Sexual mass allocation in species with inflorescences as pollination units: a comparison between Arum italicum and Arisaema (Araceae)

Sex allocation models predict that cosexuality is stabilized by high allocation to attractive structures in pollen-limited species or by high allocation to shared structures that contribute to both genders. High investment in unilateral fixed costs favor the evolution of dioecy or gender change. With these predictions in mind, I studied sexual mass allocation at flowering in the monoecious Arum italicum (Araceae) and compared it with information available for its sex labile relative Arisaema dracontium. In A. italicum, 68% of biomass was allocated to structures believed to be involved in pollinator attraction and capture. This allocation pattern contrasts with that of Arisaema dracontium, in which 70% of biomass was allocated to scape, considered to be a unilateral fixed cost. The importance of attractive structures in A. italicum was further supported by a disproportionate increased allocation, in larger inflorescences, to the appendix (an attractive structure) compared to fertile flowers. In addition, an increase in inflorescence mass involved a disproportionate increase in mass allocation to male, rather than female, flowers. This pattern also contrasts with a size-related gender change from male to female in Arisaema species. These findings were consistent with sex allocation model predictions and shed light on the evolution of sex lability in Arisaema species.     

Modification of phenotypic and functional gender in the monoecious Arum italicum (Araceae)

Other than studies on sex-labile Arisaema species, studies of gender patterns in Araceae are scarce. The modification of phenotypic and functional gender was investigated in three populations of the monoecious Arum italicum Miller. The probability of reproduction and the number of inflorescences produced increased with plant size, and flower number (total, male, staminodes, female, pistillodes) increased with both plant and inflorescence sizes. However, plant and inflorescence sizes were poor predictors of floral sex ratio (female to male flower ratio). In contrast, change in floral sex ratio towards increasing femaleness was found among inflorescences sequentially produced by a plant. This change could not be explained by either a decrease in inflorescence size or a change in the mating environment. Differences in functional gender did not appear to be related to plant size or stage in the flowering period. Instead, different patterns of functional gender were found between plants with different number of inflorescences. Multi-inflorescence plants showed a functional gender around 0.5, while plants with one inflorescence showed a more extreme functional gender (either male, female, or functionally sterile). Sex of flowers in this species did not seem to exhibit a phenotypic trade-off.     

Evidence for stabilising selection acting on flowering time in Arum maculatum (Araceae): the influence of phylogeny on adaptation

The relationship between flowering time and reproductive success was investigated in the fly-pollinated, monoecious perennial herb Arum maculatum L. (Araceae). This species temporarily traps its principle pollinator, a psychodid midge. Probability of fruit set was analysed in relation to early, peak and late periods of the flowering phenology of four British populations between 1992 and 1997. In three out of five cases, plants which flowered during early and late periods were significantly less likely to set fruit. In addition, one population showed a similar relationship for percentage fruit set of individual inflorescences, and seeds from peak-flowering plants were significantly heavier. There was no variation in number of female flowers per inflorescence over the flowering season. Probability of fruit set appears to be mediated by the likelihood of trapping psychodid midges that have previously been trapped and picked up pollen, an unlikely event during early and late flowering periods when few inflorescences are open. The majority of plants in all populations produce only one inflorescence which means that timing of flowering may be crucial to reproductive success. We interpret our findings as evidence that stabilising selection may be acting on some populations and/or during some years. The ultimate cause, however, can be related to the very short (12–18 h) female phase of each inflorescence, a phylogenetically conservative trait within the Araceae. Received: 19 August 1998 / 15 February 1999     

Carotenoid and ultrastructure variations in plastids of Arum italicum Miller fruit during maturation and ripening

