229764430620.1.1.2284.73711source_20The diversity and ecology of ant gardens (Hymenoptera: Formicidae; Spermatophyta: Angiospermae)Mutualistic interactions between ants and plants are important features of many ecosystems, and they can be divided into three main categories: dispersal and protective mutualisms and myrmecotrophy. In both the Neotropics and the Southeastern Asian Paleotropics, ant gardens (AGs), a particular type of ant-plant interaction, are frequent. To initiate AGs, ants integrate the seeds of certain epiphyte species into the carton of their nest. The development of the plants leads to the formation of a cluster of epiphytes rooted in the carton. They have been defined as one of the most complex associations between ants and plants known because of the plurispecific, but also specialized nature of the association involving several phylogenetically-distant ant and plant species. The aim of this review is to provide a synthesis of the diversity and ecology of AGs, including the outcomes experienced by the partners in the interaction and the direct and indirect impacts ant-garden ants have on the plant and arthropod communities.2011Myrmecological NewsArticleJérôme Orivel|Céline LeroyCara M Gibson, Martha S Hunter, Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects., Article, Ecology Letters 12/2009; 13(2):223-34.|Martin Heil, D. McKey, Protective ant-plant interactions as model systems in ecological and evolutionary research, Article, Annual Review of Ecology, Evolution, and Systematics, v.34, 425-453 (2003). 01/2003;|Crisanto Gómez, Xavier Espadaler, Myrmecochorous dispersal distance: a world survey., Article, Journal of Biogeography 01/1997; 25:573-580.Myrmecological News 14 73-85 Vienna, January 2011
The diversity and ecology of ant gardens (Hymenoptera: Formicidae; Spermatophyta:
Angiospermae)
Jrme ORIVEL & Cline LEROY
Abstract
Mutualistic interactions between ants and plants are important features of many ecosystems, and they can be divided
into three main categories: dispersal and protective mutualisms and myrmecotrophy. In both the Neotropics and the
Southeastern Asian Paleotropics, ant gardens (AGs), a particular type of ant-plant interaction, are frequent. To initiate
AGs, ants integrate the seeds of certain epiphyte species into the carton of their nest. The development of the plants leads
to the formation of a cluster of epiphytes rooted in the carton. They have been defined as one of the most complex
associations between ants and plants known because of the plurispecific, but also specialized nature of the association
involving several phylogenetically-distant ant and plant species. The aim of this review is to provide a synthesis of the
diversity and ecology of AGs, including the outcomes experienced by the partners in the interaction and the direct and
indirect impacts ant-garden ants have on the plant and arthropod communities.
Key words: Ant-plant interactions, epiphytes, mutualisms, Neotropics, Paleotropics, phytotelm, parabiosis, seed dispersal,
review.
Myrmecol. News 14: 73-85 (online 26 August 2010)
ISSN 1994-4136 (print), ISSN 1997-3500 (online)
Received 23 March 2010; revision received 25 May 2010; accepted 15 June 2010
Dr. Jrme Orivel (contact author), CNRS, EDB (Laboratoire Evolution et Diversit Biologique), 118 route de Narbonne,
31062 Toulouse, France; Universit de Toulouse, EDB, 118 route de Narbonne, 31062 Toulouse, France; current address:
CNRS, UMR Ecologie des Forts de Guyane, Campus Agronomique, 97379 Kourou cedex, French Guiana, France.
E-mail: jerome.orivel@ecofog.gf
Dr. Cline Leroy, CNRS, UMR Ecologie des Forts de Guyane, Campus Agronomique, 97379 Kourou cedex, French
Guiana, France.
Introduction
Ants are ubiquitous and, in ecological terms, tremendously
successful. The major consequence of this ecological suc-
cess is the impact ants have on the other components of bio-
mass. Besides being the principal predators of arthropods
in tropical forests and even the principal herbivores in the
Neotropics, ants are also involved in a diversity of inter-
actions. Consequently, studying these interactions is of key
importance in enabling us to determine ants' impact on the
structure of ecological communities. Many of these inter-
actions are mutualistic and most of these mutualisms are
either based on the protection provided by the ants in ex-
change for food rewards and / or shelter (HEIL & MCKEY
2003, STADLER & DIXON 2008), or they are purely nutrition-
based interactions with bacteria or fungi (KANE & MUEL-
LER 2002, GIBSON & HUNTER 2010).
