Observations on ant-plant interactions in Pachycentria and other genera of the Dissochaeteae (Melastomataceae) in Sabah and Sarawak

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© by Gustav Fischer Verlag

Observations on ant-plant interactions in Pachycentria and other genera of the Dissochaeteae (Melastomataceae) in Sabah and Sarawak GUDRUN CLAUSING Institut flir Spezielle Botanik, Johannes Gutenberg-Universitat Mainz, D-55099 Mainz Accepted: May 30, 1997

Summary In Sabah and Sarawak (Malaysia) ant-plant interactions of Dissochaeteae were studied in the field. Whereas some species of Dissochaeteae show only loose and fortuitous interactions with ants as the result of the provision of pearl bodies and nesting places which are used by ants facultatively, Pachycentria constricta and P. glauca show a complex relationship with ants mediated by other ant plants. Both species provide pearl bodies and potential nesting space or shelter for ants in dried out and hollow root swellings. The main characteristic which differentiates them from all other Melastomataceae interacting with ants are their particular seeds which are attractive to ants and carried into their nests. As a result Pachycentria constricta grows in ant gardens, e.g., together with Hoya, and P. glauca is frequently found growing on Hydnophytum and Dischidia. Both species might increase the fitness of the community in which they live by the provision of food in form of pearl bodies and by water storage in their root swellings. In return, Pachycentria constricta and P. glauca are planted in a favourable nutrient-rich environment and perhaps are protected by the ants. Key words: Ant-plant interactions, seeds, root swellings, pearl bodies, Melastomataceae, Dissochaeteae, Pachycentria

I. Introduction The Melastomataceae is a species-rich pantropical family with a number of species which have characters predisposing them for ant-interactions. Thus, many are provided with dense long trichomes, which may protect small ants especially during the early stages of plant colonization (DAVIDSON et al. 1989). In addition, many members of the family have glandular hairs containing substances which may be attractive to ants as nutrients. Furthermore many species provide nesting places, e.g., in hollow stems or leaf pouches, and the strongly arcuate leaf venation typical of the family may facilitate the development of leaf base pouches or interpetiolar pockets. There exists a considerable number of genera in which ant-plant interactions have been suspected. Examples are Allomaieta GLEASON, Axinaea RUIZ & PAVON, Blakea P. BROWNE, Clidemia D. DON, Conostegia D. DON, Henriettea DE CANDOLLE, Medinilla GAUDICHAUD-BEAUPRE, Miconia RUIZ & PAVON, Sagraea DE CANDOLLE, Tococa AUBLET and Topobea

AUBLET(DAVIDSON & MCKEY 1993, S. S. RENNERpers. comm.). Only in a few species of the neotropical tribe Miconieae have these ant-plant interactions been studied in the field (e.g., SCHNELL 1963, 1967, WHIFFIN 1972, HERRE et al. 1986, DAVIDSON et al. 1989, MORAWETZ et al. 1992, NICKOL 1993, VASCONCELOS 1993, RENNER & RICKLEFS in press). The present study deals with observations of antplant interactions in a paleotropical tribe of the family, the Dissochaeteae. The tribe consists of eleven genera distributed from Madagascar, throughout SE Asia, New Guinea and northern tropical Australia. There appears to be no field or laboratory work on ant-plant interactions in the Dissochaeteae except for the morphological work by HOLMGREN (1911) and O'DowD (1982) on pearl bodies in Medinilla magnifica LINDL. and by SOLEREDER (1920) on leaf domatia in M. disparifolia C. B. ROBINSON. Species of Pachycentria have long been suspected to occasionally house ants in hollow swollen roots (BECCARI 1884-6; HUXLEY 1980), but relevant observations in the field are lacking. JANZEN (1974) FLORA (1998) 193