The changes in the pigment pattern and composition occurring in the Arum italicum berry during the various steps of maturation (ivory to deep-green stages) and ripening (yellow and red-orange stages) were studied and correlated to the ultrastructural modifications of plastids. Transmission electron microscopy showed that each stage was characterized by a specific plastidial type following the unusual sequence amyloplast-->chloroplast-->chromoplast. Plastidial transitions were accompanied by profound modifications in the pigmental composition, in particular, in the pattern of carotenoids and their precursors. The HPLC analysis of the carotenoids showed that, besides the two usual all-trans metabolic pathways leading to lutein through alpha-carotene and to auroxanthin through beta-carotene, an additional cis-isomeric biosynthetic pathway leading to cis-neoxanthin through cis-beta-carotene exists. During the pre-ripening stages, the three pathways were present even if with qualitative and quantitative variations. When complete ripening was reached, a block occurred at the cyclization level causing the accumulation of both all-trans (i.e. gamma-carotene and neurosporene) and cis-isomer (i.e. lycopene and zeta-carotene) carotene precursors. Because of the occurrence of unusual pigments and the presence of the three main plastidial types, the fruit of A. italicum may constitute a most instructive model for the study of carotenogenesis.     

Reproduction of the West Mediterranean endemic Arum pictum (Araceae) on Corsica

Pollination in the genus Arum appears to be in general a complex deceptive pollination process. The genus Arum is composed of 28 species, all belonging to the subgenus Arum, except A. pictum, the only species of the subgenus Gymnomesium, which is basal and sister to all other Arum species. The aim of this paper is to document the pollination ecology of the insular Arum pictum, the only Arum species to flower in autumn, on the island of Corsica (France). The anthesis cycle of A. pictum occurs during the day, attracting sphaerocerid flies and staphylinid beetles early in the morning and late in the afternoon of the first day. The pollen is released from the anthers early in the morning of the second day before the departure of the insects. Its thermogenic cycle matches the anthesis cycle with an original and unique, bimodal temperature pattern of the appendix (morning and afternoon), contrary to the unimodal pattern found in all other studied Arum species. Data from reproductive success and seed sets suggest that sexual reproduction in this species is limited by pollen (e.g. attracting lured insects) rather than by resources. The biology of this Western Mediterranean species appears to be different from other Western European Arum and close to some Eastern Mediterranean species. Further studies are needed to establish whether Arum pictum represents some ancestral stage or whether its peculiar biological traits are adapted to its insular distribution.     

Predicting the pathway to wind pollination: heritabilities and genetic correlations of inflorescence traits associated with wind pollination in Schiedea salicaria (Caryophyllaceae)

The transition from biotic to abiotic pollination was investigated using Schiedea, a genus exhibiting a remarkable diversity of inflorescence architecture associated with pollination biology. Heritabilities and genetic correlations of inflorescence traits were estimated in gynodioecious Schiedea salicaria (Caryophyllaceae), a species that has likely undergone a recent transition to wind-pollination. Using a partial diallel crossing design, significant narrow-sense heritabilities were detected for inflorescence condensation (h2 = 0.56 to 0.68 in the two sexes) and other traits related to the extent of wind pollination in Schiedea species. Heritabilities were generally higher in hermaphrodites than in females. Strong genetic correlations may constrain the evolution of some inflorescence traits that facilitate wind pollination, such as simultaneous shortening of inflorescence length and elongation of the subtending internode. The presence of significant narrow-sense heritabilities for traits associated with wind pollination suggests, however, that selection for more effective wind pollination in the windy, pollinator-limited environments where S. salicaria grows could lead to the evolution of the highly condensed inflorescences characteristic of other wind-pollinated species of Schiedea.     

Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana

The pollination of Philodendron solimoesense (subgenus Meconostigma) was studied in four populations of French Guiana. Flowering is asynchronous within each population during July, and the flowering cycle is a 2-d process. Numerous insects visit Philodendron inflorescences, but the main pollinator seems to be Cyclocephala colasi (Scarabaeidae, Dynastinae). The pollination process displays aspects typical of beetle pollination: the production of heat and of a strong odor, the presence of a food reward (stigmatic secretion and sterile male flowers), and the presence of a copulation chamber. Flower heat production is important (ca. 11 degrees C above the ambient air) and may help to volatilize the fragrance. Attraction and choice-test experiments showed that C. colasi is not likely to depend on chemical information (such as pheromone) to localize conspecifics but may rely instead on stimuli produced by the inflorescences in order to meet mating partners.     

