The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.     

Fig wasp dispersal and the stability of a keystone plant resource in Borneo

The stability of interactions in remaining rainforest fragments is an issue of considerable concern for conservation. Figs are a pre-eminent tropical keystone resource because of their importance for wildlife, but are dependent on tiny (1-2 mm) species-specific wasps for pollination. To investigate fig wasp dispersal I trapped insects at various heights (5-75 m) in an isolated fragment (ca. 4500 ha) of Bornean rain forest. Fig wasps constituted the majority of captures above the canopy (pollinators 47%, non-pollinators 5%). However, genera were not evenly represented. There were 50% more species of monoecious fig pollinator than there were host species in the fragment, indicating some must have arrived from forests with different assemblages of figs at least 30 km away. Dioecious fig pollinators were poorly represented suggesting more limited dispersal, which could account for higher endemism and vulnerability to catastrophic disturbance in these figs. Diurnal activity and flight height also varied among genera. Most non-pollinating fig wasps were very rare.     

Direct costs of forest reproduction,bee-cycling and the efficiency of pollination modes

The bee guild represents direct primary costs of angiosperm reproduction. Tropical flower visitors take an amount comparable to herbivores, exceeding 3% of net primary production energy. Therefore herbivory and aboveground net primary production have been underestimated. Comparing pollinators to other herbivores, harvest in mature forest by tropical bees is greater than leafcutter ants, game animals, frugivores, vertebrate folivores, insect defoliators excluding ants, flower-feeding birds and bats, but not soil organisms. The ratio of total aboveground net primary production to investment in pollen, nectar and resin used by pollinators suggests wind pollination is several times more efficient in temperate forests than is animal pollination in neotropical moist forest. Animal pollination may be favoured by habitat mosaics and an unpredictable or sparse dispersion of conspecifics — consequences of fluctuating abiotic and biotic environments. Natural selection evidently favours diminished direct reproductive costs in forests, for example by wind pollination, regardless of latitude and disturbance regime. An example is “wind pollination by proxy” of dominant trees in seasonal southeast Asian forests. They flower only occasionally and their pollen is dispersed by tiny winged insects that are primarily carried by the wind — rather than the nectar-hungry bees, bats, birds and moths used by most tropical flora. Increasing evapotranspiration is associated with greater net primary production; I show its correlation with species richness of social tropical bees across the isthmus of Panama, which may indicate increasing forest reproductive effort devoted to flowering, and its monopolization by unspecialized flower visitors in wetter and less seasonal lowland forests.     

Pollen and seed dispersal among dispersed plants

The ecological significance of spacing among plants in contributing to the maintenance of species richness, particularly in tropical forests, has received considerable attention that has largely focussed on distance- and density-dependent seed and seedling mortality. More recently it has become apparent that plant spacing is also relevant to pollination, which often constrains seed production. While seed and seedling survival is reduced at high conspecific densities, pollination success, by contrast, is positively correlated to local conspecific density. Distance-dependent mechanisms acting on pollination and seed production have now been described for a variety of plants, with relatively isolated plants or fragmented populations generally suffering reduced fecundity due to pollen limitation. Yet there is considerable variability in the vulnerability of plant species to pollination failure, which may be a function of breeding system, life history, the pollination vector, the degree of specialisation among plants and their pollinators, and other indirect effects of habitat change acting on plants or pollinators. As reduced tree densities and population fragmentation are common outcomes of anthropogenically altered landscapes, understanding how pollination processes are affected in such degraded landscapes can inform effective conservation and management of remaining natural areas.     

Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology

The obligate mutualism between pollinating fig wasps in the family Agaonidae (Hymenoptera: Chalcidoidea) and Ficus species (Moraceae) is often regarded as an example of co-evolution but little is known about the history of the interaction, and understanding the origin of functionally dioecious fig pollination has been especially difficult. The phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus were inferred from mitochondrial cytochrome oxidase gene sequences (mtDNA) and morphology. Separate and combined analyses indicated that the pollinators of functionally dioecious figs are not monophyletic. However, pollinator relationships were generally congruent with host phylogeny and support a revised classification of Ficus. Ancestral changes in pollinator ovipositor length also correlated with changes in fig breeding systems. In particular, the relative elongation of the ovipositor was associated with the repeated loss of functionally dioecious pollination. The concerted evolution of interacting morphologies may bias estimates of phylogeny based on female head characters, but homoplasy is not so strong in other morphological traits. The lesser phylogenetic utility of morphology than of mtDNA is not due to rampant convergence in morphology but rather to the greater number of potentially informative characters in DNA sequence data; patterns of nucleotide substitution also limit the utility of mtDNA findings. Nonetheless, inferring the ancestral associations of fig pollinators from the best-supported phylogeny provided strong evidence of host conservatism in this highly specialized mutualism.     

