Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

Orivel, Jérôme; Lambs, Luc; Malé, Pierre‐Jean G.; Leroy, Céline; Grangier, Julien; Otto, Thierry; Quilichini, Angélique; Déjean, Alain

doi:10.1007/s00442-010-1739-5

Cited by 26 publications

(26 citation statements)

References 36 publications

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“…The size and structure of the ant colonies were calculated from 30 different A. octoarticulatus colonies, whereas data for the A. decemarticulatus colonies were taken from Orivel et al [24]. All of the leaves and stems on each plant individual were cut off and placed into a plastic bag, and then preserved in 70% ethanol.…”

Section: Materials and Methods (A) Study Site And Speciesmentioning

confidence: 99%

“…Hirtella physophora is a long-lived myrmecophyte that grows strictly in the understory of terrafirme Amazonian forests, mostly in patches located on the uppermost parts of hillsides [24,25]. Its leaves bear extrafloral nectaries and a pair of pouches (domatia) at the base of each lamina that house ant colonies [26].…”

Section: Materials and Methods (A) Study Site And Speciesmentioning

confidence: 99%

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Trade-offs in an ant–plant–fungus mutualism

et al. 2017

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Species engaged in multiple, simultaneous mutualisms are subject to trade-offs in their mutualistic investment if the traits involved in each interaction are overlapping, which can lead to conflicts and affect the longevity of these associations. We investigate this issue via a tripartite mutualism involving an ant plant, two competing ant species and a fungus the ants cultivate to build galleries under the stems of their host plant to capture insect prey. The use of the galleries represents an innovative prey capture strategy compared with the more typical strategy of foraging on leaves. However, because of a limited worker force in their colonies, the prey capture behaviour of the ants results in a trade-off between plant protection (i.e. the ants patrol the foliage and attack intruders including herbivores) and ambushing prey in the galleries, which has a cascading effect on the fitness of all of the partners. The quantification of partners' traits and effects showed that the two ant species differed in their mutualistic investment. Less investment in the galleries (i.e. in fungal cultivation) translated into more benefits for the plant in terms of less herbivory and higher growth rates and vice versa. However, the greater vegetative growth of the plants did not produce a positive fitness effect for the better mutualistic ant species in terms of colony size and production of sexuals nor was the mutualist compensated by the wider dispersal of its queens. As a consequence, although the better ant mutualist is the one that provides more benefits to its host plant, its lower host–plant exploitation does not give this ant species a competitive advantage. The local coexistence of the ant species is thus fleeting and should eventually lead to the exclusion of the less competitive species.

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Section: Materials and Methods (A) Study Site And Speciesmentioning

confidence: 99%

Section: Materials and Methods (A) Study Site And Speciesmentioning

confidence: 99%

Trade-offs in an ant–plant–fungus mutualism

et al. 2017

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“…As a result of its modular growth, H. physophora can produce several reproductive units per individual during each flowering season. In addition, Hirtella physophora has been proven to have a lifespan 10 times superior to that of A. decemarticulatus colonies (Orivel et al 2011), which can count in the determination of the overall fitness of the individuals.…”

Section: Resultsmentioning

confidence: 99%

“…The ultimate cause of this castration behaviour has been demonstrated to be related to the reallocation of plant energy from reproduction to growth (Yu 2001;Frederickson 2009). Since A. decemarticulatus colony size greatly depends on the number of domatia (Orivel et al 2011), the ants should directly benefit from having more living space in which to expand their colony. The novelty of this system lies in the survival of almost one-third of the buds after the partial castration of the plant (but see Edwards and Yu 2008).…”

Section: Direct Negative Impact Of Ant Presence On Plant Reproductionmentioning

confidence: 99%

An ant symbiont directly and indirectly limits its host plant’s reproductive success

et al. 2011

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In theory, mutualisms are intrinsically unstable, and the search for the maximum profit at the minimum cost should lead every mutualist to become a parasite. From an empirical point of view, mutualisms are ubiquitous and of major importance to ecosystems, suggesting the existence of mechanisms that enhance the maintenance of such relationships. We focused on the obligatory myrmecophytic association between the Neotropical plant Hirtella physophora (Chrysobalanaceae) and the ant Allomerus decemarticulatus (Myrmicinae). The plant shelters the ants in leaf pouches in exchange for protection from phytophagous insects. We experimentally demonstrated that the ants partially castrate their host plant by destroying almost two-thirds of its floral buds. The ants also impede pollination through their presence and interactions with pollinators. These results reveal that ant activity negatively affects the plant's reproduction both directly and indirectly. This dual negative effect does not result in the complete castration of the plant. We also highlight major limitations to plant reproduction due to the spontaneous abscission of flowers and to the limited quantity and/or poor quality of the pollen. These limitations must not be overlooked since they can alter the outcome of the association of H. physophora with its ant partner. We therefore conclude that the evolutionary fate of the relationship depends on both ant castration intensity and obstacles to plant fertilization not related to the presence of ants.

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“…decemarticulatus is the main obligatory inhabitant of Hirtella physophora (Chrysobalanaceae) with a single mature colony per plant; this ant species has never been found associated with other myrmecophytic species (Grangier et al 2009). H. physophora is a long-lived understory treelet that has leaves with a pair of domatia at the base of each lamina (Leroy et al 2008; Orivel et al 2011). The species occurs mostly in patches on the upper slopes of hillsides (Solano et al 2003).…”

Section: Methodsmentioning

confidence: 99%

Convergent structure and function of mycelial galleries in two unrelated Neotropical plant-ants

2017

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The construction process and use of galleries by Azteca brevis (Myrmicinae: Dolichoderinae) inhabiting Tetrathylacium macrophyllum (Salicaceae) were compared with Allomerus decemarticulatus (Myrmicinae: Solenopsidini) galleries on Hirtella physophora (Chrysobalanaceae). Though the two ant species are phylogenetically distant, the gallery structure seems to be surprisingly similar and structurally convergent: both are pierced with numerous holes and both ant species use Chaetothyrialean fungi to strengthen the gallery walls. Al. decemarticulatus is known to use the galleries for prey capture and whether this is also the case for Az. brevis was tested in field experiments. We placed Atta workers as potential prey/threat on the galleries and recorded the behaviour of both ant species. We found considerable behavioural differences between them: Al. decemarticulatus was quicker and more efficient at capture than was Az. brevis. While most Atta workers were captured after the first 5 min by Al. decemarticulatus, significantly fewer were captured by Az. brevis even after 20 min. Moreover, the captured Atta were sometimes simply discarded and not taken to the nest by Az. brevis. As a consequence, the major function of the galleries built by Az. brevis may, therefore, be defense against intruders in contrast to Al. decemarticulatus which uses them mainly for prey capture. This may be due to a higher need for protein in Al. decemarticulatus compared to coccid-raising Az. brevis.Electronic supplementary materialThe online version of this article (doi:10.1007/s00040-017-0554-y) contains supplementary material, which is available to authorized users.

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Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

Cited by 26 publications

References 36 publications

Trade-offs in an ant–plant–fungus mutualism

Trade-offs in an ant–plant–fungus mutualism

An ant symbiont directly and indirectly limits its host plant’s reproductive success

Convergent structure and function of mycelial galleries in two unrelated Neotropical plant-ants

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