Regulation of thermogenesis in flowering Araceae: the role of the alternative oxidase

The inflorescences of several members of the Arum lily family warm up during flowering and are able to maintain their temperature at a constant level, relatively independent of the ambient temperature. The heat is generated via a mitochondrial respiratory pathway that is distinct from the cytochrome chain and involves a cyanide-resistant alternative oxidase (AOX). In this paper we have used flux control analysis to investigate the influence of temperature on the rate of respiration through both cytochrome and alternative oxidases in mitochondria isolated from the appendices of intact thermogenic Arum maculatum inflorescences. Results are presented which indicate that at low temperatures, the dehydrogenases are almost in full control of respiration but as the temperature increases flux control shifts to the AOX. On the basis of these results a simple model of thermoregulation is presented that is applicable to all species of thermogenic plants. The model takes into account the temperature characteristics of the separate components of the plant mitochondrial respiratory chain and the control of each process. We propose that 1) in all aroid flowers AOX assumes almost complete control over respiration, 2) the temperature profile of AOX explains the reversed relationship between ambient temperature and respiration in thermoregulating Arum flowers, 3) the thermoregulation process is the same in all species and 4) variations in inflorescence temperatures can easily be explained by variations in AOX protein concentrations.     

Quantitative developmental analysis of homeotic changes in the inflorescence of Philodendron (Araceae)

Background and Aims: The inflorescence of Philodendron constitutes an interestingmorphological model to analyse the phenomenon of homeosis quantitativelyat the floral level. The specific goals of this study were (1)to characterize and quantify the range of homeotic transformationin Philodendron billietiae, and (2) to test the hypothesis thatthe nature of flowers surrounding atypical bisexual flowers(ABFs) channel the morphological potentialities of atypicalbisexual flowers. Methods: Inflorescences of P. billietiae at different stages of developmentwere observed using SEM. The number of appendices in male, femaleand sterile flowers were counted on 11 young inflorescences(5–6 flowers per inflorescence). The number of staminodesand carpels on ABFs were counted on 19 inflorescences (n = 143).These data were used for regression and ANOVA analyses. Results: There was an average of 4·1 stamens per male flower,9·8 carpels per female flower and 6·8 staminodesper sterile male flower. There was an average of 7·3floral appendices per atypical flower. Staminodes and carpelsare inserted on the same whorl in ABFs. A negative exponentialrelationship was found between the average number of staminodesand the number of carpels in ABFs. If only the ABFs consistingof less than six carpels are considered, there is a linear relationshipbetween the number of carpels and the average number of staminodes.The value of the slope of the regression equation indicatesthat on average, in P. billietiae, 1·36 carpels are replacedby one staminode. Conclusions: In P. billietiae, the number of appendages in female flowersimposes a constraint on the maximum total number of appendages(carpels and staminodes) that can develop on ABFs. The quantitativeanalyses indicate that the average number of different typesof floral appendages on an ABF and the number of organs involvedin a homeotic transformation are two independent phenomena.     

Size-dependent flowering behavior and heat production of a sequential hermaphrodite, Symplocarpus renifolius (Araceae)

We examined the flowering performance in a population of the protogynous perennial herb Symplocarpus renifolius (Araceae), with special consideration of plant size. Flowering of S. renifolius occurred in very early spring, soon after snow melt. The spadices generated heat throughout the pistillate (female) and bisexual phases, but heat production decreased quickly after the beginning of the staminate (male) phase. During the flowering season, the sex ratio within the population dramatically changed from a dominance of females to a dominance of males. The duration of the female phase was negatively correlated with the onset time of flowering, and the duration of the male phase was positively correlated with plant size. Larger plants began blooming earlier, produced more heat, made the transition from female to male phase more rapidly, and lasted longer as males than smaller ones. Such size-dependent flowering performance caused unidirectional pollen flow from large to small plants. The number of seeds produced per spadix was positively correlated with the duration of the female phase, although it was not correlated with plant size. However, the estimated number of seeds sired during the male phase was positively correlated with plant size. Early flowering, rapid gender change, and higher heat production of the spadices by larger plants were factors considered to promote the higher success of the male function without decreasing the success of the female function.     