Ant-plant mutualisms are important components of trop-
ical communities. Their diversity, associated with a simi-
lar global pattern of interactions, makes them useful model
systems for understanding the origin and evolution of mu-
tualisms. Ants and flowering plants have a long, shared
history as the ants' diversification between 100 million
years ago (mya) and 50 mya closely tracks the rise of
Angiosperms (MOREAU & al. 2006, MOREAU 2009). The
ecological dominance of ants is notable by the mid-Eocene
(50 mya), suggesting an explosive radiation just before this
period (WILSON & HLLDOBLER 2005, MOREAU & al.
2006). Today, ant-plant mutualisms either involve ants as
dispersal agents of plant diaspores, the indirect protection of
plants thanks to the predatory ability of ants, or the feeding
on plants by ants.
Dispersal mutualisms occur in more than 3,000 plant
species bearing elaiosomes (i.e., nutritive bodies attached
to the seeds) that are dispersed by ants (BEATTIE & HUGHES
2002, GILADI 2006). The elaiosomes are consumed by the
ants and the seeds are then either rejected or kept inside the
nest (MARK & OLESEN 1996, GOMEZ & ESPADALER 1998,
WILLSON & TRAVESET 2000, WENNY 2001). Such seeds
can then be dispersed far from the parent plants into micro-
habitats suitable for their germination and growth (i.e., ant
nests), and away from predators (reviewed in GILADI 2006).
Protective ant-plant mutualisms derive from the provi-
sion of food in the form of extrafloral nectar and / or a per-
manent shelter for the ants in specialized structures by the
so-called myrmecophytic plants (HEIL & MCKEY 2003,
RICO-GRAY & OLIVEIRA 2007). Extrafloral nectaries are
present in 93 angiosperm and five fern families (BENTLEY
1977, KOPTUR 1992). In exchange for these food rewards,
the ants generally protect the plants from herbivores (OLI-
VEIRA 1997, DE LA FUENTE & MARQUIS 1999, BEATTIE &
HUGHES 2002, DIAZ-CASTELAZO & al. 2004, MODY & LIN-
SENMAIR 2004, RUDGERS & GARDENER 2004). In addition
to these interactions in which a variety of partners are in-
volved (BLTHGEN & al. 2000, APPLE & FEENER 2001,
HOSSAERT-MCKEY & al. 2001), strict and obligatory mu-
tualisms do exist. The constancy and specificity of these
associations are facilitated by the presence of domatia and,
often, such interactions are the result of co-evolutionary
specializations (HEIL & MCKEY 2003, RICO-GRAY & OLI-
VEIRA 2007). In turn, the resident ants also protect their
hosts from herbivory and / or competition, and they can
also provide them with nutrients (HEIL & MCKEY 2003).
Nutrient provisioning to their host plant by the ants,
called myrmecotrophy, has been demonstrated in several
systems (BENZING 1991, TRESEDER & al. 1995, LETOUR-
NEAU 1998, SAGERS & al. 2000, FISCHER & al. 2003). Ants
provide the plant nutrients either through the accumulation
of their waste in the domatia or by favouring the growth of
epiphytic plants in the carton of their nest. Nitrogen and
probably other nutrients are absorbed by the myrmeco-
phytes through the walls of the domatia or by protuberances
growing inside of them, and the plants can even benefit
from ant respiration by absorbing carbon dioxide (TRESE-
DER & al. 1995, FISCHER & al. 2003, SOLANO & DEJEAN
2004). In carton-growing epiphytes, the growth of the plants
is enhanced by the accumulation of the rich organic mat-
ter that the ants accumulate around the roots (LONGINO
1986, BENZING 1991, BLTHGEN & al. 2001).
