Ant guards influence the mating system of their plant hosts by altering pollinator behaviour

Abstract

31Ant guards can increase plant fitness by deterring herbivores but may also 32 reduce it by interfering with pollination, hence ant-plant interactions are ideal 33 systems in which to study costs and benefits of mutualisms. While ant impacts 34 on herbivory are well-studied, much less is known about impacts on 35 pollinators and associated consequences for plant mating systems and fitness. 36 We used field experiments to quantify the effect of ant guards on pollinator 37 community composition, frequency and duration of flower visits, and 38 cascading effects on plant mating system and plant fitness in Turnera velutina 39 (Passifloraceae). Although ant patrolling did not affect pollinator community 40 composition or visitation frequency, it decreased pollinator foraging time and 41 flower visit duration. Such behavioural changes resulted in reduced pollen 42 deposition on stigmas, decreasing male fitness whilst increasing outcrossing 43 rates. This study contributes to understanding how non-pollinators, such as 44 these defensive mutualists, can shape plant mating systems.45 46 87 tested. Alternatively, an increase in fruit set in ant-patrolled plants of 88 Psycothria limonensis was attributed to pollinator relocation, where ant 89 threats might have caused pollinators to spend less time per flower and visit 90 5 more flowers, promoting pollen transfer (Altshuler 1999). Again, this 91 mechanism was inferred, but not experimentally tested. Previous experiments 92 on Turnera velutina showed that ant corpses placed inside flowers reduce 93 pollinator visit duration (Villamil et al. 2018). However, such an experimental 94 setup may differ from natural circumstances as flower occupation by ants is a 95 rare event, and live ants (in contrast to dead ones) do not remain immobile in 96 the flowers for long periods. Overall, the presence of ants can promote 97 changes in pollinator community composition, visit frequency and duration. 98 This, in turn, could drive positive or negative impacts of ant-pollinator 99 interactions on plant reproduction (Altshuler 1999; Ness 2006). To date, no 100 study has quantified the impacts of ant patrolling on pollinator visitation 101 behaviour, plant mating systems, and fitness under natural conditions. 102 We estimated the ecological and potential evolutionary consequences 103 of myrmecophily on the pollination biology, mating system, and fitness of 104 Turnera velutina (Passifloraceae), a self-compatible ant-plant using an ant 105 exclusion field experiment. We addressed the following questions: (i) What is 106 the effect of ant patrolling on pollinator visitation? (pollinator community 107 composition, visitation frequency, duration, and behaviour) (ii) Does ant 108 patrolling affect the host plant mating system? (iii) Does ant patrolling affect 109 pollen transfer dynamics? (iv) Does ant patrolling affect plant male fitness? 110 First, because smaller or solitary pollinator taxa are expected to be more 111 vulnerable to predation risk than larger or social species (Dukas & ...

Negative effects of ant-plant interaction on pollination: costs of a mutualism

“…Visitors spent in average less time per flower in AA than in the other three treatments. Time is another important variable related to plant fitness, leading to a decrease in pollen removal and fruit set (Calixto et al under review) or an increase in cross-pollination, which can lead to an increase of fruit set (Villamil et al, 2020). For instance, Calixto et al (under review) showed that more aggressive ants can significantly decrease the time spent by pollinators when visiting flowers, resulting in a significant decrease of fruits produced in Qualea multiflora (Vochysiaceae).…”

“…For instance, Calixto et al (under review) showed that more aggressive ants can significantly decrease the time spent by pollinators when visiting flowers, resulting in a significant decrease of fruits produced in Qualea multiflora (Vochysiaceae). On the other hand, Aguirre-Jaimes et al (2018) showed that the effective pollinator of Vigna luteola (Fabaceae) spent less time visiting flowers in order to avoid ant predation, which might result in an increase of fruit set; and Villamil et al (2020) observed in Turnera velutina (Passifloraceae) that ants decreased pollinator foraging time and flower visit duration, but increased outcrossing rates. Given that, it seems that the time spent by pollinators can have different effects depending on the system that they are involved, resulting in negative, neutral, or positive effects to plants (Gonzálvez et al, 2013;Sousa-Lopes et al, 2020).…”

Emerging Trends in Ant–Pollinator Conflict in Extrafloral Nectary-Bearing Plants

“…Although there seems to be a clear negative effect of the presence of ants when foraging on flowers on pollinator behavior, a few studies have shown positive outcomes [ 23 , 33 , 51 , 54 ]. Decreasing pollinator visitation to flowers in response to the presence of ants may lead to decreased self-pollination or may increase the likelihood of cross-pollination, as pollinators are forced to constantly change flowers within plants and/or to move to other plants due to the presence of ants [ 23 , 33 , 51 , 54 ]. In this context, there is a decrease in the foraging efficiency of pollinators on the same plant individual but an increase in movement between individual plants, bringing positive effects for plant reproductive success.…”

“…Knowing the identity of the ants, herbivores, plants, and pollinators can be essential to understanding the levels of protection and pollination disruption established. More aggressive ants are expected to provide better protection to plants against herbivore attack, but at the same time they can have a greater influence on pollination processes than less aggressive ants, showing context-dependent outcomes [ 54 , 101 , 102 , 103 , 104 ].…”