Ant Plants, Macaranga
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Associations of Macaranga Species with Ants: From Facultative to Obligate
Myrmecophytism: Obligate Associations with Specific Ants and Other Partners
Myrmecophytism, the obligate association of host plants with permanent ant inhabitants, has evolved independently in the sections Pachystemon and Pruinosae as well as in the section Winklerianae [1, 3]. Approximately 30 species of Macaranga are obligately associated with ants, mostly with nine species of Crematogaster, of which the majority are in C. borneensis group. These ants colonize Macaranga hosts in the sections Pachystemon and Pruinosae (except for M. puncticulata, which is associated with a Colobopsis species from the subfamily Formicinae), whereas plants in the section Winklerianae are colonized only by C. morphospecies 8 that belongs to a different Crematogaster subclade [2, 3].
Associations of ants of the C. borneensis group and Macaranga hosts are not strictly species-specific. Each of the eight species of ants inhabits between two to seven different Macaranga host species. In turn, each species of Macaranga may also be colonized by up to three different Crematogaster ants [1, 2, 3]. Nonetheless, recurring association patterns between the ants and plants can be observed over a wide geographic range. Traits of Macaranga host plants that enhance the specificity of their association with ants are stems coated with wax blooms in some species and/or stems whose central cavity has to be actively excavated by the Crematogaster ants. Only some Crematogaster species obligately associated with Macaranga are able to walk on the wax-coated stem surfaces, while for other Crematogaster species and most unspecific arboreal ants, the stem surface is too slippery to walk on [1, 3]. Active excavation of the stem cavities, also by founding queens, requires more energy, and thus only the larger bodied species among the specific Crematogaster ant partners are able to utilize Macaranga species with this trait [1, 3].
Endophytic coccids are a third specific partner in the associations between Decacrema ants and Macaranga365体育网站 and are collected from the plant’s surface during the coccid’s crawler stage and carried into the nest cavities by workers. Recently another potential partner in the symbiosis was recognized: nematodes reside in refuse piles of the ants in the hollow stems. Queens carry these nematodes in their postpharyngeal glands and thus bring these nematodes along on their nuptial flights. The nematodes may contribute to nitrogen recycling and may be consumed by the ants.
Development and Stability of Ant-Plant Associations
Myrmecophytic Macaranga plants are colonized by Crematogaster ants as seedlings or small plants. Macaranga species such as M. hypoleuca produce swollen internodes that are utilized as nest cavity by ant queens already at a height of 10–15 cm. After the nuptial flight, a Crematogaster queen searches for a Macaranga host plant and enters it by gnawing a hole into the stem to reach the hollow cavity inside [1, 3]. She seals this entrance hole from the inside, lays eggs, and feeds the brood using her metabolic reserves. Once the first workers eclose, they make small entrance holes from inside the stem and start patrolling the plant’s surface as they search for food (Fig. 2a–c). Food sources are presented as extrafloral nectar at nectaries on young leaves as well as nutrient-rich food bodies that Macaranga plants produce either on the stipules or leaves. Another food source provided by the plant is honeydew produced by endophytic coccids (Fig. 2d). Coccids seem to play a major role in the provisioning of carbohydrate-rich food for workers, especially in times when direct food production of the plant is reduced. While the ant colony relies entirely on food sources and nesting space offered by the plant, the ants defend the plant against herbivores as well as encroaching vegetation. Climbing plants are destroyed, which allows a better growth of the light-demanding Macaranga pioneer plants and hinders access of potential competitors to the plant [3, 5].
Myrmecophytic associations between Crematogaster (borneensis group) and Macaranga are obligate for ants and plants alike. However, the dependence of the ant partner on the host plants is even stronger, as the ants depend exclusively on the food provided by the plant. Thus, the specific Crematogaster ants have to date never been found nesting or foraging away from their hosts. In contrast, host plant seedlings have to survive without the protective services offered by the ants until they have reached a size large enough for an ant queen to enter. Seedlings without ants usually do not survive in the natural environment over longer periods of time [3, 5]. Large Macaranga trees that have lost their ant partners due to the comparatively shorter life-span of the ant colony will often also survive the time lag until they are colonized again by Crematogaster queens .
In spite of the association being obligate for plants and ants alike, associations are not free of conflict. When the Macaranga365体育网站 hosts flower, ants are attracted to the flower buds by the plant with an increased production of food bodies in the young stipules and directly on the flower buds. However, when the flowers are fully developed, many host plant species abscise stipules in proximity to the flowers and stop food body production on the flowers, so that ants are not attracted to the flowers. While this reduces potential interference of the ants with pollinators, it also reduces food availability for the ants temporarily until new stipules regrow after the flowering period. This conflict over resource allocation is sometimes “solved” by the ants to their advantage by destroying the flower buds to ensure a constant food supply.
Due to the increasing conversion of tropical lowland rainforests of Southeast Asia, Macaranga pioneer species have become more abundant in recent decades. However, high levels of disturbance may result in a disruption of their symbiotic associations with ants in the future. Since obligately ant-associated Macaranga365体育网站 species are important trees in the regeneration of secondary forest, changes or even disruption of the associations might impact forest restoration.
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