Different species interact with each other in complex and diverse ways. Why and how do we study these interspecies interactions? How do we introduce students to these interactions through real-world observations of plants, aphids, and ants from their own backyards?

Children begin observing and wondering about interspecies interactions in and around their home and school long before their science textbook introduces them to related concepts. Giving students the opportunity to study some of these interactions may help teachers connect abstract concepts in the textbook to real-world observations from their backyard. For example, have you come across a plant in your garden, school compound, or fields that seems to be covered with tiny creatures? Does it look like these parts of the plant are bustling with ants? If your answer to both these questions is ​‘yes’, then you may be at the right place to witness a fascinating three-way interaction between ants, aphids, and plants (see Box 1).

The plant – aphid interaction

As you may have guessed, the tiny white, yellow, green, or black creatures are insects called aphids (see Fig. 1).

Like mealybugs, whiteflies, and plant hoppers, aphids have needle-like mouth parts (called stylets) that they inject into the tender parts of the plant to feed upon the phloem sap that the plant makes for its own nourishment (see Box 2).¹ The loss of nutrition caused by these phytophagous (phyto= plants, phagy = to eat) or sap-sucking insects, affects the health of the plant, and causes wilting and yellowing of its parts. It may also affect the reproductive fitness of the plant, reducing its fruit and seed set. 

Aphids may also act as vectors of deadly plant viruses such as cucumber mosaic virus and potato virus. These viruses can enter their host plant through the saliva of a feeding aphid. Weakened by the aphid infestation, the plant becomes more susceptible to these and other diseases. Since the aphid benefits at the expense of the plant, the plant – aphid interaction offers a real-world example of an antagonistic (parasitic) interaction.

The aphid – ant interaction

While the aphids feed on phloem sap, they excrete droplets of a sticky, sugary, nutrient-rich liquid, called honeydew, from their rectum. This attracts certain species of ants to the host plant. How? Studies show that these ants ​‘smell’ the presence of certain volatile organic compounds (VOCs) in the honeydew through sensory organs called olfactory lobes that act like our nose (see Box 2).

These VOCs are produced by the action of specific bacteria that reside in the inner gut wall of the aphids.² The ants feed on the honeydew, and herd and tend to the aphids (see Fig. 2). Some ant species also deter the natural enemies of aphids (see Box 2).^3,5

These could include the larval and adult stages of insects such as ladybird beetles, hoverflies, and parasitic wasps that either feed on the aphid or lay eggs within its body (see Fig. 3). Since both partners benefit from this association, the aphid – ant interaction offers a real- world example of mutualism.^{3, 4, 5} This type of mutualism is referred to as ​‘food for protection’ mutualism.⁵

However, like many other interspecies interactions, the ant-aphid association is more complex and dynamic than it may seem. Most ants are opportunistic foragers — eating almost anything they can find to fulfill the needs of their colony. This may lead one to wonder if ants also prey on aphids? 

They do, when their protein requirement exceeds their carbohydrate requirement (which can be met by honeydew). Under such circumstances, the aphid – ant interaction changes from being mutualistic to becoming antagonistic. However, studies also suggest that ants prefer to prey upon aphid species that are non-myrmecophilous rather than those that are myrmecophilous (see Box 3).⁶

This raises the question — how do ants distinguish between the two kinds of aphids? Studies suggest that the body odour of every aphid has species-specific chemical signatures known as cuticular hydrocarbons (CHCs). Depending on the nature of these CHCs, the relationship between an aphid species and its tending ant species may be obligatory (both species depend entirely on, and cannot survive without services from each other) or facultative (the ant species is partly dependent on the aphid species). CHCs also help a partner ant species to differentiate between myrmecophilous and non- myrmecophilous aphids.⁷

The plant – ant interaction

Recent studies on interactions between plants, ants, and aphids have shown that some species of ants protect the host plant against other non-sap-sucking insect herbivores such as caterpillars and beetles.⁸

Other studies show that accumulation of honeydew can attract fungal infection. By cleaning plant parts of honeydew, ants protect the host plant against these infections.^{9, 10} This suggests that despite the harm caused by aphids to the host plant, the presence of protective ants might save the plant from further damage.

Parting thoughts

Detailed studies on interspecies interactions like the plant – aphid – ant interaction have helped reveal the dynamics and complexity of such interactions in general, as well as their role in maintaining ecological balance. 

For example, several studies show that when ants are blocked from access to aphids (using a sticky insect barrier, like Tanglefoot), aphid colony size reduces. This also causes an increase in abundance of the natural enemies of aphids and herbivory on host plants, which reduces both aphid and host plant fitness. The excluded myrmecophilous ants tend to show a preference for insect prey, suggesting a shift from carbohydrate-seeking to protein-seeking foraging behaviour.