Pollination and breeding systems of woody plant species in tropical dry evergreen forests,southern India

Tropical dry evergreen forests (TDEF) are a unique forest type found along the east coast of India. They mostly occur as small, isolated fragments of varying sizes (0.5 to ≈10 ha) and are considered as endangered forests types in peninsular India. Although plant diversity is well documented in these forests, there is a paucity of ecological studies vital for conservation and for planning restoration activities. We studied reproductive biology of 13 woody species: four trees, six shrubs, and three lianas in fragments of TDEF in southern India. The phenology of reproduction, floral biology, anthesis and sexual system of each species were recorded. The pollination mode was assessed through observations of the visitation frequency of pollinators and from the floral characters. The breeding system was determined by hand-augmented self- and cross-pollination experiments. The plants flowered during the dry season from January to July. Plants of nine species had both flowers and fruits at the same time. Twelve species were hermaphrodites and one was polygamo-dioecious. Flowers of 11 species opened at dawn and two at dusk. Four species were self-incompatible and six were self-compatible. Natural fruit set ranged from 10% to 56%, self-incompatible species having low fruit set. Cross-pollen augmentation increased fruit set, suggesting presence of outcrossing in all species. The majority of plants species (85%) had a generalized pollination system, receiving visits from diverse insects, such as social bees, solitary bees, wasps, moths and flies. However, only few of them were functionally important for the species. Two species namely: Capparis brevispina and C. zeylanica had butterflies and birds, respectively, as their main pollinators. Our data reveal that there is a predominance of outcrossing in plant species and a generalized pollination system in these forests. We suggest that restoration of TDEFs is crucial as habitats, not only for wild plants but also for pollinating insects.     

How to be an ant on figs

Mutualistic interactions are open to exploitation by one or other of the partners and a diversity of other organisms, and hence are best understood as being embedded in a complex network of biotic interactions. Figs participate in an obligate mutualism in that figs are dependent on agaonid fig wasps for pollination and the wasps are dependent on fig ovules for brood sites. Ants are common insect predators and abundant in tropical forests. Ants have been recorded on approximately 11% of fig species, including all six subgenera, and often affect the fig–fig pollinator interaction through their predation of either pollinating and parasitic wasps. On monoecious figs, ants are often associated with hemipterans, whereas in dioecious figs ants predominantly prey on fig wasps. A few fig species are true myrmecophytes, with domatia or food rewards for ants, and in at least one species this is linked to predation of parasitic fig wasps. Ants also play a role in dispersal of fig seeds and may be particularly important for hemi-epiphytic species, which require high quality establishment microsites in the canopy. The intersection between the fig–fig pollinator and ant–plant systems promises to provide fertile ground for understanding mutualistic interactions within the context of complex interaction networks.     

Sexual Systems and Ecological Correlates in an Azonal Tropical Forests, SW China

Unlike the seriate lowland rain forests in SE Asia, the tropical vegetation of Xishuangbanna (SW China) has developed in habitats with comparatively lower temperatures and precipitation. Consequently, although most of the families and genera of the flora are components of tropical ecosystems, many have reached their distribution limits in latitude. Selection pressures on sexual systems in these environments may be different from that experienced in lowland tropical regions. Here, we examine the sexual systems of 685 species of flowering plants belonging to 109 families and 356 genera based on 42 plots with a total area of 15.4 ha and compare our results with surveys of sexual systems from other tropical ecosystems. Among these species, 60.6 percent were hermaphroditic, 14.3 percent were monoecious, and 25.1 percent were dioecious. The percentage of dioecious sexual system among tree species (26.1%) was similar or higher than that of other tropical tree floras. Monoecy was significantly associated with the tree growth form and was relatively common in seasonal forest vegetation. Sexual systems involving unisexual flowers (dicliny) are particularly well represented in the tropical forests of Xishuangbanna accounting for 39.4 percent of all species surveyed. This pattern may be associated with the prevalence of relatively small inconspicuous flowers in the tropical forests of SE Asia and their correlation with diclinous sexual systems generally.     