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T' reported that in Bako National Park in Sarawak, Malaysia, Pachycentria tube rosa (nom. illeg. = Pachycentria glauca TRIANA) sometimes grows epiphytically on the rubiaceous ant-plant Hydnophytum formicarum JACK, albeit without itself being occupied by ants. In agreement with this is the report by KIEW & ANTHONYSAMY (1987) that Medinilla maingayi (CLARKE) MAXWELL and Pachycentria constricta (BLUME) BLUME may grow epiphytically on ant-plants or in ant nests without themselves being inhabited by ants. During monographic work on several genera of the Dissochaeteae, including Pachycentria BLUME, Dissochaeta BLUME, Diplectria (BLUME) H. G. L. REICHENBACH, and subgroups of Medinilla, I have made ecological field observations. In the field I came across several more or less intense ant-plant interactions within these genera. The closest and most complex interaction with ants are observed in Pachycentria constricta and P. glauca. All observations are described, and discussed in the light of the evolution of ant-plant interactions in general and in the Melastomataceae, and the more complex ones are supplemented by anatomical and morphological studies of relevant plant parts.

II. Material and methods This study is based on field observations, herbarium specimens, and morphological and anatomical studies of dried and fresh material. Field observations were made from March to June 1995 in Sabah and Sarawak, Malaysia. In addition, I have examined about 350 herbarium collections of Pachycentria constricta and P. glauca, paying particular attention to information on the specimen labels. Pearl bodies were observed in the field and in the greenhouse on bagged stems, leaves, and inflorescences, and also studied using light microscopy. Their chemical composition was analyzed using standard tests for lipid and starch. Microtome sections served to investigate swelling anatomy. Plant vouchers made in connection with this study are deposited in the herbaria of the Sabah Forestry Department in Sandakan, the Mount Kinabalu National Park, and the University of Malaysia, Sarawak. Ant vouchers are kept in the private collection of the author.

III. Results 1) Ant-plant interactions in Pachycentria constricta and P. glauca The plants. - P. constricta is distributed from Burma, Thailand and Peninsular Malaysia to Sumatra, Borneo, Java, Philippines and Sulawesi, spanning an altitudinal range from sea level to 2000 m. It is an epiphytic or rarely epilithic shrub, usually about 1-2 m tall. Although it has been collected at heights of 30 m in 362

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trees, it is more commonly found three to ten meters above the ground. The adventitious roots sometimes have tuberous, orange to brown swellings, and the presence or absence of such swellings has led to the naming of a number of species, such as P. formicaria MERRILL, P. macrorhiza BECCARI, and P. tuberculata KORTHALS, which I consider conspecific with P. constricta (CLAUSING, in prep.). Pachycentria glauca is restricted to lowland and mountain forests in Borneo (Sabah, Sarawak, Kalimantan). It is a 20-60 cm tall epiphytic shrub with hanging, creeping or erect branches. Adventitious roots in this species are provided with irregular, globose swellings 2-3 cm across. Medinilla maingayi which occurs in the Malayan Peninsular is extremely similar to P. glauca including the type of globose root swellings. Medinilla maingayi should be regarded as a subspecies of P. glauca (CLAUSING, in prep.). Seed. - The fruits of Pachycentria constricta and P. glauca are, like those of most Dissochaeteae, fleshy berries dispersed by birds. Seeds of the Dissochaeteae are normally smaller than 1.0 mm and numerous, cuneate or ovate and with a smooth or reticulate testa with interdigitate cells (Fig. 1b). In P. constricta and P. glauca, however, the berries contain only 6-12, 2.0-2.5 mm long, cylindrical seeds with a foveolate testa which becomes porous when dry (Fig. 1a). These are by far the largest seeds found in the tribe. The embryo is filled with lipids. Ants take the seeds of both species from bird droppings and carry them into their nests. As a result, the plants are found growing on ant plants such as Hydnophytum spp. or in ant gardens together with Hoya R. BR. spp. (Asclepiadaceae). Indeed, in the stunted 'kerangas' forest on nutrient-poor sandstone soils at Bako National Park, P. glauca appears to grow exclusively on the tubers of Hydnophytum formicarum. Pearl bodies. - Pearl bodies of all Dissochaeteae studied (see below and Table 1), including those of P. constricta and P. glauca, measure 0.3-1.0 mm across, are translucent or whitish, globose in shape, and sessile (Fig. 2b). They can occur on leaves, stems, inflorescences and flowers (Fig. 2a, Table 1). They are neither restricted to veins, nor are they distributed evenly. The 15-40 cells of each pearl body contain about 5-20 lipid-rich vesicles which measure c. 10 !lm across, and c. 50 to 300 starch granules which measure c. 5 !lm across. The staining of the granules with Lugol's solution resulted in a reddish-brown colour with a slight violet gleam, indicating that the granules contain predominantly amylopectin rather than amylose. Pearl bodies are difficult to study in the field because they are removed by ants immediately after formation. The pearl bodies of P. constricta studied in the field were consumed by Crematogaster (Myrmicinae) ants,

