Brigitte Fiala

Specialization, constraints, and conflicting interests in mutualistic networks.

The topology of ecological interaction webs holds important information for theories of coevolution, biodiversity, and ecosystem stability . However, most previous network analyses solely counted the number of links and ignored variation in link strength. Because of this crude resolution, results vary with scale and sampling intensity, thus hampering a comparison of network patterns at different levels . We applied a recently developed quantitative and scale-independent analysis based on information theory to 51 mutualistic plant-animal networks, with interaction frequency as measure of link strength. Most networks were highly structured, deviating significantly from random associations. The degree of specialization was independent of network size. Pollination webs were significantly more specialized than seed-dispersal webs, and obligate symbiotic ant-plant mutualisms were more specialized than nectar-mediated facultative ones. Across networks, the average specialization of animal and plants was correlated, but is constrained by the ratio of plant to animal species involved. In pollination webs, rarely visited plants were on average more specialized than frequently attended ones, whereas specialization of pollinators was positively correlated with their interaction frequency. We conclude that quantitative specialization in ecological communities mirrors evolutionary trade-offs and constraints of web architecture. This approach can be easily expanded to other types of biological interactions.

Diversity of ant-plant interactions : protective efficacy in Macaranga species with different degrees of ant association

The pioneer tree Macaranga in SE Asia has developed manyfold associations with ants. The genus comprises all stages of interaction with ants, from facultative relationships to obligate myrmecophytes. Only myrmecophytic Macaranga offer nesting space for ants and are associated with a specific ant partner. The nonmyrmecophytic species are visited by a variety of different ant species which are attracted by extrafloral nectaries (EFN) and food bodies. Transitional Macaranga species like M. hosei are colonized later in their development due to their stem structure. Before the colonization by their specific Crematogaster partner the young plants are visited by different ant species attracted by EFN. These nectaries are reduced and food body production starts as soon as colonization becomes possible. We demonstrated earlier that obligate ant partners can protect their Macaranga plants against herbivore damage and vine cover. In this study we focused on nonspecific interactions and studied M. tanarius and M. hosei, representing a non-myrmecophyte and a transitional species respectively. In ant exclusion experiments both M. tanarius and M. hosei suffered significantly higher mean leaf damage than controls, 37% versus 6% in M. hosei, 16% versus 7% in M. tanarius. M. tanarius offers both EFN and food bodies so that tests for different effects of these two food rewards could be conducted. Plants with food bodies removed but with EFN remaining had the lowest mean increase of herbivore damage of all experimental groups. Main herbivores on M. hosei were mites and caterpillars. Many M. tanarius plants were infested by a shootborer. Both Macaranga species were visited by various ant species, Crematogaster spp. being the most abundant. We found no evidence for any specific relationships. The results of this study strongly support the hypothesis that non-specific, facultative associations with ants can be advantageous for Macaranga plants. Food bodies appear to have lower attractive value for opportunistic ants than EFN and may require a specific dietary adaptation. This is also indicated by the fact that food body production in the transitional M. hosei does not start before stem structure allows a colonization by the obligate Crematogaster species. M. hosei thus benefits from facultative association with a variety of ants until it produces its first domatia and can be colonized by its obligate mutualist.

Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae)

Abstract In many ant-plant species of the genus Macaranga in South-East Asia, conspicuous blooms of epicuticular wax crystals cover the stem surface. We found that many ant species were unable to walk on these surfaces. Only the specific ant partners of glaucous Macaranga host plants were capable of moving on the slippery stems without difficulty. Therefore, the epicuticular coatings of Macaranga myrmecophytes appear to have a selective function and protect the associated ants against competitors. The epicuticular aggregates function as a physical barrier; no evidence of chemical repellence was found. The extent to which ”foreign” ant species are excluded from a tree strongly depends on inclination, diameter and length of the glaucous stem sections. The particular growth form of some glaucous Macaranga ant-plants enhances the influence of the wax barriers. The ant associates of glaucous and glossy Macaranga ant-plants (genera Crematogaster and Camponotus) differ strongly in their capacity to adhere to the glaucous stems. For this reason, the wax blooms in Macaranga can act as an ecological isolation mechanism for the sympiotic ants. Within the genus Macaranga, we find a high correspondence between the occurrence of glaucousness and obligatory ant association (50% in ant-plants; 6.7% in non-myrmecophytes). The genus Macaranga thus represents one of the few cases known so far where epicuticular wax crystals are likely to have evolved in relation to insects.