Pollination and parasitism in functionally dioecious figs

Fig wasps (Agaonidae: Hymenoptera) are seed predators and their interactions with Ficus species (Moraceae) range from mutualism to parasitism. Recently considerable attention has been paid to conflicts of interest between the mutualists and how they are resolved in monoecious fig species. However, despite the fact that different conflicts can arise, little is known about the factors that influence the persistence of the mutualism in functionally dioecious Ficus. We studied the fig pollinator mutualism in 14 functionally dioecious fig species and one monoecious species from tropical lowland rainforests near Madang, Papua New Guinea. Observations and experiments suggest that (i) pollinating wasps are monophagous and attracted to a particular host species; (ii) pollinating and non-pollinating wasps are equally attracted to gall (male) figs and seed (female) figs in functionally dioecious species; (iii) differing style lengths between gall figs and seed figs may explain why pollinators do not develop in the latter; (iv) negative density dependence may stabilize the interaction between pollinating wasps and their parasitoids; and (v) seed figs may reduce the search efficiency of non-pollinators. This increased pollinator production without a corresponding decrease in seed production could provide an advantage for dioecy in conditions where pollinators are limiting.     

Reproductive biology of Hechtia schottii, a dioecious Bromeliaceae, in Mexico

Hechtia schottii is a terrestrial, rosetofilous, dioecious, polycarpic succulent herb, that grows mainly in shrubby associations, and less frequently, in secondary low caducifolious forests, both on calcareous soils or limestone outcrops in Yucatan and Campeche States, Mexico. We studied phenology, floral and pollination biology, and breeding system at Calcehtok, Yucatan, during two flowering seasons. Plants bloom mainly during the dry season (November-April) and disperse seeds during the rainy season (May-October). Both floral morphs have diurnal anthesis; pollen is removed ca. 1 h after anthesis starts and both floral morphs are visited by several insect species, especially bees, but results suggest that the introduced honey bee, Apis mellifera, is the pollinator. Controlled crossings show that the species is functionally dioecious and requires to be serviced by pollinators based on fruit setting only in unassisted cross pollination crosses.     

Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig–fig wasp interaction

Like other mutualisms, pollination mutualisms attract parasites, as well as opportunistic and specialist predators of the pollinators and parasites. These associated species influence the evolutionary dynamics of pairwise mutualisms. Predatory ants are frequent associates of pollination mutualisms, but their effects on the complex interactions between plants, pollinators and parasites have not yet been clearly established, even in the case of the well-described obligate interaction between figs and fig wasps. We attempted to quantify such effects for ants associated with three fig species, two dioecious ( Ficus condensa [Bruneï], F . carica [France]) and one monoecious ( F . racemosa [India]). In all these cases, ant presence on a fig tree strongly reduced the number of parasitic wasps on the figs. Experimental exclusion of ants resulted in an increase in the number of non-pollinating fig wasps on F . condensa and F . racemosa . Experimental ant supplementation led to a decrease in the number of non-pollinating fig wasps on F . carica . Moreover, on F . condensa , the level of reduction of the number of parasitic wasps depended on the number and identity of the ants. On F . carica , non-pollinating fig wasps even avoided trees occupied by the dominant predatory ant. The consistency of the effect of ants in these three cases, representing a geographically, ecologically, and taxonomically broad sample of figs, argues for the generality of the effect we observed. Because reduction of parasitism benefits the pollinator, ants may be considered as indirect mutualists of plants and pollinators in the network of complex interactions supported by fig trees.     