Flowering biology of Aspidistra (Asparagaceae): new data on pollination by dipteran insects

The genus Aspidistra comprises about 160 species of herbaceous plants. In previous investigations, different authors suggested that Aspidistra is pollinated by flies, fungus gnats, slugs, amphipods and even collembolans. The vast majority of data was based on only one species, A. elatior, and was not confirmed by direct observations. Recent field observations of anthetic plants confirm the idea of pollination by flies for two other species of the genus. The present study summarizes direct observations of flowering phenology and pollination of five previously unstudied species of Aspidistra. Flowering biology was studied using visual observations as well as video and photo monitoring. Flowers and captured pollinators were investigated using scanning electron microscopy. As a result, knowledge of the flowering biology of Aspidistra has been increased. The absence of heat production and an ultraviolet pattern were verified. The present data show that flowers of Aspidistra can serve as a food resource for animals. The investigated species of Aspidistra are pollinated by dipteran insects: A. formosa, A. marasmioides and A. subrotata are pollinated by fungus gnats; A. multiflora and A. oviflora are pollinated by flies. The occurrence of fungus‐gnat pollination was directly demonstrated for the first time in the genus Aspidistra. The present study confirmed the idea of myiophily in the genus Aspidistra. Apparently, myiophily is common and diverse in Aspidistra. More likely, pollinators are attracted by scent, which is undetectable by humans, but the attraction mechanism is still not completely clear.     

Beetle pollination and flowering rhythm ofAnnona spp. (Annonaceae) in Brazil

Dynastid scarab beetles are the main or exclusive pollinators ofAnnona spp. with large flowers and wide floral chambers. These nocturnal beetles are attracted by the characteristic odours which are caused by measurable temperature elevation of the flowers up to 10°C or even 15°C above the ambient air temperature. TheAnnona spp. investigated showed different floral rhythms varying from one to three days. The elaborate and wellcoordinated flowering processes, along with floral heating and olfactorial attraction of the night-activeCyclocephala spp., result in a very precise and effective pollination. The floral chamber provides alimentation for the beetles in the form of nutritious food-tissues and pollen and offers a mating place and a well developed shelter against predation and environmental changes. A staggered flowering period and an alternative attraction of different beetle species seems to be more a device for diminishing competition between the cooccurringAnnona spp. than a hybridization barrier.     

Wind pollination, sexual dimorphism, and changes in floral traits of Schiedea (Caryophyllaceae)

Both changes in sex allocation and pollination mode may promote the separation of sexes in plant populations. Simultaneous evolution of wind pollination and dimorphism has occurred in Schiedea, where species with different female frequencies provide an opportunity to observe the effect of wind pollination on sex allocation and floral morphology. Differences among species in the ratio of anther to ovary volume were not the result of sex allocation trade-offs, but instead resulted from production of vestigial stamens in females; there were no changes in ovary volume in males and hermaphrodites (MH) of dimorphic species. Relative to hermaphroditic species, dimorphic species had more condensed inflorescences, a pattern often associated with wind pollination. Within dimorphic species, MH had longer filament lengths than females, and females had longer stigmas than MHs. These traits are characteristic of wind pollination, but there was no relationship between the degree of sexual dimorphism and female frequency. Ovary volume and ovule number and size had positive phenotypic correlations between females and MH of dimorphic species, making sex specialization more difficult. In dimorphic Schiedea species, selection for wind pollination may have a greater effect on floral traits than trade-offs in allocation between male and female function.     

