Investment in reward by ant-dispersed plants consistently selects for better partners along a geographic gradient

Abstract

Seed dispersal by ants (myrmecochory) is an asymmetric, presumably mutualistic interaction, where a few ant species benefit many plants. Myrmecochorous plants express specialized adaptations, most notably a large elaiosome, which promote interactions with efficient seed dispersers while decreasing interactions with poor dispersers, resulting in de facto partner choice. However, because variation in plants’ investment in reward and ant response to them may vary spatially and temporally, it is unclear whether such specialization is consistent along geographic gradients; especially towards myrmecochory’s range margin. To answer this question on context-dependent partner choice, we first estimated variation in reward investment by co-occurring myrmecochores along a steep environmental gradient in a Mediterranean region. Second, we tested whether variation in plant investment in reward was positively and consistently correlated with the quality of dispersal plant received along the same gradient. Using in situ cafeteria experiments, we simultaneously presented diaspores of locally co-occurring myrmecochorous species to ants of two guilds representing high- and low-quality dispersers. We then recorded ant-seed behaviour, seed preference and seed removal rates for each ant guild. We found both overall and within-site high variation among plant species in the total and relative investment in elaiosomes. Both ant guilds removed substantial proportion of the seeds. However, scavenging ants (high-quality dispersers) clearly preferred diaspores with larger elaiosomes, whereas granivorous ants (low-quality dispersers) exhibited no preference. Furthermore, both the variation in plant traits and the corresponding response of different ant guilds were consistent along the studied geographic gradient. This consistency holds even when granivores, which removed seeds in a non-selective fashion and provided apparently low-quality seed dispersal services, were, at least numerically, the dominant ant guild. This dominance and the consistency of the partner choice shed light on the functionality of elaiosomes at the margins of myrmecochory’s distribution.

Effects of seed morphology and elaiosome chemical composition on attractiveness of five Trillium species to seed‐dispersing ants

“…Contrary to our prediction, elaiosome mass, elaiosome width, and elaiosome-seed mass ratio were not significantly different among species. These results are not consistent with the results of several studies showing that ants prefer larger elaiosome biomass and/or elaiosome-seed mass ratios (Leal et al, 2014;Levine et al, 2019;Mark & Olesen, 1995), although they do support the finding that ants do not exert significant selection on elaiosome size in Helleborous foetidus . Considering that the most attractive species in our study, T. catesbaei, had smaller average elaiosome mass and smaller elaiosome-seed mass ratios than all of its congeners, these aspects of elaiosome morphology do not appear to be the most important factors contributing to the attractiveness of Trillium seeds to ants.…”

“…Diaspore size, elaiosome biomass, and the elaiosome-seed mass ratio are all known to influence the attractiveness of diaspores to ants (Leal, Lima Neto, Oliveira, Andersen, & Leal, 2014;Mark & Olesen, 1995). Interspecific variation in elaiosome size and elaiosome-seed mass ratios is substantial, and these traits are often correlated (Edwards, Dunlop, & Rodgerson, 2006;Leal et al, 2014;Levine, Ben-Zevi, Seifan, & Giladi, 2019;Reifenrath, Becker, & Poethke, 2012), meaning any interpretation of the effects of one trait should be considered in light of the other. In many systems, effective ant dispersers prefer the seeds of species that produce heavier elaiosomes (Levine et al, 2019;Ness, Bronstein, Andersen, & Holland, 2004;Takahashi & Itino, 2015), although Manzaneda, Rey, and Alcántara (2009) found that ants exerted significant selection on seed size, but not on elaiosome size when both traits were considered simultaneously.…”

“…Interspecific variation in elaiosome size and elaiosome-seed mass ratios is substantial, and these traits are often correlated (Edwards, Dunlop, & Rodgerson, 2006;Leal et al, 2014;Levine, Ben-Zevi, Seifan, & Giladi, 2019;Reifenrath, Becker, & Poethke, 2012), meaning any interpretation of the effects of one trait should be considered in light of the other. In many systems, effective ant dispersers prefer the seeds of species that produce heavier elaiosomes (Levine et al, 2019;Ness, Bronstein, Andersen, & Holland, 2004;Takahashi & Itino, 2015), although Manzaneda, Rey, and Alcántara (2009) found that ants exerted significant selection on seed size, but not on elaiosome size when both traits were considered simultaneously. The nutritional quality of elaiosomes also likely plays a role in ant preference (Caut, Jowers, Cerdá, & Boulay, 2013;Fischer et al, 2008), given that ants disassemble the diaspore and feed the elaiosome to their larvae upon return to the nest (Fischer, Ölzant, Wanek, & Mayer, 2005).…”

Reduced dispersal at nonexpanding range margins: A matter of disperser identity

“…We further predict that the reduction in dispersal may originate from two, nonmutually exclusive, processes: First, plant‐mediated reduction in seed dispersal effectiveness may be related to lower elaiosome attractiveness at range margins. In general, the probability of a seed to be dispersed by a high‐quality disperser increases with elaiosome size or elaiosome/seed mass ratio (Edwards, Dunlop, & Rodgerson, 2006; Levine, Ben‐Zvi, Seifan, & Giladi, 2019; Mark & Olesen, 1996) and with the inclusion of higher concentrations of specific fatty acids (most prominently oleic acid) in the elaiosome content (Boulay, Coll‐Toledano, & Cerdá, 2006; Mayer, Ӧlzant, & Fischer, 2005). We hypothesized that plants in range margin populations, which inhabit small patches of suitable habitat, will produce smaller and less attractive elaiosomes, thus securing more localized dispersal than populations closer to the range core.…”

Ant Guild Identity Determines Seed Fate at the Post-Removal Seed Dispersal Stages of a Desert Perennial

“…However, infrequently, seeds that are carried by granivorous ants may escape predation and be effectively dispersed, either along foraging trails or at refuse piles [ 6 , 18 , 19 ]. Harvester ants, which are among the more dominant members of the granivore guild, tend to exhibit little or no affinity to the presence or size of an elaiosome on a seed [ 20 , 21 ], thus dispersing myrmecochorous seeds only occasionally. Scavenging ants, on the other hand, ignore the seeds of most plant species, but exhibit high affinity for myrmecochorous seeds, which they transport over long-distances, bring to their nest, and leave intact after removing the elaiosome [ 13 ].…”