Ant-seed interactions: combined effects of ant and plant species on seed removal patterns

Abstract

Seed dispersal by ants (i.e. myrmecochory) is usually considered as a mutualism: ants feed on nutritive bodies, called elaiosomes, before rejecting and dispersing seeds in their nest surroundings. While mechanisms of plant dispersal in the field are well documented, the behaviour of the ant partner was rarely investigated in details. Here, we compared in laboratory conditions the foraging behaviour of two ant species, the omnivorous Lasius niger and the insectivorous Myrmica rubra to which seeds of two European myrmecochorous plants (Chelidonium majus and Viola odorata) were given. Ant colonies were simultaneously presented three types of items: entire seeds with elaiosome (SE), seeds without elaiosome (S) and detached elaiosomes (E). The presence of elaiosomes on seeds did not attract workers from a distance since ants first contact equally each type of items. Although ants are mass-recruiting species, we never observed any recruitment nor trail-laying behaviour towards seeds. For ants having contacted seed items, their antennation, manipulation and seed retrieval behaviour strongly varied depending on the species of each partner. Antennation behaviour, followed by a loss of contact, was the most frequent ant-seed interaction and can be considered as a "hesitation" clue. For both plant species, insectivorous Myrmica ants removed items in larger number and at higher speed than Lasius. This fits with the hypothesis of a convergence between odours of elaiosomes and insect preys. For both ant species, the small Chelidonium seeds were retrieved in higher proportion than Viola ones, confirming the hypothesis that ants prefer the higher elaiosome/diaspore-ratio. Thus, in these crossed experiments, the ant-plant pair Myrmica/ Chelidonium was the most effective as ants removed quickly almost all items after a few antennations. The presence of an elaiosome body increased the seed removal by ants excepting for Myrmica which retrieved all Chelidonium seeds, even those deprived of their elaiosome. After 24 h, all the retrieved seeds were rejected out of the nest to the refuse piles. In at least half of these rejected items, the elaiosome was discarded by ants. Species-specific patterns and behavioural differences in the dynamics of myrmecochory are discussed at the light of ant ecology.

Mutualism between co-introduced species facilitates invasion and alters plant community structure

“…This species is biennial or perennial and usually occurs in forest edges and disturbed forests [48]. Myrmica rubra disperses C. majus seeds in its native range [23]. Both introduced species co-occur with native myrmecochores and A. rudis in their introduced ranges [49].…”

“…The approximately 11 000 myrmecochorous plant species worldwide [22] have seeds with lipid-rich appendages (elaiosomes) that attract ants. Foraging ants pick up seeds and carry them back to their nests ( primary dispersal), where they remove elaiosomes and feed them to ant larvae [23]. Intact seeds are deposited in waste middens inside or outside nests (secondary dispersal).…”

“…Like other invasive ants it forms large colonies with numerous interconnected nests (polydomy) and multiple queens ( polygyny) [34,40,41]. Unlike L. humile and S. invicta, M. rubra is an important seed disperser in its native range [23,42]; thus, it may be adapted to consuming elaiosomes as a part of its diet and may have coevolved with Eurasian myrmecochores. Several plant species that M. rubra disperses in its native range have also been introduced to North America, meaning that old and potentially co-adapted partnerships between mutualists are now occurring in a new location where they overlap with native myrmecochores and native seed-dispersing ants.…”

Testing the directed dispersal hypothesis: are native ant mounds (Formica sp.) favorable microhabitats for an invasive plant?

“…Often, collected seeds are brought to the nest where the elaiosome is consumed. Seeds then either remain in the nest or are deposited outside the nest in refuse piles (Beattie 1985;Servigne and Detrain 2008;Renard et al 2010).…”

Invasive goldenrods affect abundance and diversity of grassland ant communities (Hymenoptera: Formicidae)

“…The creation of nests favors the colonization of plant roots by mycorrhizal fungi (Dauber et al 2008) and disturbance to the soil can improve the development of annual plants, some of which are exclusively associated with anthills (Dostál 2007). Ants also spread plant seeds enabling expansion into new areas (Servigne and Detrain 2008). In the case of plant species that use obligatory myrmecochory, displacement of associated ants may cause a significant reduction in population size and may lead to local extinction (Gorb et al 2013).…”