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Ecology and Evolutionary Biology
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“Redirecting” the Study of Mutualistic Benefits To
Plants In Myrmecochory
Mariah Taylor Patton
[email protected]
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Patton, Mariah T. "“Redirecting” the study of mutualistic benefits to plants in myrmecochory" (2014). University of Tennessee
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“Redirecting” the study of mutualistic benefits to plants
in myrmecochory
By Mariah Patton
Mentor: Dr. Charles Kwit
1
Abstract
Myrmecochory is typically cast as a mutualistic relationship in which seed
dispersal of plants with elaiosome-bearing seeds is performed by ants. Benefits
of this mutualism may seem simple at first: ants gain a nutritive reward via
elaiosomes, while plant propagules gain protection and a more suitable microsite
for establishment and growth. However, there is growing literature suggesting
that ants may not consistently receive benefits from elaiosome-based diets, and
studies depicting plant benefits are constrained by the “ideal” model framework,
by temporal limitations, and by limitations of sources of mortality that have
typically been investigated. Furthermore, from the plant perspective, many key
parts as well as inconsistencies within this more complex process have not been
well explored. Here, I provide a more realistic guiding framework and identify
where research needs to be further conducted and what questions should be
answered to better address the positive mechanistic role ants may play in this
quintessential mutualism.
Introduction
Mutualisms are defined and cast as involving positive outcomes for both
partners. In this relationship, each partner benefits from the other in a positive
fashion, often through the provision of services. Mutualistic interactions among
organisms have been described and quantified in a variety of ways, with specific
benefits gained from each partner being easily recognizable. In mutualisms
involving plant-animal interactions, each partner gains a fitness advantage from
the other’s involvement (Bronstein 1994).
2
Quintessential examples of mutualisms involving plants and animals include
pollination (Fenster et al. 2004), ants and extra-floral nectaries (Bentley 1976),
and animal-mediated seed dispersal (Howe and Smallwood 1982). While each of
these general interactions is cast as a mutualism, their coevolutionary nature
invokes complexities. Thus, the notion that both partners typically benefit belies
the mutualistic assertion. In pollination, there is a clear view of gains from both
partners- the pollinator gains food and the plant gains the benefit of spreading its
genetic material. In the mutualistic relationship between ants and extra-floral
nectaries, ants benefit from the food gained by these nectaries while the plants
benefit from protection by their ant partners from herbivorous predators. In
animal-mediated seed dispersal, the disperser often gains food while the plant
gains advantage by obtaining distance from the parent plant (Janzen 1970;
Connell 1971; Cheplick 1992). Despite numerous examples of mutualistic
animal-mediated seed dispersal, one of the best-supported examples is that of
myrmecochory (Howe and Smallwood 1982; Hanzawa et al. 1988; Wenny 2001;
Wang and Smith 2002). As with other coevolutionary relationships, though,
myrmecochory may not be a perfect mutualism, and is arguably a poorly
conceived mutualistic process.
Myrmecochory
Myrmecochory, seed dispersal by ants of plants with elaiosome-bearing seeds, is
a widespread phenomenon, pertaining to over 11,000 plant species in over 77
plant families (Lengyel et al. 2009) as well as at least 71 different species of
omnivorous and carnivorous ants (Christianini et al. 2012). Not only has this
3
mutualism become widespread among types of plants, but myrmecochory has
also been shown to independently evolve somewhere from 101 to 147 times
(Lengyel et al. 2009). This mutualistic relationship can be found in a variety of
sites, including nutrient-poor soil areas of sclerophyllous Australia (Berg 1975;
Rice and Westoby 1986; Orians and Milewski 2007) and South Africa (Milewski
and Bond 1982), Mediterranean climates (Espadaler & Gómez 1996), a mix of
dry forest patches and more semi-arid sclerophyllous areas of the Caatinga
ecosystem in Brazil (Leal et al. 2007), and north temperate meadows and forests
(Beattie and Culver 1981; Handel et al. 1981; Beattie 1983).