Ant gardens (AGs) represent a particular type of inter-
action involving the three types of above-mentioned inter-
actions between ants and plants (i.e., protective and disper-
sal mutualisms, and myrmecotrophy). They constitute an
outstanding example of an ant-plant association, and also
probably one of the most complex (BUCKLEY 1982, KLEIN-
FELDT 1986). In this review, we summarize the diversity
and ecology of AGs and we provide a synthesis of the out-
comes experienced by the partners in the interaction and
the direct and indirect impacts AG ants have on plant and
arthropod communities.
Ant gardens
Ant gardens were first described by ULE (1901) based on
his work in the Neotropics, and, subsequently, VAN LEEU-
WEN (1929a, b) demonstrated the same type of ant-epiphyte
association in Southeastern Asia. They can be roughly de-
fined as aggregates of epiphytes assembled by ants. More
specifically, they refer to the particular mutualistic interac-
tions between plants and ants in which ants integrate the
seeds of certain epiphyte species into the carton of their
arboreal nests. These epiphytes subsequently germinate and
develop on this rich substrate to form hanging structures on
the branches of host trees (Fig. 1).
The complexity of these interactions comes from the
plurispecific, but also specialized nature of the association.
Indeed, several species of phylogenetically-distant ants can
be associated with several, also phylogenetically-distant,
epiphyte species, but none of them is found outside of AGs.
Moreover, AG epiphytes lack obvious morphological adap-
tations, such as domatia (but see KAUFMANN & MASCH-
WITZ 2006, about the occurrence of ant-house epiphytes in
AGs). Such an "apparent" absence of morphological adap-
tation, despite the specificity of their interactions with ants,
might also have contributed to viewing AGs as complex
ystems. Finally, the commonness of one of the most intri-
s
guing interspecific associations between ant species within
AGs, called parabiosis, contributes to the overall intricacy
of AGs (FOREL 1898, MANN 1912, WEBER 1943).
Ant and plant diversities
Only a few ant species are known for their ability to initiate
AGs. True AG ant species are defined as species sharing
the following two behavioral characteristics: (I) the capa-
city to build an arboreal carton nest rich in humus, and (II)
a retrieval behavior concerning the seeds of epiphytic plants
that they retrieve to their nest and incorporate into its
walls (CORBARA & al. 1999). Data in the literature are, how-
ever, lacking for many species recorded in AGs, so that
such a definition applies to only a few ant species. Conse-
quently, we will consider here that the definition of true AG
ants can be also extended to species that have been re-
corded only in AGs and nowhere else. These AG ants be-
long to four ant subfamilies (i.e., the Dolichoderinae, For-
micinae, Myrmicinae and Ponerinae) both in the Paleo- and
in the Neotropics (see Tab. 1). In Southeastern Asia, the
most abundant ant species is Crematogaster sp. with a pre-
valence of more than 80% (KAUFMANN & al. 2001, KAUF-
MANN & MASCHWITZ 2006), whereas in tropical America
the parabioses between Camponotus femoratus (FABRICIUS,
1804) and Crematogaster levior LONGINO, 2003 and the
AGs inhabited by Pachycondyla goeldii (FOREL, 1912) are
by far the most frequent (DAVIDSON 1988, CORBARA & DE-
JEAN 1996, MARINI-FILHO 1999, DEJEAN & al. 2000).
A wide diversity of ant species can, however, inhabit
AGs (KLEINFELDT 1978, 1986, DAVIDSON 1988, KAUF-
MANN & MASCHWITZ 2006). Indeed, even if true AG ants
and plants are restricted to such associations, the epiphytes
are, nevertheless, able to survive after the death of the ant
colony that initiated the AG, and so can be colonized by
opportunistic arboreal ant species. Moreover, because of the
scarcity of suitable nesting sites in the arboreal environ-
ment, AGs represent appealing nesting structures for a var-
iety of ant species and even for other insects (see COR-
BARA & DEJEAN 1998). During the expansion of their ter-
ritories, dominant arboreal ant species are frequent secon-
dary residents (DEJEAN & al. 1997, CORBARA & al. 1999),
and several opportunistic species can also be found in AGs
(DAVIDSON 1988, DEJEAN & al. 2000). Moreover, the sec-
ondary colonization of AGs by other ant species is facili-
tated when local ecological conditions change and drive a
decrease in the population of AG ants (DEJEAN & al. 2000).