Bimodal Pollination by Wasps and Beetles in the African Milkweed Xysmalobium undulatum

It has been suggested that flowers of some plants are specialized for pollination by two unrelated species (or functional groups) of pollinators. However, evidence for 'bimodal pollination systems' has been extremely limited. Studies of the milkweed Xysmalobium undulatum in South Africa showed that its flowers are visited by a range of different insects (representing 18 families), but only two groups, represented by the chafer beetle Atrichelaphinis tigrina and pompilid wasps in the genus Hemipepsis , effect pollination. Experiments showed that both these pollinator groups are effective in removing and inserting pollinia. Pollinia are attached to clypeal hairs and mouthparts on the wasps and tarsal hairs and spines on the beetles. Although considerably less abundant than the beetles, Hemipepsis spp. wasps move more quickly among flowers and appeared to be more effective pollinators overall. Experimental hand-pollinations conducted in the field showed that X. undulatum is genetically self-incompatible and thus completely reliant on pollinators for reproduction. We conclude that X. undulatum has a bimodal pollination system, specialized for pollination by Hemipepsis pompilid wasps and the chafer beetle A. tigrina .     

Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae)

The flowers and inflorescences of animal-pollinated dioecious plants are generally small and inconspicuous in comparison with outcrossing cosexual species. The net benefits of an attractive floral display may be different for dioecious compared to cosexual populations because dioecious species experience a more severe reduction in pollen delivery when pollinators forage longer on fewer individuals. Here, we develop a model that predicts the decrease in pollen delivery in dioecious relative to cosexual populations from female-female, female-male and male-male visit sequences as the number of individuals visited varies. To evaluate the predictions of our model we conducted a common garden experiment with dioecious and monoecious (cosexual) arrays of the insect-pollinated herb Sagittaria latifolia. We find that, although increasing the advertisements of floral rewards (i.e. increasing floral display) attracts more pollinators to individuals, the probability that these pollinators subsequently deliver pollen to neighbouring plants depends on sexual system. Because the number of individual plants visited per foraging trip did not increase significantly with floral display, the relative pollination success of dioecious versus monoecious populations decreases with increased floral display. We propose that this could explain why dioecy is strongly correlated with reduced floral display among angiosperm species.     

REPRODUCTIVE BIOLOGY OF A TROPICAL PALM SWAMP COMMUNITY IN THE VENEZUELAN LLANOS

The reproductive biology of a tropical palm swamp community, called morichal in the Venezuelan Central Llanos, was studied. Of the 128 woody and herbaceous species of plants recorded, 99 (77.34%) were hermaphrodites, 25 (19.53%) were monoecious, and four (3.13%) were dioecious. The morichal is characterized by a low number of species with obligate cross-fertilization. The frequencies of species with different breeding systems in a subsample of 26 species showed that eight (30.77%) were self-incompatible, 14 (53.85%) were self-compatible, and four (15.38%) were agamospermous. Ten of 14 self-compatible species were autogamous. Regardless of the self-incompatibility level estimated, seed and fruit set were greater in self-fertilized flowers than in hand-pollinated flowers in three of the nine self-incompatible species. These results are related to the facts that: 1) the relative isolation of the plant population limits the gene flow among similar communities and enforces the intrapopulation pollen flow; 2) the overlapping flowering patterns and infrequent and unspecialized pollinators may be enforcing self-compatibility and agamospermy; 3) self-compatibility is the rule among short-lived species in the morichal; and 4) three out of four agamospermous species are of the Melastomataceae family.     

A quantitative review of pollination syndromes: do floral traits predict effective pollinators?

The idea of pollination syndromes has been largely discussed but no formal quantitative evaluation has yet been conducted across angiosperms. We present the first systematic review of pollination syndromes that quantitatively tests whether the most effective pollinators for a species can be inferred from suites of floral traits for 417 plant species. Our results support the syndrome concept, indicating that convergent floral evolution is driven by adaptation to the most effective pollinator group. The predictability of pollination syndromes is greater in pollinator‐dependent species and in plants from tropical regions. Many plant species also have secondary pollinators that generally correspond to the ancestral pollinators documented in evolutionary studies. We discuss the utility and limitations of pollination syndromes and the role of secondary pollinators to understand floral ecology and evolution.     

Why do fig wasps actively pollinate monoecious figs?

Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.     

