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Encyclopedia of Social Insects

Living Edition
| Editors: Christopher K. Starr

Ant-Plants: Epiphytic Rubiaceae

  • Guillaume ChomickiEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-90306-4_10-1

Synonyms

Introduction

The Hydnophytinae (Rubiaceae, Psychotriae) is the largest group of ant-plants, with approximately 117 almost exclusively epiphytic species distributed through Southeast Asia to Vanuatu and Fiji [3, 8]. The Hydnophytinae comprise five genera: Hydnophytum, Myrmecodia, Anthorrhiza, Myrmephytum, and Squamellaria [1, 3, 8].

All species form a tuber that consists in a modified hypocotyl and a network of self-formed galleries connected to the outside via entrance holes. The Hydnophytinae show stark variations in their symbioses with ants. Some 45 species form generalist and facultative symbioses with almost any arboreal ant species [2, 3] (Fig. 1a). This includes the majority of Hydnophytum species, as well as a few species of Myrmephytum and Anthorrhiza [3]. In these symbioses, the plants get ant-derived nutrients but no anti-herbivore defense from their ant occupants, while the ants are provided with a nesting site (domatium). Some 46 other species across most of the range of the Hydnophytinae form specialized symbioses with one or two dolichoderine ant species, typically from the genera Philidris or Anonychomyrma [2] (Fig. 1b). This involves all ~26 Myrmecodia species, 6 species of Squamellaria, 1 of Myrmephytum, and 3 of Anthorrhiza [3]. These symbioses involve higher levels of dependence since the plant provides not only a nesting site but also food rewards. Some dolichoderine species are obligately dependent on the plant for nesting, with one extreme case being the Fijian ant Philidris nagasau that has entirely lost the ability to build carton nests [2]. Finally, some 26 species, largely Hydnophytum, but including 1 species of Squamellaria and another of Anthorrhiza, have lost the symbiosis with ants; they retain the tuber, but it no longer form domatia [3] (Fig. 1c). The unique natural history of the Hydnophytinae makes them an ideal system to ask various questions about the evolution of mutualisms. Below I outline some of their unique features and how they can inform the evolution of symbioses.
Fig. 1

Illustration of the symbioses between ants and epiphytic Rubiaceae. (ac) Three main types of symbioses in epiphytic Rubiaceae. (a) Squamellaria wilkinsonii, forming generalist symbioses with ants in Fiji. (b) Myrmecodia alata, forming specialized symbioses with dolichoderine ants in Indonesian Papua. (c) Hydnophytum myrtifolium forming no symbioses with ants but instead accumulates rainwater where the frog, Cophixalus riparius, breeds in the highlands of Papua New Guinea. (di) The farming symbiosis between Philidris nagasau ants and Squamellaria. (d) P. nagasau worker dispersing a Squamellaria seed. (e) Squamellaria “nursery” where a sunken site has been planted with seeds and two seedlings are emerging (see holes in the bark where a worker emerges; bark removal revealed that many seeds were present guarded by P. nagasau workers). (f) P. nagasau worker visiting the tiny domatia of a Squamellaria seedling to fertilize it. (g) Longitudinal section through a large Squamellaria imberbis, revealing two types of inner wall structures: the warted walls (left inset) where ants defecate and place detritus and the smooth walls (right inset) where ants rear their brood. (h) Squamellaria farm with dozens of individuals, here S. major and S. thekii, overlooking a bay, in Taveuni, Fiji. (ij) Food rewards (post-anthetic nectary) in specialized Hydnophytinae. (i) Squamellaria wilsonii, Fiji. (j) Longitudinal section through a Myrmecodia horrida, New Guinea, revealing the hidden nectaries sunken under the stem arrow heads and accessible to the ants via channels under the stem. (Photos B, C, and J by Matthew Jebb)

How Do These Symbioses Form and Re-establish?

Hydnophytinae involved in generalist symbioses all have fleshy fruits that are bird-dispersed [2, 7]. These tend to occur in more variable locations in the canopy than do specialized species, with the symbiosis forming when arboreal ant colonies occupy the domatia. The large number of ant species found in generalist Hydnophytinae [2] suggests that there is frequent turnover of the ant inhabitants. In these generalist symbioses, it is also frequent to find other arthropods or even small vertebrates such as gecko or skinks in the oldest (central) cavity of the plant in old specimens.

The situation is very different in specialized symbioses, which involve seed dispersal by ants in addition to bird dispersal, or even exclusively ant dispersal [2] (Fig. 1d). Dolichoderine ants cultivate the plants either in multi-species ant-gardens [4] or in exclusive obligate agriculture, as in the Fijian ant-plant symbiosis [5]. Ants do not plant their epiphytes haphazardly but discriminate in favor of trees with seasonal (fruits) or continuous (extrafloral nectaries) food rewards, or trees with natural defenses [2, 6], similarly to Neotropical ant-gardens.