Fig. 1. a. seed of Pachycentria glauca, b. typical seed of Dissochaeteae.

those of P. glauca by Philidris (Dolichoderinae) ants. In several plants of P. glauca I observed, the Philidris ants which are known to be associated with Hydnophytum patrolled their host as well as P. glauca and were particularly frequent on the pearl body-carrying inflorescences and leaves of this species. Adventitious roots. - Pachycentria constricta and P. glauca have elongate or globose swellings on their adventitious roots. The swellings are irregular in shape and separated by parts of the roots which are not swollen. The elongate, orange-brown root swellings of P. constricta are up to 20 cm long and measure about 4 cm in diameter (Fig. 3 a). When the species is growing in an ant nest, the roots often form tangled masses which hold carton material. By comparison, the globose, grey-green root swellings of P. glauca are much smaller, measuring 2-3 cm across (Fig. 3b). Elongate and globose root swellings of these two species have the anatomical structure of a storage root (Fig. 3c). Their woody core consists of pith, rays and xylem elements (sc1erenchymatic cells and vessels). It is surrounded by a cylinder of meristematic tissue, for-

ming a cambium. The cambium layer is surrounded by phloem, which grades into a multilayered soft parenchymatic tissue with relatively large cells, forming the cortex. This in tum is followed by 5-8 layers of periderm. The root swellings are the result of a hypertrophic development of the cortical parenchyma in certain sections of the root. Cell walls in this tissue are thin and not sc1erified, and the cells are filled with water. Small side roots penetrate phloem, cortex and periderm (Fig. 3 c). When the root swellings dry out, the cortex shrinks, and the bark bursts in some places because its lignified cells are incapable of adjusting to the shrinking. Then the parenchyma becomes exposed and damaged, and the swellings eventually dry out and become hollow. The drying-out of a typical root swelling takes several days. Apparently, the plants are not harmed when some their root swellings dry out. The roots of P. glauca growing at Bako National Park were penetrating the tuber cavities of H. formicarum without entering tuber tissue. The root swellings of P. glauca themselves were not inhabited by ants unless they were partly or totally dried out. FLORA (1998) 193

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t Table 1. Pearl body-producting species in the Melastomataceae (pers. obs.) Species

Pearl body-producing plant part

Site

Diplectria glabra var. kinabaluensis (VELDK.) J. F.

stem; interpetiolar ridges; leaves

Sabah: Mt. Kinabalu National Park, around Park Headquarter; montane rain forest

KUNTZE

stem; interpetiolar pockets

Sarawak: Bukit Matang, along road, edge of primary forest

Dissochaeta divaricata (WILLD.)

inflorescence

Sabah: Mt. Kinabalu National Park, near Poring, secondary vegetation

Gravesia guttata (HOOK.) TRIANA

leaves

Greenhouse in Mainz

Kendrickia walkeri (WIGHT ex GARDN.) TRIANA

leaves

Greenhouse in Stockholm

Medinilla alpestris (JACK) BLUME

inflorescence; leaves

Greenhouse in Mainz

Medinilla basaltarum JUMELLE &

inflorescence; leaves

Madagascar: Massif du Marojezy ; montane rain forest

Medinilla bigradata PERRIER

inflorescence; leaves

Madagascar: Andasibe (Perinet Reserve); lowland primary forest

Medinilla speciosa (REINW. ex BLUME) BLUME

inflorescence; leaves

Sabah: Mt. Kinabalu National Park, around Park Headquarter; montane rain forest

Medinilla suberosa REGALADO

inflorescence; leaves

Sabah: Mt. Kinabalu National Park, around Park Headquarter; montane rain forest

Medinilla succulenta (BLUME)

inflorescence, leaves

Greenhouse in Mainz

MAXWELL

Diplectria beccariana (COGN.)