A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long‐distance dispersals

Macaranga (Euphorbiaceae) includes about 280 species with a palaeotropic distribution. The genus not only comprises some of the most prominent pioneer tree species in Southeast Asian lowland dipterocarp forests, it also exhibits a substantial radiation of ant‐plants (myrmecophytes). Obligate ant‐plant mutualisms are formed by about 30 Macaranga species and 13 ant species of the genera Crematogaster or Camponotus. To improve our understanding of the co‐evolution of the ants and their host plants, we aim at reconstructing comparative organellar phylogeographies of both partners across their distributional range. Preliminary evidence indicated that chloroplast DNA introgression among closely related Macaranga species might occur. We therefore constructed a comprehensive chloroplast genealogy based on DNA sequence data from the noncoding ccmp2, ccmp6, and atpB‐rbcL regions for 144 individuals from 41 Macaranga species, covering all major evolutionary lineages within the three sections that contain myrmecophytes. A total of 88 chloroplast haplotypes were identified, and grouped into a statistical parsimony network that clearly distinguished sections and well‐defined subsectional groups. Within these groups, the arrangement of haplotypes followed geographical rather than taxonomical criteria. Thus, up to six chloroplast haplotypes were found within single species, and up to seven species shared a single haplotype. The spatial distribution of the chloroplast types revealed several dispersals between the Malay Peninsula and Borneo, and a deep split between Sabah and the remainder of Borneo. Our large‐scale chloroplast genealogy highlights the complex history of migration, hybridization, and speciation in the myrmecophytes of the genus Macaranga. It will serve as a guideline for adequate sampling and data interpretation in phylogeographic studies of individual Macaranga species and species groups.

Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia

Discussion about thrips (Thysanoptera) as main pollinators has been controversial in the past because thrips do not fit the preconception of an effective pollinator. In this study, we present evidence for thrips pollination in the dioecious pioneer tree genus Macaranga (Euphorbiaceae). Macaranga hullettii is pollinated predominantly by one thrips species, Neoheegeria sp. (Phlaeothripidae, Thysanoptera). As a reward for pollinators, the protective floral bracteoles function as breeding sites for thrips and trichomal nectaries on the adaxial surface of the floral bracteoles provide alimentation. Flowering phenology of both staminate and pistillate trees was highly synchronized within 3-4 wk periods. In contrast to pistillate trees, staminate trees start to breed the thrips inside the developing inflorescences ∼2 wk before anthesis. Breeding of Neoheegeria sp. in the laboratory indicates that the thrips development is completed within ∼17 d. Thus, staminate trees offer breeding sites for one thrips generation until the onset of pollen presentation. Intraspecific pollen transfer by thrips was proved by pollen loads of thrips taken from receptive pistillate inflorescences of M. hullettii. Bagging experiments of different mesh sizes showed that seed set reached almost the level of open-pollinated flowers when exclusively tiny insects like thrips were able to enter the net bags, but no apomictic seed set occurred when no insect access was given to the flowers.

The soft scale (Coccidae) associates of Malaysian ant-plants

Myrmecophytic species of the Paleotropical plant genus Macaranga (Euphorbiaceae) have hollow stems that are almost always occupied by ants of the genus Crematogaster and scale insects of the family Coccidae (Hemiptera: Coccoidea). The coccids have a cryptic endophytic lifestyle and are confined to this microhabitat. They are much more diverse than previously recognised. First data are presented on the diversity, prevalence, specificity and distribution of the coccids associated with myrmecophytic Macaranga species. Twenty-two species of Coccidae in total, including 15 previously unknown from Macaranga, were disco- vered from 19 species of Macaranga in Peninsular Malaysia and Borneo. The ori- ginal describers tentatively assigned the known coccid species to Coccus (Coccinae) but the Macaranga coccids still require taxonomic research to establish their correct placing. The coccids varied in their host-plant specificity from species that occurred in most of the sampled Macaranga to one species that was found almost exclusively only on a single host species. In addition to their occurrence on Macar- anga, only three species, C. macarangae and C. secretus and morphospecies C. 214 were found on rare occasions in the stem interior of a few other myrmecophytes and in a non-myrmecophytic liana, but did not regularly colonise these plants. Most of the coccids can be regarded as highly specific at the plant genus level.

Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia

The first data on the taxonomic distribution and abundance of woody plants with extrafloral nectaries (EFN) from SE Asia are reported. The species richness and frequency of woody angiosperm plants with extrafloral nectaries was studied in the Pasoh Forest Reserve, a primary lowland forest in Peninsular Malaysia. EFN were present on 12.3% of the 741 species surveyed. 91 plant species belonging to 47 genera and 16 families were found to have EFN. Euphorbiaceae, Dipterocarpaceae, Rosaceae, Leguminosae, and Ebenaceae were the families most frequently bearing EFN whereas EFN were rare in the more primitive subclasses of the Magnoliopsida and common in the more advanced taxa (Dilleniidae, Rosidae, Asteridae). Most common were flattened glands associated with the leaf blade. A comparison with data from the Neotropics showed a great similarity in regard to the taxonomic distribution of plants with EFN. EFN-plants occupied 19.3% of the cover of the Pasoh Forest 50 ha plot.Species with EFN were under-represented among shrubs and trees of the understorey. We found an increase in the number of species with EFN as well as in their cover from the understorey to the canopy emergents. EFN were found more often among the abundant species (species with n>500/50 ha). Percentage occurrence and cover of EFN-bearing plants in the 50 ha plot of primary forest was lower than recorded for secondary habitats in tropical areas. At present, in the core zone of the Pasoh Forest Reserve which has been investigated only few species known to indicate disturbance occur. Therefore most of the recorded EFN-species cannot be regarded as secondary forest plants.The interactions between ants and EFN-bearing plants appear to be rather facultative and nonspecific. In Pasoh we found 28 ant species from seven genera visiting EFN. Most of the EFN-associated ants belonged to the subfamily Myrmicinae while Ponerines were rare, a pattern which was also reported for the Neotropics.

Patterns of the crematogaster-macaranga association: the ant partner makes the difference

Summary. One of the most species-rich ant-plant mutualisms worldwide is the palaeotropical Crematogaster-Macaranga system. Although the biogeography and ecology of both partners have been extensively studied, little is known about the temporal structuring and the dynamics of the association. In this study we compared life-history traits of the specific Crematogaster (Decacrema) partner-ants and followed the development of ant colonies on eight different Macaranga host plant species, from colony founding on saplings to adult trees in a snapshot fashion. We found differences in the onset of alate production, queen number and mode of colony founding in the ant species and examined the consequences of these differences for the mutualism with the host plant.The lifespan of some host plants and their specific ant partners seemed to be well matched whereas on others we found an ontogenetic succession of specific partner ants. The partner ants of saplings or young plants often differed from specific partner ants found on larger trees of the same species. Not all specific Crematogaster species can re-colonize the crown region of adult trees, thus facilitating a change of ant species. Therefore lifespan of the ant colony as well as colony founding behaviour of the different partner ant species are important for these ontogenetic changes. The lifespan of a colony of two species can be prolonged via secondary polygyny. For the first time, also primary polygyny (pleometrosis) is reported from this myrmecophytic system.

Trade-off between chemical and biotic antiherbivore defense in the South East Asian plant genus Macaranga

The plant genus Macaranga is known for its manifold mutualistic associations with ants. The plants provide food for the ants and in turn get protection from herbivores. Depending on the strength of the plant–ant interaction, the plants investment in ants and the biotic defense derived from them is more or less effective. We conducted a comparative study on tannin content in 12 Macaranga species that were selected based on their associations with ants (three nonmyrmecophytes and nine myrmecophytes, three of which start their ontogeny as nonmyrmecophytes). Different developmental stages were investigated in three Macaranga species. Extracts of every individual plant analyzed for tannins were also tested for their effects on larval growth employing larvae of the common cutworm (Spodoptera littoralis). The studied Macaranga species differed significantly in their tannin contents as well as in the effects of their leaf extracts on the growth of S. littoralis larvae. A correlation analysis shows a connection between tannin contents and larval growth. High tannin contents and, thus more effective chemical defense, were observed in nonmyrmecophytic Macaranga species associated only facultatively with ants as compared to obligate myrmecophytes. Our study supports the hypothesis of a trade-off between chemical and biotic defense in the genus Macaranga.

Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees

To elucidate the evolution of one of the most species-rich ant-plant symbiotic systems, the association between Crematogaster (Myrmicinae) and Macaranga (Euphorbiaceae) in South-East Asia, we conducted a phylogenetic analysis of the ant partners. For the phylogenetic analysis partial mitochondrial cytochrome oxidase I and II were sequenced and Maximum Parsimony analysis was performed. The analyzed Crematogaster of the subgenus Decacrema fell into three distinct clades which are also characterized by specific morphological and ecological traits (queen morphology, host-plants, and colony structure). Our results supported the validity of our currently used morphospecies concept for Peninsula Malaysia. However, on a wider geographic range (including North and North-East Borneo) some morphospecies turned out to be species complexes with genetically quite distinct taxa. Our phylogenetic analysis and host association studies do not indicate strict cocladogenesis between the subgenus Decacrema and their Macaranga host-plants because multiple ant taxa occur on quite distinct host-plants belonging to different clades within in the genus Macaranga. These results support the view that host-shifting or host-expansion is common in the ants colonizing Macaranga. Additionally, the considerable geographic substructuring found in the phylogenetic trees of the ants suggests that allopatric speciation has also played a role in the diversification and the current distribution of the Decacrema ants.