One identifying feature that defines myrmecochory is the presence of a seedattached elaiosome. The elaiosome is a lipid- and protein-rich appendage that
attracts ants to carry away the plant’s diaspore (dispersal unit of seed and
elaiosome) (Giladi 2006) and provides nutritional reward primarily to developing
brood in the nest (Boulay et al. 2005). Elaiosomes vary in physical and chemical
structure from plant to plant and place to place (Beattie 1985; Turner and
Frederickson 2013; Reifenrath et al. 2012). The morphology of these elaiosomes,
along with that of the ants involved (especially size and shape of mandibles)
determines diaspore movement success (Gunther and Lanza 1989; Oostermeijer
1989; Hughes and Westoby 1992). The variation of chemical makeup of
elaiosomes influence movement as well. To attract ants, a diglyceride component
called diolene 1:2 has been shown to be very effective (Marshall et al. 1979).
However, it has been shown that an increased expression of a different
compound, oleic acid, can be used as a competitive advantage to attract even
4
more ants to retrieve seeds (Turner and Frederickson 2013). Oleic acid in nature
often induces what is known as corpse-carrying behavior, wherein ants carry
their dead to a midden pile (Skidmore and Heithaus 1988). This acid is also
similar to insects’ haemolymph, which also incites a prey-carrying behavior as
well among carnivorous ants (Skidmore and Heithaus, 1988; Hughes et al. 1994;
Boulay et al. 2006; Gammans et al. 2006; Fischer et al. 2008). Nutritional
makeup of elaiosomes differs among myrmecochores as well, especially in lipid
composition (Pizo and Oliveira 2001). While their presence is important for
diaspore detection and movement to nest locations, ramifications of elaiosome
consumption and removal are in need of further and better-formulated studies, as
well as better integration into mutualistic models of myrmecochory.
Benefits of Myrmecochory
Benefits to ants
The putative benefits ants derive from elaiosomes are dietary in nature, yet the
fitness consequences of engaging in the mutualism (i.e., incorporating
elaiosomes into the diet) have not been well explored. Beattie (1985)
emphasizes that the food needed to support ants is dependent on the state of the
colony. Different castes of the ant colony have different energetic needs. Ant
workers, for example, need quick sugar sources or carbohydrates to sustain their
more active roles in the colony (Wilson and Eisner 1957). Thus, food sources
other than elaiosomes that contain mostly fatty acids and other lipids as well as
essential amino acid and less sugar and protein may be more preferential
(Fischer et al. 2005).
5
This being said, elaiosomes may serve as an important food source for a
colony that may be comprised of a high density of larvae whose nutritional
requirements consist of proteins and fats (Vinson 1968; Hölldobler and Wilson
1990). Elaiosomes could also potentially serve as a vital resource when other
foods may not be available (Hughes et al. 1994; Clark and King 2012). Morales
and Heithanus (1998) claim that not only do ants use these elaiosomes as a food
source, but also these elaiosomes can alter sex ratios in colonies in producing
more reproductive females. Other than the work of Gammans et al. (2005), there
is little support for the fitness benefits conferred to ants via elaiosomes of
myrmecochorous plants.
Some recent studies have suggested that feeding on elaiosomes may not
always be of benefit to ant populations. For example, Turner and Frederickson
(2013) showed that while Trillium grandiflorum diaspores attracted more seed
dispersers with higher oleic acid content, more ant worker death were reported
compared to ants that dispersed diaspores of other myrmecochores. This study
shows a significant detrimental effect to the ant in this relationship, and
corroborates other work showing that signaling outweighs nutritional benefit
when seeds are dispersed by ants (Pfeiffer et al. 2012). An isotope study form
Clark and King (2012) also show that nutrition from elaiosomes is more
facultative in nature; ants benefit more from elaiosomes when insect prey is not
as abundant. An additional isotopic study revealed similar results, in that pupae
production in Aphaenogaster senilis was not enhanced by supplementation of
elaiosomes (Caut et al. 2013). While the benefits conferred to ants do not
6
constitute the main subject of this review, as these studies suggest, it is clear that
the direct benefit gained from ants in the mutualism of myrmecochory remain
unsolved.