Of the 15,500 epiphyte species known from the Neo-
tropics, some are regularly found in AGs. A review of the
literature on Neotropical AGs resulted in the recording of a
total of 53 epiphyte species from 12 families. True AG epi-
phytes represent only a subset of these species, and they
are defined as plant species specifically incorporated into
the nest at the seed stage by the ants (Tab. 2). As mentioned
above for true AG ant species, data are also lacking for many
epiphyte species, so that here we will consider several spe-
cies as true AG epiphytes on the basis of their only having
been observed in AGs. Because of the nutrient-rich compo-
sition of the carton nest and the probable absence of both
pruning behavior by the ants and allelopathy by the plants,
a variety of epiphytes can live on AGs if their seeds reach
the carton nest. This is the case, for example, for the few
Orchidaceae and Polypodiaceae species that are regularly
found in AGs and whose seeds or spores are tiny and wind-
74
Fig. 1: The developmental stages of ant gardens. (A) Founding queens first build a carton nest from vegetal fibres into which
they incorporate epiphyte seeds (arrows) example from Pachycondyla goeldii; (B) Young ant garden inhabited by Cam-
ponotus femoratus and Crematogaster levior with numerous seedlings growing on the carton nest; (C) Mature Neotropical
ant garden inhabited by Ca. femoratus and Cr. levior with the epiphytes Codonanthe calcarata and Aechmea mertensii;
(D) Mature Southeastern Asian ant garden inhabited by the ant Camponotus sp. with the epiphyte Hoya elliptica.
dispersed (DAVIDSON 1988, DEJEAN & al. 2000, BLTH-
GEN & al. 2001). A limited number of unrelated, true AG
epiphytes can be found in AGs in a single location. Vari-
ations across locations (over a large geographical scale) af-
fect the floristic composition of the AGs in terms of changes
in species rather than through changes at a higher taxono-
mic level. Consequently, at the family and even the genus
level, the floristic composition of Neotropical AGs is very
similar with four families and six genera representing the
ast majority of AG epiphytes (Bromeliaceae: Aechmea,
v
Streptocalyx; Areaceae: Anthurium, Philodendron; Gesne-
riaceae: Codonanthe; Piperaceae: Peperomia) (KLEINFELDT
1978, DAVIDSON 1988, MARINI-FILHO 1999, ORIVEL & DE-
JEAN 1999).
By contrast, information on AG associations from the
Paleotropics remains scarce (KAUFMANN & al. 2001, KLEIJN
& VAN DONKELAAR 2001, KAUFMANN & MASCHWITZ
2006). While AGs are locally abundant and widespread in
the Neotropics, the so-called ant-house epiphytes (Hydno-
phytum sp. and Myrmecodia tuberosa JACQ., both Rubi-
75
Tab. 1: True ant-garden ant species (i.e., species able to initiate ant gardens or restricted to AGs) in both the Paleo- and the
Neotropics.
References: a BENSON (1985), b CORBARA & DEJEAN (1996), c DAVIDSON (1988), d DEJEAN & al. (2000), e KAUFMANN
& al. (2001), f KAUFMANN (2002), g KAUFMANN & MASCHWITZ (2006), h KLEINFELDT (1978), i KLEINFELDT (1986), j
LONGINO (1999), k LONGINO (2003c), l LONGINO (2003a), m LONGINO (2003b), n MANN (1912), o MARINI FILHO (1999),
p ORIVEL & al. (1997), q ORIVEL & al. (1998), r ORIVEL & al. (1999), s SCHMIT-NEUERBURG & BLTHGEN (2007), t WE-
BER (1943), u WHEELER (1921), v WILSON (2003), w YOUNGSTEADT & al. (2009).
