Ant Gardens

Holldobler and Wilson (1990) provide an introduction to ant gardens.

Perhaps the most complex mutualism between plants and ants is the ant garden, which is an aggregate of epiphytes assembled by ants. The ants bring the seeds of the epiphytes into their carton nests. As the plants grow, nourished by the carton and detritus brought by the ants, their roots become part of the framework of the nests. The ants also feed on the fruit pulp, the elaiosomes (food bodies) of the seeds, and the secretions of the extrafloral nectaries.

It is a curious fact that while epiphytic myrmecophytes are generally diverse and abundant throughout the tropics, they form ant gardens principally in Central and South America, with some examples having been recently found in tropical Asia by Diane Davidson (personal communication). First reported by Ule (1902), the gardens are typically round or ellipsoidal, and they range from 6 to more than 60 centimeters in greatest diameter; a typical example is shown in Figure 14-9. The ants construct irregular nest chambers divided by carton walls among their roots (Weber, 1943; Kleinfeldt, 1978, 1986). Specialized garden plants representing no fewer than 16 genera have been identified to the present writing (Buckley, 1982b; Davidson, 1988). At one locality in the Manu National Park alone, Davidson identified ten such specialists belonging to the following seven families: Araceae (Anthurium, 2 species; Philodendron), Bromeliaceae (Neoregelia, Streptocalyx), Cactaceae (Epiphyllum), Gesneriaceae (Codonanthe), Moraceae (Ficus), Piperaceae (Peperomia), and Solanaceae (Markea). Peperomia macrostachya was by far the dominant species, occurring in 76 percent of the gardens. It was followed by Anthurium gracile and Ficus paraensis, with 29 and 23 percent occurrence rates respectively. Seven other genera in six families were represented among the unspecialized, adventitious species in the gardens. In general, the dominant plants of gardens in South and Central America are five species of Codonanthe, followed in abundance by Aechmea mertensii and Anthurium gracile (Kleinfeldt, 1986).

The dominant ants in the ant gardens across Central and South America generally are members of the genera Crematogaster, Solenopsis, Azteca, Dolichoderus, and Camponotus, with Anochetus and Odontomachus occurring much less commonly (Kleinfeldt, 1986). The overwhelmingly dominant species in the Peruvian Amazon are Crematogaster parabiotica (broadly defined) and Camponotus femoratus. These forms appear to be the most abundant ant species in the forest canopy generally (Wilson, 1987a; Davidson, 1988). Other, possibly adventitious ant-garden species belong to the genera Odontomachus, Anochetus, Monomorium, and Solenopsis (Mann, 1912a; Wheeler, 1921a; Macedo and Prance, 1978). Dolichoderus debilis is commonly found in the same garden with one sibling species in the Crematogaster parabiotica complex and Camponotus femoratus with another. The species pairs nest in separate but contiguous chambers within the same garden, the condition originally called parabiosis by Forel (1898). The Dolichoderus at least follow the Crematogaster out along their odor trails and aggressively displace them at food sites (Swain, 1980).

The tightness of the associations suggests that the plants and ants in the gardens have coevolved, but surprisingly little experimental evidence has been adduced to test this supposition. Kleinfeldt (1978) showed that Codonanthe crassifolia, one of the specialized garden plants, grows more quickly when in association with Crematogaster longispina than when alone. It is probable that the carton of ant nests provides a physical substrate laced with nutrients preadapting them for epiphytic growth. Longino (1986) observed that Crematogaster longispina occurs throughout the Atlantic rain forest of Costa Rica, often as a dominant element of the understory fauna. Its large, diffuse colonies manufacture loose, coarse-fibered carton to build large numbers of nests, shelters for scale insects, and galleries that connect all of these components. The bulk of the carton is placed under and around the roots and stems of aroids and gesneriads running up and down the tree trunks. Whenever new carton is laid down, there is usually a flush of newly sprouted epiphytes in the walls. As Longino points out, it is but a short further step in evolution to nurture an obligate garden species such as Codonanthe crassifolia.