Benefits to plants
In a much better fashion than for ants, plants have been shown to benefit in a
number of ways through the mutualism of myrmecochory. Indeed, a thorough
review of the topic describes the advantages gained by plants as the placement
of seeds in an appropriate germination site: below ground, away from predators,
and probably in enriched soil (Rico-Gray and Oliveira 2007). An overlooked
portion of this model is the assumed importance and removal of elaiosomes,
often by larvae within ant nests. When combined, the model depicted in Fig. 1
exemplifies the positive benefits gained by plants in this relationship. In short,
foraging worker ants detect diaspores (an intact seed with elaiosome attached),
pick them up and carry them to the nest, where elaiosomes are consumed by
larvae. Afterwards, seeds remain in the nest or are redispersed out of the nest to
nearby midden piles (Beattie 1985; Hughes and Westoby 1992; Gomez and
Espadaler 1998; Gorb et al. 2000), where they subsequently germinate and
establish in nutrient-rich microsites. While numerous empirical and experimental
studies attest to various facets of these ant-mediated advantages (see below),
the advantages in this framework (1) are not consistent across all systems, and
are sometimes ephemeral, (2) lack explicit mention of physical or chemical seed
treatment, and (3) rarely if ever incorporate multiple participants, including not
only multiple ant species (and ramifications thereof), but also involvement of
7
other taxa (e.g., microbes). As cast, the “perfect picture” of myrmecochory for
plants posed in Fig. 1 has rarely been documented in its entirety; some examples
come close (Aranda-Rickert and Fracchia 2011), while others fail to meet the
standards (see Bas et al. 2007; Leal et al. 2007; Martins et al. 2009). Here, we
confront the three aforementioned issues and in the process, pose a new
framework to consider this classic coevolutionary relationship, in particular from
the plant perspective.
!"
!"
Figure 1. The more commonly viewed and simple process of myrmecochory where ants
take diaspores (seeds + elaiosomes) back to the nest, where elaiosomes are consumed
by developing larvae, followed by subsequent seed germination in nutrient-rich
environments.
8
The plant advantages of myrmecochory meet at the nexus of the ‘directed
dispersal’ hypothesis and the ‘nutrient enrichment’ hypothesis. These hypotheses
have been developed independently, and have been considered together in
some vertebrate-mediated seed dispersal processes (Andresen 1999; Brewer
and Rejmánek 1999; Chapman 1989; Chapman et al. 1992; Chavez-Ramirez
and Slack 1994; Davidar 1983; Janzen 1986), though their intermingling is
regularly posed in descriptions of myrmecochory. Howe and Smallwood (1982)
first proposed the directed dispersal hypothesis as a phenomenon where
adaptations of a diaspore ensure that the seed is taken to a more suitable site for
establishment. The nutrient enrichment hypothesis was first developed in a
myrmecochorous system by Beattie and Culver (1982), stating that seeds are
placed in microsites that may be dense in available nutrients which allows for
successful establishment as opposed to areas elsewhere. The primary
advantages of ants moving seeds in this relationship include burial, escape from
predators (which may or may not be tied to burial), and placement in enriched
soil conferring higher germination success. Each of these has substantial
backing in the literature.
Seed burial in myrmecochory is often intertwined with escape from dangers
such as predators and fire. Positive effects of seed burial on seed survival have
been determined experimentally in a number of systems, including a variety of
forest and non-forest habitats in Spain (Manzaneda et al. 2005), deciduous
forests of eastern North America (Kwit et al. 2012), and fire-prone fynbos in
South Africa (Christian and Stanton 2004). In the latter case, deeper-buried
9
Leucospermum truncatulum seeds experienced less predation by granivorous
rodents; however, this came with the caveat of remaining dormant in the
seedbank (Christian and Stanton 2004). So even though burial within ant nests
may translate into short-term escape from fire and predators, it may prove
detrimental without redispersal (Renard et al. 2010).
Ants disperse seeds of myrmecochorous plants short distances, but these
distances may be enough to escape distance-dependent predation. Based on
7889 observations from multiple studies, the mean ant-mediated seed dispersal
distance currently ranks at 2.24 +/- 7.19 m, with variation depending on the
vegetation found in the area studied and the ants observed in the relationship
(Gomez and Espalder 2013). Andersen (1988) related observed seed dispersal
distances and % frequency of the seeds found in ant nests. Since fitted models in
Andersen (1988) resemble those of known optimal dispersal curves shown by
Green (1983), and distances agree with scales that were shown by Antonovics et
al. (1987) to respond well to environmental heterogeneity, dispersal away from
the parent plants would be expected to be beneficial. The short dispersal
distances provided by ants may also be complemented by enough integration of
non-sib individuals such that distance- or frequency-dependent seed mortality
may be offset (Kalisz et al. 1999).