Introducing students to some of the most interesting insights that ecologists have learnt about plant – aphid – ant interactions through scientific investigation can spark their interest and curiosity in related life science topics from their curriculum. It can also strengthen and expand their understanding of the nature and process of scientific inquiry.

Here’s a checklist for observation of plant-aphid-ant interactions:

Key takeaways

• Real-world observations of plant – aphid – ant interactions in their immediate surroundings can be used to introduce students to textbook concepts around interspecies interactions and their role in maintaining ecological balance.

• The plant – aphid relationship offers a relatable example of an antagonistic interaction, while the aphid – ant relationship offers a fascinating example of a mutually beneficial interaction.

• Since the aphid – ant interaction remains mutualistic only as long as the benefit that the ant gains from it is high, the context-dependent nature of this interaction can be used to illustrate the complex and dynamic nature of interspecies interactions.

• Sharing details of the kind of experiments used to understand these interactions can help expand student understanding of the nature and process of scientific inquiry.

Acknowledgements: The authors are grateful to the Department of Biotechnology (DBT), India for funding (Project No. DBT-NER/Agri/24/2013 dated 30/03/2015). We are indebted to our collaborators — the National Centre for Biological Science (NCBS), Indian Institute of Science (IISc.) and University of Agricultural Science (UAS), Bangalore for organizing workshops and training programs for students. Our sincere thanks go to Dr. Shannon B. Olsson, Dr. Joyshree Chanam, Dr. Lucy Nongbri, Dr. Dibyendu Adhikari, Dr. Raghuvar Tiwary, Satyajeet Gupta, and Anita Gupta for their valuable suggestions during the preparation of the manuscript. We are thankful to Prof. Uma Ramakrishnan, Dr. Dhruba Sharma, and Dr. Arkamitra Vishnu for coordinating and providing assistance whenever required. The authors would like to extend their sincere thanks to the Head, Department of Botany, North-Eastern Hill University, Shillong, and Director, National Botanical Research Institute, Lucknow for providing necessary facilities.

Note

Source of the image used at the beginning of the article: https://​com​mons​.wiki​me​dia​.org/​w​i​k​i​/​F​i​l​e​:​A​n​t​_​g​u​a​r​d​s​_​i​t​s​_​A​p​h​i​d​s​.​j​p​g​#​/​m​e​d​i​a​/​F​i​l​e​:​A​n​t​_​g​u​a​r​d​s​_​i​t​s​_​A​p​h​i​d​s.jpg
Credits: viamoi, Wikimedia Commons. License: CC-BY.

References

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2. Fischer CY, Lognay GC, Detrain C, Heil M, Grigorescu A, Sabri A, et al. Bacteria may enhance species association in an ant – aphid mutualistic relationship. Chemoecology. 2015; 25(5): 223 – 32.
3. Powell BE, Silverman J. Impact of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae) on three natural enemies of Aphis gossypii (Hemiptera: Aphididae). Biol. Control. 2010; 54(3): 285 – 91. http://​dx​.doi​.org/​1​0​.​1​0​1​6​/​j​.​b​i​o​c​o​n​t​r​o​l​.​2​0​1​0​.​0​5.013
4. Del-claro K, Oliveira PS. Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia. 2000; 124: 156 – 65.
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7. Lang, C., and Menzel, F. Lasius niger ants discriminate aphids based on their cuticular hydrocarbons. Animal Behavior 2011; 82: 1245 – 1254.
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About the Authors

Rudra Prasad Banerjee is a doctoral student at CSIR-National Botanical Research Institute (CSIR-NBRI), Lucknow where he studies spatio-temporal variations in the tri-trophic interaction between plants, aphids, and ants. He can be contacted at rudrabanerjee1042@​gmail.​com

Renee M Borges is Professor at the Centre for Ecological Sciences at Indian Institute of Science (IISc), Bangalore. Her research team is interested in understanding the coevolutionary dynamics between plants, insects, other invertebrates, and microbes. She can be reached at renee@​iisc.​ac.​in.

Saroj Kanta Barik is Director of CSIR-National Botanical Research Institute (CSIR-NBRI), Lucknow. His research interests include ecology and environment, conservation biology, and chemical ecology. He can be reached at sarojkbarik@​gmail.​com.

Prem Prakash Singh is pursuing his doctoral degree at Department of Botany, North-Eastern Hill University, Shillong. His research is related to the impact of climate change on plant diversity and conservation of threatened plants. He can be contacted at prem12flyhigh@​gmail.​com.

Madhoolika Agrawal is Professor in the Department of Botany at Banaras Hindu University (BHU), Varanasi. She studies the physiological adaptations of important agronomic plants in the context of global warming and climate change. She can be reached at: madhoo.​agrawal@​gmail.​com.

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