How do individual symbiotic gardens get planted in the first place? Ule (1905, 1906) observed that ants retrieved the seeds of the epiphytes, and he proposed that they establish the gardens within the confines of their own nests to start the symbiosis. Wheeler (1921a) argued that the gardens might be autonomous instead, with the ants colonizing the plants later. The evidence has consistently favored Ule. Later authors, including Madison (1979), Kleinfeldt (1978), and Davidson (1988), have repeatedly observed that the symbiont ants are strongly attracted to the fruits and seeds of the garden epiphytes. After the workers consume the adhering fruit pulp and elaiosomes, they place the seeds near their own brood piles. Workers of Camponotus femoratus have been observed to build epiphytic gardens over the carton chambers of Crematogaster parabiotica in this manner. Davidson notes that the myrmecophyte seeds remain attractive even after they pass through the digestive tracts of frugivorous bats. She suggests that they contain pheromone-mimicking substances rather than just food material. Seidel (1988) has identified several of the compounds as 6-methyl-methylsalicylate, benzothiazole, and a few phenyl derivatives and monoterpenes. Many precedents exist in the behavior of myrmecophilous arthropods that gain entrance to their hosts' nests by pheromonal mimicry (see The Ants, Chapter 13). It may also be significant that at least some ant species not associated with gardens are repelled by the seeds. Finally, Davidson (personal communication) tested Wheeler's competing hypothesis by setting out garden epiphytes in sites where they could be found by the symbiotic ants. None was colonized.

To summarize our existing knowledge of the ant gardens, the epiphytes restricted to the gardens appear to be truly adapted to this symbiosis. Their seeds are transported to favorable sites by the ants in response to what appear to be specialized attractive substances, and the subsequent growth of at least some of the species is enhanced by the presence of the ants. For their part, the ants are not so clearly adapted to benefit from the ant gardens. They feed on the extrafloral nectar, fruit pulp, and elaiosomes supplied by the plants. But this is not a restrictive diet, and in fact all of the garden ant species forage away from the gardens. The best evidence that some ants have coevolved with the plants is that the dominant garden species of South America, Dolichoderus debilis, Camponotus femoratus, and the two Crematogaster in the parabiotica group, usually if not invariably nest in the gardens. They are behaviorally specialized to some extent for bringing the seeds of the epiphytes to their carton nests, in effect planting the gardens.

Not All Ant-Garden Inhabitants Are Ant-Garden Ants
Orivel & Leroy (2011) note that a wide diversity of ant species can inhabit ant gardens (KLEINFELDT 1978, 1986, DAVIDSON 1988, Kaufmann & Maschwitz 2006). Indeed, even if true ant-garden 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 ant garden, and so can be colonized by opportunistic arboreal ant species. Moreover, because of the scarcity of suitable nesting sites in the arboreal environment, AGs represent appealing nesting structures for a variety of ant species and even for other insects (see CORBARA & Dejean 1998). During the expansion of their territories, dominant arboreal ant species are frequent secondary residents (Dejean & al. 1997, CORBARA & al. 1999), and several opportunistic species can also be found in ant gardens (DAVIDSON 1988, Dejean & al. 2000). Moreover, the secondary colonization of ant gardens by other ant species is facilitated when local ecological conditions change and drive a decrease in the population of AG ants (Dejean & al. 2000).

Plant Cultivation
Outside humans, true agriculture was previously thought to be restricted to social insects farming fungus. However, obligate farming of plants by ants was recently discovered in Fiji. However Campbell et al. (2022), re-examination plant cultivation by ants and identified three main types, and found that these interactions evolved primarily for shelter rather than food. They found that plant cultivation evolved at least 65 times independently for crops (~200 plant species), and 15 times in ant lineages (~37 ant taxa), and occurs in the Neotropics, Asia/Australasia and Fiji.

True Agriculture
"True agriculture" has been defined as having four key characteristics:
 * 1) habitual planting
 * 2) cultivation
 * 3) harvest
 * 4) obligate dependency on the crop for food

This type of agriculture has only arisen in humans and three groups of social or subsocial insects, namely ants, termites, and beetles, all of which farm fungi [8].

However, an additional type of obligate agriculture has recently been discovered in Fiji. The dolichoderine ant Philidris nagasau was found to cultivate six species of the epiphytic plant genus Squamellaria. This is the only known example of insects farming plants and the first example of insect agriculture not involving fungal crops.