Last, locations of ant seed dispersal have been documented as being
nutrient-rich. The seed without its elaiosome is often assumed to be abandoned
in the nest or a midden or pile in the immediate vicinity: a nutrient-rich
environment, where probabilities of emergence and establishment are enhanced
10
(Beattie and Culver 1982, 1983; Beattie 1985; Smith et al. 1989; Woodell and
King 1991; Hughes and Westoby 1992; McGinley et al. 1994). Being placed in a
nutrient-rich microsite, can lead to some crucial benefits gained by the dispersed
seed. For example, a study by Prior et al. (2014) showed that the longer that
Chelidonium majus seeds remained in Aphaenogaster rudis nests, the more
seedlings emerged. Seeds that remain in these nests have a longer time frame
to take advantage of absorbing essential nutrients in such a nutrient enriched
microsite. Emerging seedlings from these microsites have also been considered
more numerous, healthy, and having a longer longevity (Beattie 1985). This has
been exemplified by some studies, including those of the invasive Euphorbia
esula, which was found in higher densities on Formica obscuripes ant mound
soils, which contained higher levels of nitrogen and phosphorous than
surrounding non-mound soils (Berg-Binder et al. 2012). Aside from being
nutrient-rich, these ant nests may also provide preferred moist microhabitat
conditions that are more suitable to germination. While some work has been
done to clarify the exact benefits of the two players of this relationship, the exact
benefits or whether these services always remain beneficial remains unclear.
Inconsistencies in the Mutualism of Myrmecochory
While many of the cases above illustrate the utility of ants dispersing seeds of
myrmecochores, they do not provide a consistent, all-encompassing view of plant
benefits. Each of the aforementioned advantages conferred by ants can be
thrown into suspicion when one considers that (1) benefits from seed burial are,
in some cases, detrimental, and in many cases, ephemeral; (2) benefits from the
11
direct seed treatment of elaiosome removal are overstated; and (3) ants may
involve other taxa into the equation for plant fitness.
Seed burial
Though ant-dispersed seed burial can lower probabilities of seed depredation,
the locations of nest chambers can make any short-term benefits null and void.
Many destinations may be too far underground for germination to ever take
place. One study conducted by Renard et al. (2010) showed that Ectatomma
brunneum ants in French Guinnea would carry diaspores from Manihot esculenta
subsp. flabellifolia 14 to 40 cm deep within chambers of the nest, where
elaiosomes are consumed by their brood. Such depths are considered much too
deep for successful germination to occur for this plant species. In addition to this,
the microsites of nests of numerous seed-dispersing ant species are not
conducive to seed germination and subsequent seedling establishment. In
addition to nesting in leaf litter, the most prominent seed-dispersing ant genus in
North America, Aphaenogaster, is known to nest in rotting logs and under rocks
(Canner et al. 2012), both of which are inhospitable to establishment. This
emphasizes the importance of ants redispersing the elaiosome-removed seeds
to more favorable depths and/or microsites outside the nest. Very few studies,
with the exception of Renard et al. 2010 and Servigne and Detrain 2010, actually
follow seed destination into the nest, emphasizing the need for further empirical
or experimental work on burial depths and their effects on seed germination.
The time ant-dispersed seeds remain in ant nests may be short in a number
of cases. While redispersal of seeds out of ant nests and into middens or piles
12
has been documented (see above), new evidence points towards isotropic
redispersal at short distances from the nest. Canner et al. (2012) showed that the
keystone ant partner in myrmecochory in eastern North America, Aphaenogaster
rudis, redisperses around 93% of handled seeds outside of the nest and into the
surrounding leaf litter within one week of the primary dispersal event. Hence, antdispersed seeds may not gain a long-assumed, long-term benefit of remaining
hidden below-ground in ant nest chambers, or the even longer-term, longassumed advantage of nutrient-rich ant nest sites that would be advantageous
post-germination. Short-distance isotropic redispersal from ant nests may still
result in advantageous circumstances. Canner et al. (2012) emphasized that
such redispersal away from ant nests can widen the spatial density of
myrmecochorous seeds, which may lower the probability of seed predation by
density-dependent predators, particularly mammals (see Heithaus 1981).