G.DON

PERRIER

BLUME

Monolena primulaejlora HOOK. f. Pachycentria constricta (BLUME) BLUME

Pachycentria glauca TRIANA

leaves

Greenhouse in Mainz

inflorescence; leaves

Sarawak: Bukit Matang, along road, edge of primary forest; Greenhouse of the Palmengarten Frankfurt

inflorescence, leaves

Sarawak: Bako National Park, along Lintang Trail, Kerangas forest

O.lmm

b

Fig. 2. a. pearl bodies on a flower of Pachycentria glauca, b. typical pearl body of the Dissochaeteae. 364

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On Bukit Matang (also known as Mt. Surapi) near Kuching in Sarawak, I observed an individual of P. constricta which was growing in an ant nest together with a species of Boya. The adventitious roots of P. constricta formed a tangled mass and had several large swellings, but these were not inhabited by ants. Between them, however, were several small nests of Crematogaster ants with their brood. The association of P. constricta and P. glauca with rubiaceous, asclepiadaceous, or other ant-plants is facultative; collectors' notes on about 3% of herbarium specimens of P. constricta and 12,5% of P. glauca specifically mention an association with ants, including root occupation by ants. A few labels on P. constricta specimens also state that the plant was growing in an ant nest. Also, 40% of the herbarium collections of P. constricta and almost 80% of those of P. glauca show or mention root swellings.

t"

phloem cambiurn-H---~

xylem

Fig. 3. a + b Root swellings of Pachycentria constricta (a) and Pachycentria glauca (b); drawings taken from BECCARI 1884-6, c. schematic cross section of a root swelling of Pachycentria, detail: cortical parenchyma.

2) Ant-plant interactions in other Dissochaeteae Pearl bodies. - I have observed pearl bodies on stems, leaves and inflorescences of a number of Dissochaeteae in the field and in the greenhouse. In the field I used gauze bags which prevented ants from removing the pearl bodies in order to show pearl body production (Table 1). The pearl bodies observed were of the same type as those described for P. constricta and P. glauca. In Medinilla speciosa and Diplectria glabra var. kinabaluensis, I observed pearl bodies being harvested regularly by a colony of the herdsmen ant Dolichoderus sp. (Dolichoderinae) which tended their trophobionts. In Diplectria glabra var. kinabaluensis, the ants stayed on the plants for two weeks, in Medinilla speciosa over six weeks; M. speciosa can produce more than 200 pearl bodies per leaf. In Dissochaeta divaricata, the pearl bodies were harvested by a colony of Oecophylla smaragdina (Formicinae). Root swellings, hollow stems and interpetiolar pockets. - Root swellings of the elongate type as described for P. constricta also occur in M. homoeandra

(STAPF) NAYAR, M. muricata BLUME, M. varingiaefolia (BLUME) NAYAR, and most Medinilla species from Madagascar. The swellings of these species show the same anatomy as described for P. constricta and P. glauca. Species of Diplectria and Dissochaeta observed in the field (including the three species discussed in the previous section as having pearl bodies) never had swellings on their adventitious roots like those species of Medinilla and Pachycentria named. Instead, Dissochaeta and Diplectria possess a wide soft pith so that the stems can become hollow relatively easily. Additionally, some species of these two genera show interpetiolar pockets which provide shelter or nesting places for small insects. The interpetiolar pockets of Diplectria beccariana (COGN.) KUNTZE, which I observed on Bukit Matang near Kuching (Sarawak), were occupied by a colony of Crematogaster sp. which used these pockets to house their mealybugs. At the Sikog Waterfall (Penrissen, Sarawak) I found a species of Dissochaeta the stem of which was inhabited by Crematogaster sp. (Myrmicinae). The stem measured 0.5-1 cm FLORA (1998) 193

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in diameter and the inner two thirds of the cross section were filled by a soft yellowish pith. The colonized internodes showed 10-20 holes, and the nodes were not hollowed.