Outside this obligate plant farming by ants, there is also the cultivation of epiphytic plants by ants. These so-called ‘ant-gardens’ were discovered over 100 years ago [10]. However, it is unclear how these fit within a broader framework of farming mutualisms, and whether they represent, or are ecologically close to, true agricultural systems.

Ant Agriculture
Campbell et al. (2022) examined all forms of plant cultivation by ants and argue that:
 * 1) plant cultivation by ants involves a range of dependences, with partnerships ranging from loose facultative cultivation systems to tight obligate agricultures
 * 2) several systems likely represent true agriculture systems, but quantifications are not possible yet as most of these symbioses are understudied
 * 3) because plant cultivation partnerships range in their level of specialisation and dependence and involve many independent lineages of plants and ants, they are powerful model systems to study the ecological and evolutionary consequences of agriculture
 * 4) a more inclusive ecoevolutionary framework focused on evolutionary stages is useful for understanding the evolution of farming behaviour across the tree of life

They identified three types of plant cultivation mutualisms, which occur in three distinct geographical areas:
 * 1) Neotropical ant-gardens
 * 2) SE Asian and Australasian ant-gardens
 * 3) Fijian agriculture

All three plant cultivation systems have the same core function: nutrient-stressed epiphytes receive nutritional resources in return for providing ants with nesting space. However, both nesting space and nutrients are provided in very different ways across the three types of cultivation mutualisms. Nutrients are provided to plants by being dispersed into a nutrient-rich carton nest, constructed by ant-garden ants (Neotropical and SE Asian ant-gardens) or by being actively fertilised with ant faeces (Fijian agriculture). The roots of planted epiphytes provide a scaffolding which increases the stabilisation of the carton nests – which allows for the construction of larger nests (Neotropical and SE Asian ant-gardens). In addition to the structural support from the roots, epiphytes also remove excess moisture via transpiration [16]. Additionally, nest space is provided with domatia (SE Asian ant-gardens and Fijian agriculture).

Neotropical Ant-Gardens
Ant-gardens were first described in 1901 in Brazil by Ule who reported ants as being precise and active constructors of ant-gardens [10]. Ule posited that foundress queens first prepare their carton nests, and plant epiphyte seeds. However, this was challenged by Wheeler [17] and Weber [18] who both argued that young queens colonised the roots of already established epiphytes. Ule’s hypothesis has subsequently been supported both by the presence of volatile compounds in ant-garden epiphyte seeds that exclusively attract ant-gardens ants in cafeteria experiments [19–22] and direct observations of ants collecting and planting seeds into their nests [21,23,24], fulfilling the first of the criteria for true agriculture set out by Mueller et al. [8], namely habitual planting of the crop.

Southeast Asian and Australasian Ant-Gardens
While seed planting by ants was suspected in Central Java by Leeuwen in 1913 [33], it was previously believed that ant-gardens do not occur in Southeast Asia or Australasia – their presence was only confirmed more recently [34]. Similar to Neotropical ant-gardens, Southeast Asian and Australasian ant-gardens are founded by queens actively collecting and planting seeds into nutrient-rich carton nests [34], fulfilling the two first criteria for a true agriculture. Less than half of Southeast Asian and Australasian ant-garden epiphytes offer food rewards (figure 2C, Supplementary dataset 1 in the supplemental information online), meaning that the third criterion – harvest of food rewards – is only sometimes met. The fourth criterion – obligate dependence – is also unclear; while Southeast Asian ant-garden ants have been described as obligate, there is inconsistency in how the term ‘obligate’ has been used, and further work should focus on better quantifying dependence in these systems (Box 1)

Fijian Agriculture
The first known system that can be defined as true plant agriculture by a non-human animal was discovered in Fiji in 2016 [9]. In this system, Philidris nagasau (Dolichoderinae) obligately farms epiphytic Squamellaria plants (Rubiaceae). Philidris nagasau fulfils all four of the criteria for true agriculture. First, P. nagasau habitually collects and plants Squamellaria seeds under tree bark. Second, it actively fertilises Squamellaria plants throughout their entire lifetime [9,39] as well as protects them from herbivory and selects sites highly sun-exposed to optimise crop productivity [40]. Third, it harvests food rewards in the form of post-anthetic nectar rewards [37], but it does not obligately depend on crop-produced food, as workers can hunt insects when needed [9,37]. Fourth, the ant farmer, however, obligately depends on Squamellaria for nesting space due to an evolutionary loss of the ability to construct its own carton nests [39].