Elaiosome removal
Removal of elaiosomes is often posed as the most important direct treatment
seed-dispersing ants provide to seeds. Indeed, a number of myrmecochorous
plants, though not all, have been shown to benefit from the removal of
elaiosomes (Table 1). Advantages include increased probabilities of seed
germination, and the hastening of seed germination. In addition, seeds not
having elaiosomes removed are exposed to higher predation risks, especially by
mammals (Heithaus 1981; Garrido et al. 2009; Kwit et al. 2012). Much of the
evidence therefore hints towards the importance of elaiosome removal, which is
often assumed to take place in the nest of seed-dispersing ants. It should be
13
noted, however, that with the exception of the work conducted by Boyd (2001),
the vast majority of the work on benefits of elaiosome removal have all involved
experimental removal of elaiosomes by humans. Hence, there is little information
known about the specific benefits of the direct physical handling of
myrmecochore seeds by ants.
Table 1. Various studies showing the effects of ants “handling” seeds. (G = germination,
SP = seed predation, E= emergence, + = advantageous to plant, - = disadvantageous to
plant).
Paper
Location
Plant Species
Ant Species Observed Handling
Variables
Prior et al.
2014
Cumberlan
d&
Kirkman
2013
Kwit et al.
2012
SalazarRojas et al.
2012
Deciduous forest
southern Ontario
Chelidonium majus
Aphaenogaster rudies & Myrmica rubra
G(+)
SW Georgia
common ground
cover sp.
Solenopsis invicta
G(NS)
Ohio, USA
Asarum canadense
Most likely Aphaenogaster rudis
SP(+)
CICOLMA Mexico
Turnera ulmifolia L.
Forelius analis
E(+)
Soriano et
al. 2012
Central Apennine
(Mediterranean, EuroSiberian regions)
Moehringia
papulosa
N/A
G(+)
Garrido et
al. 2009
Iberian Peninsula
Helleborus foetidus
36 species mostly from Aphaenogaster,Camponotus,
and Lasius
E(+),SP(+)
Cassaza et
al. 2008
Italy, Argentina
Moehringia trinervia
L., M. mucosa L., M.
sedoides, M. lebrunii
Merxm
Lasius emarginatus, Pheidole pallidula, Crematogaster
scutellaris
G(+)
Leal et al.
2007
Caatinga ecosystem
(north-east Brazil
Euphorbiaceae
Cyphomyrmex, Crematogaster, Dorymyrmex,Pheidole
and Trachymyrmex species
G(+)
Imbert 2006
Massif de la Cape, near
Narbonne (S of France
Euphorbia
characias,Centaurea
corymbosa
Pheidole pallidula, Crematogaster scutellaris
G(-)
fynbos shrublands of
South Africa.
Leucospermum
truncatulum
Anoplolepis custodiens, A. steingroveri, Pheidole
capensis
E(NS),
SP(+)
semideciduous forest in
S.E. Brazil
Croton priscus
(Euphorbiaceae)
Atta sexdens and Pheidole
G(NS)
Pheidole pallidula, Aphaenogaster senilis, Tapinoma
nigerrimum, Messor barbarus
SP(+)
Grevillea buxifolia,
G. linearifolia, G.
speciosa, G. caleyi,
G. longifolia, G.
shiressii
Crematogaster, Iridomyrmex ‘vicinus’, Pheidole,
Rhytidoponera, I. ‘purpureus’, I. ‘gracilis’,Dolichoderus
‘doriae’, Anonychomyrma, Paratrechina
SP(+)
Fremontodendron
decumbens
Messor andrei
G(NS),
SP(+)
Polygala vayredae
Crematogaster scutellaris, Formica gagates
G(NS),
SP(NS)
Christian &
Stanton
2004
Passos and
Ferreira
1996
Espadaler
& Gómez
1996
Auld &
Denham
1999
Euphorbia characias
Barcelona, Spain
Sydney, Australia
central California
Boyd 2001
Castro et al.
2010
Alta Garroxta, Girona
(Catalunya, Spain)
14
Carney et
al. 2003
Bas et al.