1 The number in parentheses represents the number of species of the genus recorded as specialists of ant gardens (see
KAUFMANN 2002, KAUFMANN & MASCHWITZ 2006).
2 Crematogaster limata, Cr. carinata and Cr. levior belong to the Cr. limata complex (see LONGINO 2003c), and are dif-
ficult to differentiate at the morphological level (especially Cr. carinata and Cr. levior). Moreover, the species have often
been recorded as Cr. limata and / or Cr. limata parabiotica in the literature, so that these three species are listed together
with the same references. It should be noted, however, that Cr. levior is a specialized parabiotic associate of Camponotus
femoratus, while Cr. carinata and Cr. limata are parabiotic associates of Odontomachus panamensis and Dolichoderus
debilis or D. inermis (although not in AGs in these two latter cases) or O. mayi, respectively.
3 References that explicitly support the role of the ant species as an AG initiator.
Subfamily Species Geographic area References
Dolichoderinae
Philidris spp. (6) 1
Peninsular Malaysia e, f 3, g
Formicinae
Camponotus spp. (4) 1
Peninsular Malaysia e, f 3, g
Myrmicinae
Crematogaster spp. (6) 1
Peninsular Malaysia e 3, f 3, g
Pheidole spp. (2) 1
Peninsular Malaysia e, f 3, g
Ponerinae
Diacamma sp. (1) 1
Peninsular Malaysia e, f 3, g
Dolichoderinae
Azteca trailii EMERY, 1893, Azteca sp. Brazil, Peru c 3, i, o 3, s
Formicinae
Camponotus femoratus (FABRICIUS, 1804) Brazil, French Guiana, Peru, Venezuela c 3, d, i, o, r 3, s, t, u, w 3
Myrmicinae
Crematogaster limata F. SMITH, 1858 2
Crematogaster levior LONGINO, 2003 2
Crematogaster carinata MAYR, 1862 2
Brazil, French Guiana, Peru, Venezuela c, d, i, k, o, s, t, u, w
Crematogaster longispina EMERY, 1890
Costa Rica d, h 3, i, k
Crematogaster jardinero LONGINO, 2003 Costa Rica l
Pheidole violacea WILSON, 2003 Costa Rica m, v
Ponerinae
Odontomachus mayi MANN, 1912 Brazil, French Guiana d, n, o, q 3
Odontomachus panamensis FOREL, 1899 Costa-Rica, Panama j, k
Pachycondyla goeldii (FOREL, 1912) Brazil, French Guiana a, b, d, p, q 3, r 3
________________________________________________________________________________________________
Tab. 2: True ant-garden epiphyte species (i.e., species that are specifically incorporated into the nest
at the seed stage by the ants and / or observed only in AGs) in both the Paleo- and the Neotropics.
References: a BLTHGEN & al. (2001), b CATLING (1995), c CEDENO & al. (1999), d CORBARA & DEJEAN (1996), e DA-
VIDSON (1988), f DAVIDSON & EPSTEIN (1989), g DEJEAN & al. (2000), h KAUFMANN & al. (2001), i KAUFMANN
(2002), j KAUFMANN & MASCHWITZ (2006), k KLEIJN & VAN DONKELAAR (2001), l KLEINFELDT (1978), m LONGINO
(1999), n LONGINO (2003b), o NIEDER & al. (2000), p ORIVEL & DEJEAN (1999), q SCHMIT-NEUERBURG & BLTHGEN
(2007), r YOUNGSTEADT & al. (2009).
1 Some of the Dischidia species cited in KAUFMANN (2002) are not included here because they can be found outside of
AGs (see WEIR & KIEW 1986).
2 These species have been rarely observed in AGs, and no data are available on the incorporation of their seeds into the
carton nest by the ants. Although data are also lacking about their occurrence outside of AGs, these species are still
included as true AG species.