It's About Shelter As Well As Food
Campbell et al. (2022) found that less than half of the epiphyte species cultivated by ants provide food rewards (figure 2C), which strongly suggests that plant cultivation by ants is driven by an incentive for shelter rather than food. In contrast, structural support is ubiquitous. This is true across the gradient of specialisation and dependence of these partnerships. A key illustration of this occurs in one of the six obligately farmed Fijian Squamellaria species (Squamellaria grayi), which has secondarily lost food rewards, yet is still cultivated in the same way by P. nagasau farming ants [37].

Thus, in these systems farming is for shelter and is likely being driven by the limitation of nesting space in tropical forest canopies, rather than food. This forces us to reconsider our definition of agriculture to include the dependence on shelter rather than exclusively on food, and may in turn help us to decipher the evolutionary steps in the origin of agriculture. These farming systems have an unrivalled level of evolutionary replication, and they also vary greatly in the level of dependence and specialisation (Box 1) of both crop and farmers. This offers unique opportunities to study the ecology and evolution of agriculture, using a large cross-species comparative phylogenetic framework and field studies (Box 2). Despite the great promise of plant cultivation mutualisms as tools to study agriculture, many aspects of their biology remain unknown.

Ant-Gardening Ants
Genera known to have species which form ant gardens, but where the species identifications are unknown.

Species known to form ant gardens.

Recent Studies

 * Chomicki, G. and S. S. Renner. 2019. Farming by ants remodels nutrient uptake in epiphytes. New Phytologist. 223:2011-2023. doi:10.1111/nph.15855

True agriculture - defined by habitual planting, cultivation, harvesting and dependence of a farmer on a crop - is known from fungi farmed by ants, termites or beetles, and plants farmed by humans or ants. Because farmers supply their crops with nutrients, they have the potential to modify crop nutrition over evolutionary time. Here we test this hypothesis in ant/plant farming symbioses. We used field experiments, phylogenetic-comparative analyses and computed-tomography scanning to investigate how the evolution of farming by ants has impacted the nutrition of locally coexisting species in the epiphytic genus Squamellaria (Rubiaceae). Using isotope-labelled mineral and organic nitrogen, we show that specialised ants actively and exclusively fertilise hyperabsorptive warts on the inner walls of plant-formed structures (domatia) where they nest, sharply contrasting with nitrogen provisioning by ants in nonfarming generalist symbioses. Similar hyperabsorptive warts have evolved repeatedly in lineages colonised by farming ants. Our study supports the idea that millions of years of ant agriculture have remodelled plant physiology, shifting from ant-derived nutrients as by-products to active and targeted fertilisation on hyperabsorptive sites. The increased efficiency of ant-derived nutrient provisioning appears to stem from a combination of farming ant behaviour and plant 'crop' traits.


 * Vergara-Torres, C. A., A. M. Corona-Lopez, C. Diaz-Castelazo, V. H. Toledo-Hernandez, and A. Flores-Palacios. 2018. Effect of seed removal by ants on the host-epiphyte associations in a tropical dry forest of central Mexico. Aob Plants. 10:11. doi:10.1093/aobpla/ply056

Seed depredation is recognized as a determining factor in plant community structure and composition. Ants are primary consumers of seeds influencing abundance of epiphytes on trees. This study was conducted in two subunits of a tropical dry forest established on different soil substrates in San Andres de la Cal, Teportlan, in Morelos, Mexico, and experimentally tested whether seed removal activity is higher in tree species with smaller epiphyte loads compared to those with greater epiphyte loads. Five trees were selected at random from six species of trees with high (preferred hosts) or low (limiting hosts) epiphyte loads. Seed removal differed among hosts and different soil substrates in the forest. On relating seed removal to the abundance of arboreal ants, the most consistent pattern was that lower seed removal was related to lower ant abundance, while high seed removal was associated with intermediate to high ant abundance. Epiphyte seed removal by ants influences epiphyte abundance and can contribute considerably to a failure to establish, since it diminishes the quantity of seeds available for germination and establishment.