While little is known about the ant partners’ population structure and colony cycle, the hypothesized way to form new symbiosis involves a splitting and budding of the colony [2, 9]. This makes sense, because it is clear that some colonies are polydomous and extend over several trees [2, 9], and the presence of multiple alate female reproductive in the numerous plants cultivated by a single ant colony would allow such splitting. Moreover, a key aspect, especially evident in the Fijian farming symbiosis, is the multigenerational nature of the mutualism. This buffers the large difference in ant and plant life cycles, enabling small yet rewardless ant-plants (providing neither food rewards nor domatia) to be taken care of by the ants, while neighboring mature epiphytes supply the nesting sites and food.

The Fijian Farming Symbiosis

If cultivation mutualisms have evolved many times across the tree of life, from snails to deep-sea crabs, damselfishes, and sloths, only some social insects form true agricultures –defined by habitual planting, cultivation, harvest, and dependence on the crop [10]. Recently, it has been evidenced that true agriculture is not restricted to fungus-farming but also involves plant farming by ants: the dolichoderine ant Philidris nagasau farming Squamellaria species in Fiji [2]. This ant species forms large “farms” with dozens of Squamellaria plants high in the canopy. The ants collect seeds in the fruits before they are fully ripe (which in turn prevents their removal by birds) and plant them in sunken pockets under tree bark. They place a few seeds (up to 10) in a pocket, and a small group of workers stays under the bark with the seeds, presumably to prevent seed predation (Fig. 1e). To emerge from their sunken sites under tree bark, the seedlings have evolved an elongation “foot” of the hypocotyl, which delays domatium development until the seedling has escaped from the bark [2]. Once the seedling has a ~1.5 cm large domatium with its first entrance hole, ant workers enter the seedling and actively fertilize it by defecation [2] (Fig. 1f). The fertilization by ants continues throughout the life of the plant and exclusively occurs on some hyper-absorptive structures called “warts” inside the domatia (Fig. 1g). Similar to other specialized Hydnophytinae such as Myrmecodia [7], plants from multiple overlapping generations occur in the same ant colony (Fig. 1h). Sexually mature farmed Squamellaria produce food rewards consisting of post-anthetic nectaries, which produce a sap rich in sugars and to a lower extent amino acids [5] (Fig. 1i365体育网站). The planting of several generations of plants together implies that the re-establishment of the symbiosis – a critical step in other ant-plant symbioses involving bird-dispersed trees or shrubs that needs to be found at each generation by founder queens – is mitigated since the symbiotic ants take care of it.

Nutrition and Defense in Ant/Hydnophytinae Symbioses

In the generalist symbioses, ant-derived nutrients are by-products of ant nesting (i.e., detritus brought into the domatia, defecation). By contrast, in specialized symbioses and in particular the Fijian farming symbiosis, dolichoderine ant symbionts only bring detritus and defecate in the warted chambers of the domatia, while the smooth chambers are used for brood rearing [7]. Hydnophytinae forming specialized symbioses with dolichoderine ants have evolved a physiological partitioning with warty cavities being extremely absorptive and the smooth cavities being poorly absorptive (Fig. 1g). Anti-herbivore defense seems to be secondary in the symbiosis, apparently absent in generalist symbioses, presumably because generalist arboreal ants have no patrolling behavior. In specialized symbioses, dolichoderine ants appear to provide some defense against herbivores [6365体育网站]. Contrary to other ant-plant symbioses in which the ants have patrol – for instance, mediated by chemical cues emitted by young, vulnerable leaves or damaged leaves – the defense function performed by dolichoderine ants seems to be mediated by the continuously produced food rewards (nectary in old flowers), similar to indirect defense in plants with extrafloral nectaries.

Hydnophytinae as a Model for the Evolution of Mutualisms

The unique natural history, clade size, and evolutionary replication of the Hydnophytinae make them an outstanding system to study the evolution of mutualism. So far, this group has shown that recurrent breakdowns of the symbiosis have occurred in generalist but not in specialized mutualisms, that a common pathway to mutualism breakdown involves biome shifts to areas where the partner is scarce, in this case high elevation, or that mutualism-related traits are under strong stabilizing selection in specialized symbioses, less so in generalist symbiosis, and release from selection (hence evolving much faster) in species that have lost the symbiosis with ants [3].

Another important finding from this system is the correlated evolution of rewards and an exclusion mechanism during mutualism specialization. Increased reward is often necessary for an obligate relationship to evolve, but it also entails the risk of attracting more opportunists; here nectar rewards are concealed by a thick epidermis that can exclude exploiters [5]. In a few Myrmecodia species, rewards are sunken within the stem (Fig. 1j), possibly as a way to reduce access of exploiters.

Cross-References

References

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Department of BioscienceDurham UniversityDurhamUK