3 References that explicitly support the dispersal of the seeds by AG ants.
76
Family Species Geographic area References
Asclepiadaceae1
Gesneriaceae
Melastomataceae
Moraceae
Urticaceae
Zingiberaceae
Araceae
Bromeliaceae
Cactaceae
Gesneriaceae
Moraceae
Orchidaceae
Piperaceae
Solanaceae
Dischidia acutifolia MAINGAY
Dischidia albida GRIFF.
Dischidia bengalensis COLEBR.
Dischidia fruticulosa RIDL.
Dischidia hirsuta DECNE.
Dischidia imbricate STEUD.
Dischidia longepedunculata RIDL.
Dischidia punctata DECNE.
Dischidia subalata WARB.
Dischidia sp.
Hoya brevialata KLEIJN & DONKELAAR
Hoya elliptica HOOK. f.
Hoya lacunosa BLUME
Hoya micrantha HOOKER
Hoya mitrata KERR
Hoya multiflora BLUME
Hoya parvifolia SCHLTR.
Hoya picta HORT.
Hoya pubera BLUME
Hoya spp.
Aeschynanthus albidus STEUD.
Aeschynanthus fecundus P. WOODS
Aeschynanthus myrmecophilus P. WOODS
Aeschynanthus spp.
Medinilla crassifolia BLUME
Pachycentria constricta BLUME
Pachycentria glauca TRIANA
Ficus sp.
Poikilospermum cordifolium MERR.
Poikilospermum microstachys MERR.
Hedychium longicornutum GRIFF. ex BAKER Peninsular Malaysia
Anthurium gracile LINDL.
Anthurium ernestii ENGL.
Philodendron deflexum POEPP.
Aechmea mertensii SCHULT. f.
Aechmea tillandsiodes BAKER
Neoregelia sp.
Streptocalyx longifolius (RUDGE) BAKER
Epiphyllum phyllanthus (L.)
Codonanthe calcarata HANST.
Codonanthe crassifolia (FOCKE)
Codonanthe macradenia DONN.SM.
Codonanthe uleana FRITSCH
Columnea linearis OERST. 2
Columnea verecunda C.V. MORTON 2
Ficus paraensis MIQ.
Coryanthes speciosa (HOOK.) 2
Epidendrum imatophyllum LINDL 2
Peperomia macrostachya A. DIETR.
Markea ulei (DAMMER)
Markea formicarum (DAMMER)2
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Sulawesi
Peninsular Malaysia
Peninsular Malaysia, Sulawesi
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Sulawesi
Sulawesi
Sulawesi
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
Peninsular Malaysia
h 3, i 3
h, i 3, j
h, i 3
i 3
h, i 3
h, i 3
i 3
h, i 3, j
i 3
i 3
k
h, i 3, j
h, i 3, j, k
i 3
i 3, j
i 3, j
k
k
k
i 3
h 3, i, j
h 3, i
i 3
i 3
i 3
i 3, j, k
i 3, j, k
i 3
i 3, j, k
i 3, j, k
i 3
a, c d, e 3, g, o, p 3, q
f
a, c, e 3, g, o, q
d, g, p 3,
a, b, q
e 3, f
e 3, f, g,
e 3, f, o, q
a, c, g, o, p 3, q
c, d, l 3,
b
e 3, f
m
n
e 3, f, g
b
b
e 3, f, g, p 3, r 3
e 3, f
g, p
Brazil, French Guiana, Peru, Venezuela
Peru
French Guiana, Peru, Venezuela
Brazil, French Guiana
Belize, Venezuela
Peru
Brazil, French Guiana, Peru
Brazil, Peru, Venezuela
Brazil, French Guiana, Venezuela
Costa Rica, French Guiana
Belize
Brazil, Peru
Costa Rica
Costa Rica
Brazil, French Guiana, Peru
Belize
Belize
Brazil, French Guiana, Peru, Venezuela
Peru
Brazil, French Guiana
77330913909734481909703933259339,2404614785