IV. Discussion Among mostly loose and fortuitous interactions between ants and Dissochaeteae there exist two cases, involving P. constricta and P. glauca, which show a more complex interaction which differs from any other ant-plant mutualism known in the Melastomataceae. The more loose interactions in the Dissochaeteae result from structures of the plants which are in one way or the other attractive to ants. Generalists among the plant-inhabiting ants are able to colonize many different nesting opportunities and use a great variety of nutrient sources offered by plants (HOLLDOBLER & WILSON 1990). The use of interpetiolar pockets of Diplectria beccariana by a Crematogaster colony as a save place for mealybugs is one example for this. A further example is the Dissochaeta with internodes which were colonized by Crematogaster ants. Here the fact that the pith was removed irregularly and that some of the holes made by the ants in order to colonize the stem were closed again argue for a facultative interaction. Indeed, many species of Crematogaster are known for their opportunistic colonization of many different plant species (HOLLDOBLER & WILSON 1990). A mutualistic association of Crematogaster with plants is known from Macaranga THOUARS (FIALA & MASCHWITZ 1991, FIALA et al. 1994). The production of pearl bodies is another example of a structure which is attractive to ants as an additional nutrition source. Although it is unknown to what extent pearl bodies contribute to the energy budget of ant colonies, the numerous pearl bodies of Medinilla speciosa are likely to be one reason why the herdsman ants stayed for more than six weeks on these plants (compare MASCHWITZ & HANEL 1985). The pearl bodies may increase the frequency and duration of ant visits to the plant which might be an advantage in terms of protection against herbivores. The loose interactions described could be regarded as unspecialized facultative interactions which nevertheless enhance the fitness of each partner, and therefore might be the starting point for the evolution of a mutualistic relationship. The more complex interactions of Pachycentria constricta and P. glauca with ants result from a complex of characters which enables these two species to grow in ant nests. First, P. glauca and P. constricta have seeds which are attractive to ants and are secondarily dispersed by them. Perhaps the seeds and/or the fruit flesh 366

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sticking to them contain chemical compounds attractive to ants, similar to, e.g., the aromatic compounds found in seeds and surrounding fruit flesh of some epiphytes in neotropical ant gardens (SEIDEL et al. 1990). In any case, P. glauca almost exclusively grows with epiphytic ant plants such as Dischidia R. BR. (Asclepiadaceae) (KIEW & ANTHONYSAMY 1987) or Hydnophytum (JANZEN 1974; this paper), where its seeds must have been deposited by ants and germinated in the nutrient-rich debris in or near the nest. Pachycentria constricta, which can also grow terrestrially, is also found in ant gardens. For example, A. WEISSFLOG (pers. comm.) who studied 30 nests of Camponotus ants between the roots of Hoya elliptica, found P. constricta in two of them. Second, P. constricta and P. glauca produce pearl bodies on their leaves and inflorescences. These are harvested by the ants and therefore contribute to the energy budget of the ant colony. This might be the reason why P. constricta and P. glauca are tolerated in ant-nests or on ant-plants and are not destroyed or removed by the ants. Finally, both species form root swellings which store water which helps these epiphytic plants to withstand temporal droughts. They enable both species to grow in ant nests or on ant plants as habitats exposed to temporal droughts. At the same time the storage roots might stabilize the water balance of the ant-plant community in which they live. The tuberous roots of P. constricta are furthermore able to hold carton material so that they increase the stability of the ant garden. In conclusion, P. constricta and P. glauca become an integrated part of the ant-plant symbiosis because they increase its fitness by supplying additional nutrients, perhaps water and stabilizing root systems. The ants might increase the fitness of the plants by planting them in a nutrient-rich habitat and patrolling them in the same way as they patrol their main hosts. It is a speculative but interesting question which character of the plant played a key role in the evolution of the ant-plant relationsphip. Work by FIALA & MASCHWITZ (1991) on Macaranga suggests that the provision of nesting places may sometimes be more important for the development of a permanent association with ants than the provision of extrafloral nectar or other kinds of food. In the same vein, WARD (1991) suggested that ant-plant-relationships commonly evolve from parasitisms in which ants inhabit living plant cavities or from the occupation of dead hollow twigs rather than from food-based interactions. In order to identify the decisive ant-attractive character in the Dissochaeteae it is nescessary to look at the distribution of these characters (i.e., pearl bodies, root swellings, seeds) among the closest relatives of Pachycentria. These are Medinilla, Plethiandra and Pogonanthera (CLAUSING, in prep.) Pearl bodies show the widest dis-

