Mutualism: Ants and their Insect Partners

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If you are interested in the title for your course we can consider offering an examination copy. To register your interest please contact collegesales cambridge. A mutualism is an interaction between individuals of two different species of organism in which both benefit from the association. With a focus on mutualisms between ants and aphids, coccids, membracids and lycaenids, this volume provides a detailed account of the many different facets of mutualisms. Mutualistic interactions not only affect the two partners, but can also have consequences for higher levels of organization.

By linking theory to case studies, the authors present an integrated account of processes and patterns of mutualistic interactions at different levels of organisation, from individuals to communities to ecosystems. Interactions between ants and their insect partners and their outcomes are explained from a resource-based, cost-benefit perspective.

Covering a fascinating and growing subject in modern ecology, this book will be of interest to community and evolutionary ecologists and entomologists, at both research and graduate student level. Preface 1. The scope of the problem 2. Historical perspective 3. Theories on mutualism 4. Mutualisms between ants and their partners 5. A special case: aphids and ants 6. Multitropic level interactions 7. Prospects and conclusions References Index. Anthony F. This title is available for institutional purchase via Cambridge Core Cambridge Core offers access to academic eBooks from our world-renowned publishing programme.

Mutualism ants and their insect partners | Ecology and conservation | Cambridge University Press

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According to the authors, the amounts of alkaloids were not sufficient to cause deleterious effect to insect metabolism and growth and thus may have other functions than deterrence. The reciprocal exchange of benefits is the key feature of mutualistic interactions but benefits are often costly to provide, which then leads conflict among partners. These conflicts can be managed by a single controlling organism that may selectively reward cooperative partners and sanction to non-cooperative ones, control partner behaviour and eventually employ recognition mechanisms that discriminate between beneficial and potentially harmful or ineffective partners Douglas All these mechanisms have been proposed to explain how ant—plant partnership may be stable under the danger of cheaters Heil and McKey In this context, ant—plant interactions represent useful and promising study models for interdisciplinary investigations involving ethology, behavioural ecology, neurophysiology, plant biology and physiology, evolutionary biology.

In spite of their ecological dominance and superorganismic efficient organization, ants are vulnerable to manipulation by other organisms. For instance, nematode infections have been found to alter the anatomy and behaviour of the parasitized ants so that it resembles a ripe fruit to be dispersed by birds Hughes et al.

Another amazing example of a parasite-extended phenotype is that of the death grip in ants, observed when Ophiocordyceps fungi infected them to facilitate spore dispersal de Bekker et al. For example, raiders of slave-making ants have been found to use chemicals to cause panic inside attacked colonies, and queens discharge appeasement substances to lower the level of aggression in resident workers during host colony usurpation Mori et al.

Interaction between ants and plants bearing EF nectars may result in aggressive behaviour upon encounters with intruders. Indeed, most of the ant species common on EF nectaries are rather aggressive showing strong ownership behaviour and fierce attack responses against intruders Bentley More specifically, as reported by Koptur , ants' discovery of EFN resources induces the following behavioural repertoire: feeding, collecting, recruitment, territoriality and aggression.

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Aggressive behaviour is particularly evident in myrmecophyte—ant associations. For example in Tetraponera—Barteria association, ants are extremely aggressive and prone to respond to fine vibration perceived on the plant; this results in ants attacking insects and even large mammalian herbivores even elephants and antelopes approaching the plant, and in extreme cases ants can drop down the tree to attack and sting painfully the intruders.

Finally, aggressive ants can also emit a strong-smelling secretion that may serve as a warning signal to approaching animals Janzen ; Dejean et al. Ants are also very active against encroaching vegetation. This aggression against competing vegetation is noteworthy since ants normally attack other invertebrates enemies or prey or vertebrates perceived as threat for the colony. These behaviours probably derive, as specialized forms, from predatory or nest cleaning behavioural patterns as that showed by some Formica and Pogonomyrmex spp.

Beattie However, not all ants behave in the same way and some species are better than others in protecting their plant partners Koptur Therefore, a strong selection is expected on plants to get the best they can among the potential partners and avoid any form of exploitation of their mutualistic habit Orona-Tamayo and Heil One of the best-studied example is that of Acacia and their obligate Pseudomyrmex partners, which feed only on the sucrose-free nectar produced by their host that is not attractive for generalist exploiters Heil et al.

In fact, invertase sucrose hydrolytic activity is not constitutionally absent in the ant midgut but is inhibited by chitinase, a dominant EFN protein. Once enclosed, young workers ingest EFN as the first diet available and their invertase becomes inhibited. In this way, they are forced to continue feeding on host-derived EFN being unable to digest any other food. In this ant—acacia mutualism, the plant manipulates the digestive capacities of the symbiotic ants to enhance their dependence on the host-derived food rewards, thus stabilizing in this way the partnership and avoiding possible interference by exploiters.

To our knowledge, this is the first clear example of partner manipulation in a plant—ant mutualism based on EFN secretion, as it represents a dramatic change which appears disadvantageous for the ant, at least when considering its possibilities to return to a free-living life style. It could be expected that the above-mentioned example is not the only case of partner manipulation in a plant—ant mutualism as EFNs may have important manipulative and direct effects on other aspects of ant biology and behaviour.