2007
coastal San Diego,
California
Mediterranean
Martins et
al. 2009
Campinas, SE Brazil
Cuautle et
al. 2005
coastal sand dune
matorral in Mexica
Ohkawara
2005
deciduous forest Japan
Perernelli et
al. 2003
Ruhren and
Dudash
1996
Brazil
SE deciduous forest in
Langley, Virginia
Dendromecon rigida
Linepithema humile, Pogonomyrmex subnitidus
SP(NS)
Rhamnus alaternus
L. (Rhamnaceae)
Aphaenogaster senilis, A. subterranean, Tetramorium
ruginode, T. semilaeve, Myrmica sabuleti, Pheidole
pallidula
G(-)
Ricinus communis
Dorymyrmex brunneus, Pheidole gertrudae, Pheidole
sp. 1, Pheidole sp. 2, Solenopsis sp. 1
G(+)
Turnera ulmifolia
F. analis, Pheidole sp. 1, Pheidole sp. 2, S. geminta, D.
bicolor, P. longicornis, M. cyaneum
G(+)
Erythronium
japonicum
Mabea fistulifera
N/A
Atta sexdens rubropilosa, Acromyrmex subterraneus
subterraneus
Erythroniu
americanum
Aphaenogaster rudis
G(+)
G(+)
SP(+)
Other predators and participants
Mammals are cast as the primary seed predators of myrmecochores, but they
may not be the only sources of mortality. The vast majority of studies addressing
seed predation of myrmecochores emphasize that mammals, especially small
rodents, are the primary sources of seed mortality (Reichman 1980; Heithaus
1981; Smith et al. 1989; Auld and Denham 1999; Fuchs et al. 2000). However,
much like fruits and arils, elaiosomes likely attract fungi and bacteria that could
cause issues with seed survival, especially in cases where diaspores are not
dispersed (and elaiosomes are not removed). Dispersed and redispersed seeds
will encounter soil microbes during the long time period (often > 6 months;
Baskin and Baskin 2001) prior to germination. Rarely have pathogenic factors
such as microbes been considered seed predators of myrmecochore seeds; this
oversight is curious given their ubiquity as seed predators in a number of
systems (Bell et al. 2006; Mangan et al. 2010; Tewksbury et al. 2008). It (see
Fricke et al. 2014) has been suggested that gastropods may play an even more
important role in myrmecochory than ants (Turke et al. 2012).
15
Little is known about what occurs to ant-dispersed seeds within ant nests,
which has led to ant nests being referred to as “black boxes” (Servigne and
Detrain 2010). Escape from predation may have more to do with ant seedhandling than previously thought. Numerous ant species have a paired set of
glands called the metapleural glands, which have been shown to store a variety
of antimicrobial compounds (Brown 1968; Beattie et al.1986; Hölldobler and
Wilson 1990; Veal et al. 1992; Mackintosh et al. 1995; Nascimento et al. 1996;
Bot et al. 2002). While these glands are constantly secreting these antimicrobial
compounds, ants have been shown to actively spread these secretions
especially when there is a threat to fungal infection (Fernández-Marin 2006) and
in instances of general nest and brood cleaning (Tranter et al. 2014). This being
said, it is reasonable to question whether secretions from metapleural or venom
glands poses any effect on the likelihood of handled seeds gaining resistance to
microbial pathogens. If exposed to these secretions, seeds may have more of a
chance to resists the many soil pathogens that may result in decreased livelihood
of the seed or death altogether.
Benefits of Myrmecochory Revisited
Despite seed burial being ephemeral, elaiosome removal being inconclusive and
not adequately tested, and seeds being subject to predators besides vertebrates,
the importance of ants in myrmecochory may still be unequivocal. To better
address the potential positive role of ants in myrmecochory, a shift in approaches
is necessary (Fig. 2).
16
!"
!"
!"
!"
Figure 2. The less commonly understood and complex process of myrmecochory where
seeds may be subjected to granivory and microbial/fungal predation, cleaned by ants
through metapleural secretions and abandoned within the nest or redispersed
elsewhere.
