Seed manipulation by ants: disentangling the effects of ant behaviours on seed germination

Abstract

1. Seed manipulation by ants can play a key role in seed germination through two main behaviours: elaiosome detachment and seed scarification. Despite the fact that these behaviours are commonplace, their effects have only been quantified independently, and their consequences on seed germination remain controversial.2. Here we experimentally investigate the effects of ant manipulation on seed germination, disentangling the contributions of these two ant behaviours to this process. To do so, under laboratory conditions, we studied the effects of seed manipulation by Acromyrmex subterraneus on germination of seeds from Mabea fistulifera, a myrmecochorous plant. We established six experimental treatments: (i) unmanipulated seeds; (ii) ant-manipulated seeds with the elaiosome detached and scarified; (iii) ant-manipulated seeds with the elaiosome detached and non-scarified; (iv) hand-manipulated seeds with the elaiosome remaining and scarified; (v) hand-manipulated seeds with the elaiosome detached and scarified; and (vi) hand-manipulated seeds with elaiosome detached and non-scarified.3. We found that both elaiosome detachment and seed scarification decreased seed germination rates. Moreover, there was no difference in germination rates whether the seeds were manipulated by researcher's hand or by ants, suggesting a lack of other ant-manipulation effects on seeds.4. The present study shows that manipulation by A. subterraneus can exert negative effects on germination of a myrmecochorous seed. Accordingly, we suggested that studies evaluating the benefits of myrmecochory for plants, based only on seed removal amount and distance, may be overestimating those benefits. Our results contribute to the understanding of the potential mechanisms influencing plant recruitment, especially for myrmecochorous plants inhabiting tropical forests.

Seed germination of a myrmecochorous plant endemic to the Brazilian semiarid region: the wolf is not so bad

“…Seed dispersal by animals, or zoochory, involves interspecific interactions with different levels of specificity between animals and plants (Giladi 2006; Barroso et al 2013;Acevedo-Quintero & Zamora-Abrego 2016;Camargo et al 2019). For example, some myrmecochorous plants produce seeds with an elaiosome, an appendage rich in lipids, proteins, sugars and minerals that can be used directly or indirectly by different ant species as a food resource (Giladi 2006;Fernandes et al 2018). In return, many ant species transport seeds with elaiosome to their nests, thus acting as important seed dispersing vectors Fagundes et al 2021) with positive effects on the organization of plant communities in different environments (Nathan & Muller-Landau 2000;Levine & Murrell 2003;Lengyel et al 2009;Snell et al 2019).…”

“…The manipulation of plant propagules by ants during the removal of the elaiosome or during the transport of the seed to nests can affect seed germinability (germination speed and percentage) (Oliveira et al 1995;Prior et al 2014). In fact, the presence of an elaiosome can affect seed germinability because these appendages have germinationinhibiting substances, or simply because they negatively affect seed imbibition (Fernandes et al 2018). Thus, the simple removal of these appendages by dispersers could break seed dormancy and accelerate germination (Souza et al 2015b;Fagundes et al 2021).…”

Ant species that remove diaspores alone are more efficient removers

“…Ants, along with birds, are the major secondary removers of fleshy diaspores falling on the grounds of Brazilian tropical Giladi, 2006;Leal et al, 2014). In addition, these ants often consume the aril, elaiosome, or even the seed at the site, performing few removals, making difficult the germination or even killing the seed embryo (Fernandes et al, 2018;Pizo & Oliveira, 2000). Conversely, large species are more attracted by elaiosomes with a greater content of some lipids because these components are also found in dead insects and in the prey of these ants (Hughes et al, 1994).…”

Switching roles from antagonist to mutualist: a harvester ant as a key seed disperser of a myrmecochorous plant

“…Despite such a dichotomy, the outcome of an ant-seed interaction is not always clear (Arnan et al, 2012;Fernandes et al, 2018Fernandes et al, , 2019. Some seeds may in fact benefit from harvester ants through 'accidental' dispersal due to seeds being dropped during transport, discarded onto the midden before being consumed, or germinating inside the nest after the nest is abandoned (O'Dowd & Hay, 1980;MacMahon et al, 2000;Aranda-Rickert & Fracchia, 2011).…”