Under the manipulative hypothesis, it is possible that some of the secondary nectar components already known or still to identify, see previous sections have significant effects on ant physiological and behavioural traits resulting in a more effective service for the plant. The core of indirect defence by mutualism with ants is defence against enemies. Hence, among the most obvious aspects of ant behaviour potentially affected by plant manipulation, there is aggression. Indeed, as stated above, ants associated with plants especially myrmecophytes are generally extremely aggressive and reactive to intruders and even alien not living objects.

Thus, it is plausible that EFN-mediated manipulation can affect aggressiveness. Extrafloral nectar could affect several other aspects of ant biology, not necessarily linked with increasing aggression that could promote ant defensive or protective effects.

Most ant—plant mutualisms are facultative or, in some cases, occasional associations, and involve groups of species that may vary in time, space and impact on plant fitness Bronstein et al. In facultative ant—plant mutualism, the mere presence of ants has been found to exert significant effects on plant performance due to non-consumptive effects that deter significantly plant predators or dramatically affect their behaviour with a beneficial cascade effect on plant fitness.

For example, in Gossypium thurberi , the associated ants Forelius pruinosus have a strong disturbing effect on the folivore caterpillars that alter their behaviour, thus reducing plant damage Rudgers et al. Finally, there are experimental evidences showing that the nutritional composition of EFN can alter foraging preferences of ants, enabling plants to manipulate the prey preferences of their mutualistic partners; in this way, plants could ultimately bias prey selection of the ants towards herbivores, competitors or predators that pose the greatest risk to the plant Wilder and Eubanks Inconspicuous actions may also be expression of other important defensive services that ant partner may offer, such as cleaning and protection against pathogens and fungi Beattie ; Rico-Grey and Oliveira ; Heil Interestingly, even inconspicuous actions by non-aggressive species may have crucial protective effects on plants, as in the case of Pheidole bicornis , a small and sluggish ant associated to Piper spp.

Hence, in order to record significant effects on the plant fitness, it is not necessary to imagine dramatic and substantial changes in ant behaviour due to eventual plant manipulation strategies. In accordance with the manipulative hypothesis, it has recently been shown that four alkaloids such as caffeine, theophylline, cocaine and atropine investigation can have significant effects on many aspects of ant physiology and behaviour Cammaerts et al.

Mutualism: Ants and Their Insect Partners

In particular, feeding on the alkaloids altered locomotion, memory, olfactory perception and reactions to stimuli in the model ants Myrmica sabuleti ; in the case of cocaine, dependence was also recorded Cammaerts et al. Interestingly, in other investigation, morphine addiction in ants was reported, as well as behavioural effects on memory and learning. Morphine administration activates the dopamine reward pathways and affects serotonin expression Entler et al.

The recent recognition that minor nectar constituents e. Increasing attention has being devoted on these aspects ant brain anatomy and neurophysiological aspects of ant behaviour thanks also to the improved analytical techniques see for example Gronenberg ; Penick et al. Further investigation in the context of ant—plant interactions will surely add more insight into this interesting topic with possible extensions to more complex neurophysiological systems and eventual applicative outputs on behavioural and physiological manipulation of animals by plants. The indirect herbivore defence service that ants provide for some plants is a fascinating relationship.

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Indeed a key point in the definition of mutualism is that both involved parties may gain benefits from the association. Mutualism, however, typically imply costs for one or both partners and in a dynamic co evolutionary scenario, it is expected that each partner maximizes the benefits and minimize their costs. In this context, a relevant role could be played by contingencies and environmental constraints, and the different outcomes may vary in time and space Menzel et al.

This is particularly likely in diffuse interactions, where multiple species can associate with each other, as is the case of facultative associations between plants bearing EF nectaries and ants. In the present review, we bring forward the hypothesis that plants could maximize ant-derived rewards i. Indeed current theory on mutualism predicts that cooperation between organisms is evolutionarily unstable in the absence of mechanisms that counteract the temptation to cheat Bronstein ; Frederickson From the perspective of each partner, a successful mutualism will maximize the ratio of benefits to costs and be minimally susceptible to cheating; thus, as already hypothesized for carbohydrate-rich EFN Ness et al.

Clearly detailed studies of the costs from both the ant and plant perspective associated with the proposed plant manipulation strategies via secondary metabolites are of outmost importance to fill all the outstanding issues. Representations of demonstrated and hypothetical plant—ant interactions. A Conceptual diagram representing ecological processes in plant—ant interactions. For clarity, the diagram is limited on the interactions that could be affected by secondary metabolites, and many other interactions e.

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The negative interaction between EFN production and plant refers to the fact that, despite being considered a cost-efficient defence strategy in the presence of herbivores, EFN production is costly for plants Bixenmann et al. B Critical processes involved in plant-driven ant manipulation and key knowledge gaps that require investigation in plants bearing extrafloral nectaries.

To conclude, given that some plant-derived chemicals i. However, despite there is evidence that secondary metabolites can influence ant behaviour, specifically preference and memory, there is still quite large knowledge gaps that need to be filled in order to fully understand the nature of plant—ant mutualistic associations see Fig.