Elaiosomes provide a starting point for a new viewpoint of myrmecochory,
and specifically the benefits ants provide myrmecochorous plants. While the
chemical composition of elaiosome is known to be involved in attracting foraging
ants to diaspores and enhance dispersal to ant nests, it may attract microbial
predators as well. Appendages such as arils, which technically are a type of
elaiosome (Lengyel et al. 2010), and fruits in general, are known to harbor
microbes (see Oliveira et al. 1995) that may well inflict considerable mortality to
17
seeds (Augspurger 1990). Indeed, fungus-culturing ants that remove fruit pulp
and arils from fallen fruits have been shown to significantly increase seed
germination probabilities (Leal and Oliveira 1998), presumably by deterring
fungal infection. Whether elaiosomes of myrmecochorous plants harbor microbes
harmful or beneficial to the seeds they are attached to is unknown. Hence, the
need to have elaiosomes quickly removed (e.g. consumed by larvae in nests) is
the first test of ants’ important roles in myrmecochory.
The framework to test the importance of elaiosome removal by ants, and the
importance of ant seed dispersal for plants in general, needs to be cast in a
series of steps, reflective of the pathways that seeds follow (Table 2). Once the
diaspore is brought to the nest, the elaiosome portion is consumed by developing
larvae. Historically, this act of elaiosome removal has been viewed as a critical
step for subsequent germination; yet other possibilities involving ant ‘treatment’
of seeds during this process within ant nests have been neglected. This includes
possible seed “cleaning” in cases where workers secrete antimicrobial
compounds in nests (and in seed-dispersing ant cases, onto seeds) to protect
the brood from fungal parasites (Tranter et al. 2014). The benefits of such
“double duty” have not been adequately tested, and present the next series of
tests of ants’ important roles in myrmecochory.
18
Table 2. Areas to further research to better understand myrmecochory.
Questions in need of future addressing in terms
of plant benefits in myrmecochorous systems
What are the chances that pathogens will kill the seed if left behind by the ant?
Are the ants providing anti-pathogenic properties to the seeds when handling
diaspores?
Do plants benefit more from being left in the nest or moved outside?
Are seeds being redispered in random/non-special areas or midden piles or
are they nutrient dense?
What are specific effects of elaiosome being removed by ants rather than
experimentally removed by researchers?
The relevance of elaiosome removal could well differ for seeds that remain in
nests versus those that are redispersed to middens are random locations near
ant nests. Elaiosome-removed seeds that remain in nests are less likely to be
subject to vertebrate seed predation than those that are redispersed. As such,
consumptive removal of elaiosomes and/or any seed treatment may be
imperative for escape from microbial pathogens for seeds remaining in nests. For
those that are redispersed, elaiosome removal and/or seed treatment may be
important for escape from previously mentioned microbes as well as vertebrate
predators.
Ultimately, any seed dispersal treatment a seed-dispersing ant provides that
enhances seed survival will need to be followed by adequate seedling
establishment. As ant nests continue to be documented as ephemeral locations
for seeds, in particular for those that are redispersed (e.g. Canner et al. 2012),
19
the locations to examine for advantageous microsites needs to shift ever so
slightly to areas near ant nests, rather than ant nests themselves. In cases where
redispersal has been documented, it remains unclear if such locations are either
more nutrient-rich or relatively freer of microbial pathogens than other areas in
the systems where myrmecochores are found.
It may indeed be necessary to question myrmecochory as an ideal example
of mutualism. There are still sections of this story not yet known and it is
imperative to further delve into these questions. It is probable that this
relationship is more of an evolved dependence (Mazancourt et al. 2005), with
plants gaining more of a benefit from this relationship. By delving further into the
details of myrmecochory, we may be able to further understand the phenomenon
of coevolution. We hope that imminent knowledge gained can be applied to other
systems where effects of seed treatment by dispersers are currently being
pursued (e.g. Fricke et al. 2013).
Acknowledgements
This literature review was conducted as an undergraduate thesis for
Mariah Patton under the direction of Charles Kwit at the University of Tennessee,
Knoxville. I thank Charlie for his persistent guidance and mentorship, helping me
further to shape questions, dig deep within the literature of myrmecochory, and
greatly help with edits. I thank Chelsea for illustrations were used in figures. I
thank Lacy Chick for helping me explore research interests using ants as a study
organism. Her guidance and advice has helped me grow into a better ecologist,
20
and I cannot thank her enough. I also thank Nate Sanders for inspiring me to
pursue ecology.
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