f' tribution in this group of genera (Medinilla alliance) and they also occur in other genera of the Dissochaeteae. Root swellings occur in most species of Pachycentria, in VELDKAMP'S (1978) Medinilla myrtiformis alliance from which Pachycentria might have originated, in Pogonanthera which should be treated as congeneric with Pachycentria, and in most Medinilla species from Madagascar. Seeds which are attractive to ants and planted in their nests are only known from P. constricta and P. glauca. These two species also show root swellings and the production of pearl bodies, which leads to the conclusion that although all three characters are integral part of the complex interaction with ants found, neither food provision nor the provision of potential nesting place but the particular seeds of P. constricta and P. glauca is the main character which may have triggered the evolution of this complex interaction. The living or dead habitable cavaties provided by P. constricta and P. glauca in the form of root swellings are not regularly occupied by ants. Only when they become hollow as the result of water-stress, ants apparently readily accept them as nesting places. That the provision of nesting places is of minor importance for the ant-plant interaction found in P. constricta and P. glauca seems to be inconsistent with the results of FIALA & MASCHWITZ (1991) and WARD (1991). This inconsistency may find its explanation in the fact that P. constricta and P. glauca are planted into an existing symbiosis or into an ant garden where nesting place is already available and no additional nesting place may be needed. Accordingly, the primary importance of the seeds for the ant-plant interaction in P. constricta and P. glauca can not be compared with symbiotic systems between only one species of plant and ants. Such an independent symbiosis with ants has not evolved in P. constricta and P. glauca. This, however, is different in ant-plant interactions of neotropical Melastomataceae in which nesting places in leaf pouches or in stems seem to play the key role for a permanent association with ants. Leaf domatia situated at the leaf base are common in neotropical Miconieae but are not known from paleotropical melastomes. DAVIDSON & McKEy (1993) have pointed out that there is a remarkable correspondence between ant-plant associations in the New and Old World tropics as a result of parallel evolution. This is not obvious from the ant-plant interactions found in the Melastomataceae so far. The comparison of ant-plant interactions in neotropical Miconieae with those described for the Dissochaeteae does not show much similarity. The seed-mediated occurrence of P. constricta and P. glauca in ant gardens and ant nests must be regarded as an evolutionary peculiarity not easily comparable to other ant-plant interactions.

Acknowledgements I am grateful to A. WEISSFLOG for identifying the ant species and informative comments about ant-plant interactions. I thank B. FIALA, C. HUXLEY-LAMBRICK, M, NICKOL, and K. WURDACK for critically reading the manuscript, and J, W, KADEREIT and S. S. RENNER for constructive discussions and encouragement. Financial support for this project came from the Deutsche Forschungsgemeinschaft (grant No. 603 to S. S. Renner). Field work was conducted with kind permission of the Unit Perancang Ekonomi (EPU, Kulala Lumpur Malaysia), and of Sabah Parks (Kota Kinabalu, Sabah, Malaysia). Logistic support came from Kinabalu Park, Sabah, and the Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak. I would like to thank the curators of the following herbaria for loan of material: A, AAU, B, BM, BKF, BO, C, HAST, HBG, K, KEP, KLU, L, SAN, SAR, SING, U, UKMS.

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