Rainfall and flowering synchrony in a tropical shrub: Variable selection on the flowering time ofErythroxylum havanense

Summary We tested the adaptive significance of flowering synchrony by means of a quantitative analysis of selection and by flowering induction experiments with the deciduous shrubErythroxylum havanense. Temporal schedules of flower and fruit production were determined for a local population (in three sites) in a Mexican seasonal forest for 2 years (1987–1988). The consequences of natural variation in flowering time (flowering initiation day) on maternal reproductive success (fecundity) were evaluated. We observed high levels of inter- and intraindividual flowering synchrony in 1987, but not in 1988 and this contrast was related to differences in rainfall patterns between the two years. A significant proportion (15.4%) of the phenotypic variation in flowering initiation day was accounted for by environmental variance. The expression of phenotypic variance of flowering time and, consequently, the opportunity for selection to act, are controlled by annual variation in rainfall. Despite the between-year difference in flowering synchrony, we detected a relatively intense directional selection on flowering initiation day in both years, but selection coefficients were of opposite sign (standardized directional gradients were –0.326 and 0.333 for 1987 and 1988, respectively). For both years there was a significant relationship between individual relative fitness and the number of neighbouring flowering plants in a given day, suggesting positive frequency-dependent selection.     

Structure and dynamics of pollination networks: the role of alien plants

Research on ecological communities, and plant–pollinator mutualistic networks in particular, has increasingly benefited from the theory and tools of complexity science. Nevertheless, up to now there have been few attempts to investigate the interplay between the structure of real pollination networks and their dynamics. This study is one of the first contributions to explore this issue. Biological invasions, of major concern for conservation, are also poorly understood from the perspective of complex ecological networks. In this paper we assess the role that established alien species play within a host community by analyzing the temporal changes in structural network properties driven by the removal of non‐native plants. Three topological measures have been used to represent the most relevant structural properties for the stability of ecological networks: degree distribution, nestedness, and modularity. Therefore, we investigate for a detailed pollination network, 1) how its dynamics, represented as changes in species abundances, affect the evolution of its structure, 2) how topology relates to dynamics focusing on long‐term species persistence; and 3) how both structure and dynamics are affected by the removal of alien plant species. Network dynamics were simulated by means of a stochastic metacommunity model. Our results showed that established alien plants are important for the persistence of the pollination network and for the maintenance of its structure. Removal of alien plants decreased the likelihood of species persistence. On the other hand, both the full network and the subset native network tended to lose their structure through time. Nevertheless, the structure of the full network was better preserved than the structure of the network without alien plants. Temporal topological shifts were evident in terms of degree distribution, nestedness, and modularity. However the effects of removing alien plants were more pronounced for degree distribution and modularity of the network. Therefore, elimination of alien plants affected the evolution of the architecture of the interaction web, which was closely related to the higher species loss found in the network where alien plants were removed.     

Infrared thermography and odour composition of the Amorphophallus gigas (Araceae) inflorescence: the cooling effect of the odorous liquid

During the second blooming of a cultivated Amorphophallus gigas Teijsm and Binnend in the Botanical Gardens of the University of Tokyo, the surface temperature of the inflorescence was measured using an infrared camera. Contrary to studies of other species in the genus Amorphophallus, the surface of the inflorescence showed only very faint thermogenesis and had a lower temperature than that of the background. This cooling effect appeared to be due to a loss of heat through evaporation, which was caused by the secretion of a very large amount of odorous liquid. Chemical analysis revealed that the major components of this liquid were acetic acid, propionic acid, butyric acid and valeric acids. The composition of the odorous liquid was slightly different between the spathe surface and the sterile appendix. The major component(s) of the odorous material from the spathe was butyric acid, and from the sterile appendix was valeric acids. These components would play dual roles of adding the characteristic smell to the inflorescence and cooling the inflorescence.     