A test for Allee effects in the self‐incompatible wasp‐pollinated milkweed Gomphocarpus physocarpus

It has been suggested that plants that are good colonizers will generally have either an ability to self‐fertilize or a generalist pollination system. This prediction is based on the idea that these reproductive traits should confer resistance to Allee effects in founder populations and was tested using Gomphocarpus physocarpus (Asclepiadoideae: Apocynaceae), a species native to South Africa that is invasive in other parts of the world. We found no significant relationships between the size of G. physocarpus populations and various measures of pollination success (pollen deposition, pollen removal and pollen transfer efficiency) and fruit set. A breeding system experiment showed that plants in a South African population are genetically self‐incompatible and thus obligate outcrossers. Outcrossing is further enhanced by mechanical reconfiguration of removed pollinaria before the pollinia can be deposited. Self‐pollination is reduced when such reconfiguration exceeds the average duration of pollinator visits to a plant. Observations suggest that a wide variety of wasp species in the genera Belonogaster and Polistes (Vespidae) are the primary pollinators. We conclude that efficient pollination of plants in small founding populations, resulting from their generalist wasp‐pollination system, contributes in part to the colonizing success of G. physocarpus. The presence of similar wasps in other parts of the world has evidently facilitated the expansion of the range of this milkweed.     

Reproductive biology of a hummingbird‐pollinated Billbergia: light influence on pollinator behaviour and specificity in a Brazilian semi‐deciduous forest

• Ornithophily has evolved in parallel several times during evolution of angiosperms. Bird pollination is reported for 65 families, including Bromeliaceae. One of the most diverse bromeliad is Billbergia, which comprises species pollinated mainly by hummingbirds.
• Based on investigations on flowering phenology, morpho‐anatomy, volume and concentration of nectar, pollinators and breeding system, this paper explores the reproductive biology and pollinator specificity of B. distachia in a mesophytic semi‐deciduous forest of southeastern Brazil.
• The results have show that B. distachia is pollinated by a single species of hermit hummingbird, Phaethornis eurynome, which search for nectar produced by a septal nectary, where the secretory tissue is located above the placenta. The species is self‐incompatible. The combination of pollinator specificity, due to long corolla tubes that exclude visitation of short‐billed hummingbirds, complete self‐incompatibility and non‐territorial behaviour of pollinators, it is very important to reduce pollen loss and increase gene flow within population.
• Our results indicate that studies on pollination biology and reproduction are essential to understand the evolutionary history of pollination systems of plants since, at least in Billbergia, variation in the pollinator spectrum has been recorded for different habitats among Brazilian forests. Furthermore, according to our data, foraging of Phaethornis on flowers is independent of air temperature and humidity, while the main factor influencing hummingbird visitation is daylight. Considering current knowledge on climatic parameters influencing hummingbird foraging, pollination and reproductive biology of Neotropical flora and environment of the hermit hummingbird in tropical forests, new insights on plant–pollinator interaction are provided.

     

Phenological diversity in tropical forests

One of the most intriguing and complex characteristics of reproductive phenology in tropical forests is high diversity within and among forests. To understand such diversity, Newstrom et al. provided a systematic framework for the classification of tropical flowering phenology. They adopted frequency and regularity as criteria with priority, and classified plants in La Selva, Costa Rica, where most plants reproduced more than once a year irregularly. Many other studies have demonstrated annual cycles corresponding to rainfall patterns at the community level in Neotropical forests, including La Selva. On the other hand, supraannual flowering synchronized among various plant species, called general flowering, is known from aseasonal lowland dipterocarp forests in Southeast Asia. Within both forests, a wide spectrum of flowering patterns is found. This range of patterns suggests the great potential of tropical phenological studies to explore the selective pressures on phenology. Various abiotic and biotic factors can be selective agents. The shared pollinators hypothesis suggests that plant species sharing pollinators segregate flowering temporarily to minimize interspecific overlap in flowering times and thus minimize ineffective pollination or competition for pollinators, indicating strong phylogenetic constraints in timing and variation of flowering. Comparison of phenology within and among forests may help our understanding of phenological diversity. Attempts are now being made to develop a common language to communicate concepts and render interpretations of data more compatible among investigators and to create a network to promote comparative studies. Received: September 8, 2000 / Accepted: January 30, 2001