Influence of neighboring plants on the dynamics of an ant–acacia protection mutualism

Abstract

Ant-plant protection symbioses, in which plants provide food and/or shelter for ants in exchange for protection from herbivory, are model systems for understanding the ecology of mutualism. While interactions between ants, host plants, and herbivores have been intensively studied, we know little about how plant-plant interactions influence the dynamics of these mutualisms, despite strong evidence that plants compete for resources, that hosting ants can be costly, and that host-plant provisioning to ants can therefore be constrained by resource availability. We used field experiments in a semiarid Kenyan savanna to examine interactions between the ant-plant Acacia drepanolobium, neighboring grasses, and two species of symbiotic acacia-ants with divergent behaviors: Crematogaster mimosae, an aggressive symbiont that imposes high costs to host trees via consumption of extrafloral nectar, and Tetraponera penzigi, a less-protective symbiont that imposes lower costs because it does not consume nectar. We hypothesized that by competing with acacias for resources, neighboring grasses (1) reduce hosts' ability to support costly C. mimosae, while having little or no effect on the ability of hosts to support low-cost T. penzigi, and (2) reduce sapling growth rates irrespective of ant occupant. We factorially manipulated the presence/absence of grasses and the identity of ant occupants on saplings and evaluated effects on colony survivorship and sapling growth rates over 40 weeks. Contrary to prediction, the high-cost/high-reward nectar-dependent mutualist C. mimosae had higher colony-survival rates on saplings with grass neighbors present. Grasses appear to have indirectly facilitated the survival of C. mimosae by reducing water stress on host plants; soils under saplings shaded by grasses had higher moisture content, and these saplings produced more active nectaries than grass-removal saplings. Consistent with prediction, survival of low-cost/low-reward T. penzigi did not differ significantly between grass-removal treatments. Saplings occupied by low-cost/low-reward T. penzigi grew 100% more on average than saplings occupied by high-cost/high-reward C. mimosae, demonstrating that mutualist-partner identity strongly and differentially influences demographic rates of young plants. In contrast, contrary to prediction, grass neighbors had no significant net impact on sapling growth rates. Our results suggest that neighboring plants can exert strong and counterintuitive effects on ant-plant protection symbioses, highlighting the need to integrate plant-plant interactions into our understanding of these mutualisms.

Frenemy at the gate: Invasion by Pheidole megacephala facilitates a competitively subordinate plant ant in Kenya

“…Because P. megacephala does not induce nectar production on A. drepanolobium , its invasion also is likely to indirectly facilitate T. penzigi by generating a landscape of low‐reward host plants, a process that may “screen” out the more energetically demanding, nectar‐dependent Crematogaster mutualists (see Archetti et al 2011, Heil 2013). Our experimental manipulation of host plant nectaries showed that establishment success was higher for T. penzigi queens and lower for Crematogaster queens on low‐reward host plants, consistent with a prior study demonstrating greater persistence of T. penzigi vs. C. mimosae colonies on saplings with lower reward levels (Palmer et al 2017). Coupled with the recruitment limitation we observed for Crematogaster spp.…”

“…“stress tolerance” traits including T. penzigi ’s lower dependence on host plant nectar (Palmer et al 2002, 2017), and avoidance and escape behaviors allow for longer persistence times on host plants, allowing colonies to reach reproductive maturity. Although C. nigriceps is also a strong colonist (Stanton et al 2002), its strong dependence on host plant nectar and high levels of interspecific aggression (Palmer 2004) likely underlie its inability to persist within invaded habitats.…”

Tree resprout dynamics following fire depend on herbivory by wild ungulate herbivores

“…new unlignified spines), compounded by the low concentrations of polyphenolics and tannins in young A. drepanolobium leaves (Rubanza et al., ), though an extensive diet study (in unburned habitat) found no evidence that cattle consume A. drepanolobium (Odadi et al., ). We suggest several other potential reasons that cattle did not increase tree height as we had expected, and may instead have reduced it: (a) by reducing grass cover, cattle may have increased the apparency of resprouts to wild ungulate browsers (Riginos & Young, ), in particular steenbok, which are small browsers that have access to all KLEE plots; (b) grass reduction by cattle may have indirectly increased stress from the physical environment, for example, by increasing evaporative demand (Maestre, Bautista, & Cortina, ; Palmer et al., ); or (c) cattle may have trampled resprouting tree tissues (Cumming & Cumming, ).…”

Intraspecific competition favors ant–plant protective mutualism

“…The result suggests that a higher population density and genetic diversity within plant populations favor the establishment of ant–plant protective mutualisms. Although I only focused on intraspecific competition, further investigations on interspecific competition may also contribute to gaining a better understanding of the ant–plant protective mutualisms (Palmer et al, 2017). Accordingly, the findings of this study highlight the need to take into consideration plant–plant interactions when investigating ant–plant mutualisms.…”