Ecological context of breeding system variation: sex, size and pollination in a (predominantly) gynodioecious shrub

BACKGROUND AND AIMS: Species that exhibit among-population variation in breeding system are particularly suitable to study the importance of the ecological context for the stability and evolution of gender polymorphism. Geographical variation in breeding system and sex ratio of Daphne laureola (Thymelaeaceae) was examined and their association with environmental conditions, plant and floral display sizes, and pollination environment in a broad geographic scale was analysed. METHODS: The proportion of female and hermaphrodite individuals in 38 populations within the Iberian Peninsula was scored. Average local temperature and precipitation from these sites were obtained from interpolation models based on 30 years of data. Pollination success was estimated as stigmatic pollen loads, pollen tubes per ovule and the proportion of unfertilized flowers per individual in a sub-set of hermaphroditic and gynodioecious populations. KEY RESULTS: Daphne laureola is predominantly gynodioecious, but hermaphroditic populations were found in northeastern and southwestern regions, characterized by higher temperatures and lower annual precipitation. In the gynodioecious populations, female plants were larger and bore more flowers than hermaphrodites. However, due to their lower pollination success, females did not consistently produce more seeds than hermaphrodites, which tends to negate a seed production advantage in D. laureola females. In the northeastern hermaphroditic populations, plants were smaller and produced 9-13 times fewer flowers than in the other Iberian regions, and thus presumably had a lower level of geitonogamous self-fertilization. However, in a few southern populations hermaphroditism was not associated with small plant size and low flower production. CONCLUSIONS: The findings highlight that different mechanisms, including abiotic conditions and pollinator service, may account for breeding system variation within a species' distribution range and also suggest that geitonogamy may affect plant breeding system evolution.     

Purification and partial characterization of two biologically active compounds from the inflorescence of Sauromatum guttatum Schott (Araceae)

The active principle triggering the metabolic outburst of theappendices of certain arum lily species has been purified andpartially characterized. Although in the past it has been thoughtof as a single factor ("calorigen"), both paper chromatographyand DEAE-Sephadex ion exchange chromatography reveal that thereare two compounds (calorigen I and II) with calorigen activity.These can act alone or together, but show no synergism. Theyare low-molecular compounds which appear to be common constituentsof the inflorescence of Sauromatum guttatum Schott. CalorigenII is also present in the spadix of Arum maculatum L., Arumdioscoridis Sibth. & Sm., and Dracunculus vulgaris Schott.Calorigen I absorbs UV at 242, 267 and 278 nm, calorigen IIat 229 and 295 nm. No spectral changes are noted in alkalineenvironment, whereas at low pH-values there is a shift of theabsorption peaks of both compounds towards longer wavelengths.Calorigen II displays a strong blue fluorescence and has a maximalemission at 410 nm when activated at 295 nm. The possible mechanismof calorigen action is discussed. ¹ Present address: Department of Biochemistry, University ofWashington, Seattle, Washington 98195, U.S.A. (Received August 26, 1974; )     

Beetle pollination of Shorea parvifolia (section Mutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia

Pollination ecology of an emergent tree species, Shorea (section Mutica) parvifolia (Dipterocarpaceae), was studied using the canopy observation system in a lowland dipterocarp forest in Sarawak, Malaysia, during a general flowering period in 1996. Although the species has been reported to be pollinated by thrips in Peninsular Malaysia, our observations of flower visitors and pollination experiments indicated that beetles (Chrysomelidae and Curculionidae, Coleoptera) contributed to pollination of S. parvifolia in Sarawak. Beetles accounted for 74% of the flower visitors collected by net-sweeping, and 30% of the beetles carried pollen, while thrips accounted for 16% of the visitors, and 12% of the thrips carried pollen. The apical parts of the petals and pollen served as a reward for the beetles. Thrips stayed inside the flower almost continuously after arrival, and movements among flowers were rare. Fruit set was significantly increased by introduction of beetles to bagged flowers, but not by introduction of thrips. Hand-pollination experiments and comparison of fruit set in untreated, bagged, and open flowers suggested that S. parvifolia was mainly outbreeding.