 * Leal, L. C., C. C. Jakovac, P. E. D. Bobrowiec, J. L. C. Camargo, and P. E. C. Peixoto. 2017. The Role of Parabiotic Ants and Environment on Epiphyte Composition and Protection in Ant Gardens. Sociobiology. 64:276-283. doi:10.13102/sociobiology.v64i3.1219

Ant gardens are formed mutualistic associations between epiphyte plants and ant species in Asian and Neotropical rainforests (Hölldobler & Wilson, 1990). Ant gardens are ant nests built on the branches of trees and on which aggregates of epiphyte species grow (Ule, 1901). The nest can hold one or, more frequently, more than one ant species and several phylogenetically distant epiphyte plant species (Orivel & Leroy, 2011). When more than one ant species occurs in the same nest, they show a parabiotic behavior, in which the ants live in close association sharing foraging trials but do not exhibit obvious parasitic or exploitative interactions (Davidson, 1988; Forel, 1898; Vantaux & Leroy, 2007; Orivel & Leroy, 2011, but see Menzel et al., 2015).

Seeds from most ant gardens epiphytes are dispersed by the associated ants, which incorporate these seeds into carton nest continuously over the lifespan of the nest (Orivel & Leroy, 2011). Although seeds from ant garden epiphytes commonly bear aril or elaiosome, seed selection by ants seem not determined by the quantity or quality of such appendages as patterns of seeds selection by ant gardens ants remains the same after the removal of such seed structures (Orivel & Dejean, 1999). In fact, it seems that ant garden ant species are attracted by a set of specific volatile compounds released by the seed coat of some of epiphyte species commonly found on ant gardens (Youngstead et al., 2008). After germination, ants of at least one species protect plants against herbivores by patrolling on leaves (Vantaux et al., 2007), while the roots and stems of epiphytes increase the stability and moisture of ant nests (Yu, 1994). Some epiphytes also provide feeding resources for ants through extrafloral nectaries (EFN), oil glands and fruits (Kleinfeldt, 1978; Hölldobler & Wilson, 1990). Although previous studies has been able to identify the general benefits for both interacting sides (see Orivel & Leroy, and references therein), it has been very hard to identify the determinants of plant and ant species composition in ant gardens, and also the roles played by different partner species in this multispecific interaction.


 * Weissflog A, Kaufmann E and Ulrich Maschwitz. 2017. Ant gardens of Camponotus (Myrmotarsus) irritabilis (Hymenoptera: Formicidae: Formicinae) and Hoya elliptica (Apocynaceae) in Southeast Asia. Asian Myrmecology 9: e009001:1-16. doi:10.20362/am.009001

A large majority of vascular epiphytes in lowland forests (except for ferns and orchids) are totally dependent on ants for their establishment and proliferation (Kaufmann & Maschwitz 2006). Generally, the establishment of ant gardens follows the same behavioral patterns in all ant garden systems that have already been described by Ule (1901): Ants construct small carton nests, into which they then retrieve seeds of their epiphyte partners. However, details on ontogenetic development of ant gardens, specificity of ant and epiphyte partners, colony structure and ants’ behavior vary greatly depending on the involved species (e.g. Belin-Depoux et al. 1987, Davidson & Epstein 1989; Orivel et al. 1997, Corbara & Dejean 1996, Cedeño et al. 1999, Orivel & Leroy 2011).

As a rule, ant garden associations are beneficial for ant and epiphyte partners. Ants provide reliable short distance seed dispersal, and a highly nutritional growth substrate with good water storing capacity. They prevent water loss of the root substrate and possibly protect the plants from herbivores (e.g. Longino 1986, Davidson 1988, Kleinfeldt 1978, 1986, Schmidt-Neuerburg & Blüthgen 2007). In addition to rain water the garden is provided with honeydew from trophobionts housed within the nest (Maschwitz et al. 2010). The epiphytes stabilize the ants’ nests with their roots and might additionally sometimes offer food in form of edible fruit pulp, seed appendages or floral and/or extra-floral nectaries (e.g. Yu 1994, Davidson 1988; Kleinfeldt 1978, 1986). Again, details and degree of the mutual benefits depend on epiphyte and ant species (Weissflog et al. 1999, Kaufmann & Maschwitz 2006).