉蚜种群相比，共生种群在叶片上的数量更少，但在茎、叶柄和新芽（SPS）上的数量更多。茎和新芽中的氮含量高于叶片，可能是导致共生种群数量增长更快的原因。相反，当暴露于七星瓢虫（Coccinella septempunctata）的信号下，蚜虫种群数量显著变小，在叶片上分布的比例更高，在SPS上分布的比例显著低于未暴露于瓢虫信号的蚜虫种群。进一步研究发现，分布在棉苗茎上的蚜虫被瓢虫捕食的风险显著高于分布在叶片上的蚜虫。当七星瓢虫存在时，蚜虫会迅速从茎转移到叶片，说明其能够对捕食者的出现迅速做出反应。本研究结果表明，棉蚜在寄主上的分布模式具有可塑性，有助于其灵活应对共生蚂蚁或捕食性天敌的存在，从而优化自身的适合度。

Abstract

Phenotypic plasticity is a crucial adaptive strategy that allows organisms to respond to environmental changes. Many aphids have evolved mutualistic relationships with ants, whereby aphids provide honeydew in exchange for protection from natural enemies. Such ant–aphid mutualisms are often facultative and aphid colonies must often cope without ants. We show here that attendance by red imported fire ants, Solenopsis invicta, alters the within-plant distribution of cotton aphids (Aphis gossypii), resulting in fewer aphids on leaves and more on the stem, petioles, and sprouts (SPS) of cotton seedlings compared to colonies without ant attendance. The nitrogen contents in stems and sprouts were higher than in leaves, which may be a reason for the significantly higher population growth in ant-tended colonies. In contrast, exposure to the signals of a predatory ladybug, Coccinella septempunctata, resulted in a remarkably smaller aphid colony size, with lower proportions of aphids distributed on SPS, but a higher proportion on the leaves, compared to those in the predator-free colonies. In addition, ladybug predation risk is considerably higher on SPS than on leaves, and aphids showed rapid positional shifts from stems to leaves upon direct exposure to a ladybug, highlighting their ability to respond swiftly to predator presence. Our findings reveal that adaptive plasticity in aphid distribution patterns enables aphid colonies to optimize their fitness by responding to the presence of mutualistic ants or predatory threats with flexibility.

Keywords: ant–aphid mutualism natural enemy phenotypic plasticity within-plant distribution

Received: 18 February 2025 Accepted: 06 May 2025 Online: 03 June 2025

Fund:

This research was supported by the National Key R&D Program of China (2021YFD1000500), the Natural Science Foundation of Hebei Province, China (C2023201075), and the National Natural Science Foundation of China (32070488).

About author: Tian Xu, E-mail: xutian@njfu.edu.cn; Yao Chen, E-mail: 1050662425@qq.com; #Correspondence Li Chen, E-mail: chenli1@hbu.edu.cn; Ted C. J. Turlings, E-mail: ted.turlings@unine.ch * These authors contributed equally to this study.

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Tian Xu, Yao Chen, Meng Xu, Xinyi Li, Ted C. J. Turlings, Li Chen. 2026. Plasticity in within-plant distribution patterns allows aphids to optimize their fitness under contrasting interactions with protective ants and predatory ladybugs. Journal of Integrative Agriculture, 25(5): 2003-2013.

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