Optimal resource allocation model for excessive flower production in a pollinating seed-predator mutualism

Many plants produce excessive flowers and several hypotheses have been proposed for adaptive significances of this behavior. Here, I develop a simple resource allocation model for plants in a mutualism with pollinating seed-predators to examine a novel hypothesis that excessive flower production can be favored to “dilute” seed predation by the pollinators. Pollinators visit flowers to deposit pollen and oviposit on them, and their offspring feed on a portion of the seeds, leaving the remainder intact. Further pollinator visits increase seed mortality by over-oviposition. Excessive flower production is favored if it decreases pollinator-visit frequency per flower, while it incurs decrease in seed production because of the resource trade-off. I examine three plant strategies: (1) no abortion, the plant allocates resource to all pollinated flowers to mature; (2) selective abortion, the plant aborts flowers depending on how many times they were visited by pollinators; and (3) random abortion, the plant indiscriminately aborts a fraction of pollinated flowers irrespective of how many times they were visited. I show that the random abortion strategy can perform much more effectively than the no-abortion strategy when the amount of resource is small, the production cost per flower is low, and the pollinator density is high, although the selective abortion strategy is always the best. This “predator dilution” effect has not been considered with regard to previous excessive flower production hypotheses.     

Benefits and costs of mutualism: demographic consequences in a pollinating seed-consumer interaction

Interspecific interactions can affect population dynamics and the evolution of species traits by altering demographic rates such as reproduction and survival. The influence of mutualism on population processes is thought to depend on both the benefits and costs of the interaction. However, few studies have explicitly quantified both benefits and costs in terms of demographic rates; furthermore there has been little consideration as to how benefits and costs depend on the demographic effects of factors extrinsic to the interaction. I studied how benefits (pollination) and costs (larval fruit consumption) of pollinating seed-consumers (senita moths) affect the reproduction of senita cacti and how these effects may rely on extrinsic water limitation for reproduction. Fruit initiation was not limited by moth pollination, but survival of initiated fruit increased when moth eggs were removed from flowers. Watered cacti produced more flowers and initiated more fruit from hand-pollinated flowers than did unwatered cacti, but fruit initiation remained low despite excess pollen. Even though water, pollination and larvae each affected a component of cactus reproduction, when all of these factors were included in a factorial experiment, pollination and water determined rates of reproduction. Counter-intuitively, larval fruit consumption had a negligible effect on cactus reproduction. By quantifying both benefits and costs of mutualism in terms of demographic rates, this study demonstrates that benefits and costs can be differentially influential to population processes and that interpretation of their influences can depend on demographic effects of factors extrinsic to the interaction.     

Body size in a pollinating fig wasp and implications for stability in a fig‐pollinator mutualism

The fig–fig pollinator association is a classic case of an obligate mutualism. Fig‐pollinating wasps often have to fly long distances from their natal syconia to a receptive syconium and then must enter the narrow ostiole of the syconium to reproduce. Large wasps are expected to have a greater chance of reaching a receptive syconium. In this study, we tested this hypothesis and then examined whether the ostiole selectively prevented larger pollinators from entering the syconial cavity. In Xishuangbanna, China, Ceratosolen solmsi marchali Mayr (Hymenoptera: Agaonidae) pollinates the dioecious syconia of Ficus hispida L. (Moraceae). The body size of newly emerged wasps and wasps arriving at receptive syconia were compared. Wasps arriving at receptive syconia were significantly larger than newly emerged wasps. We also compared the size of wasps trapped in the ostiole with those in the cavity. Wasps trapped in the ostiole were significantly larger than those in the syconial cavity. Thus, in the case of F. hispida, large wasps were more likely to reach receptive syconia, but the ostiole limited maximum fig wasp size. This indicates that the ostiole, as a selective filter to pollinators, stabilizes pollinator size. Hence, it helps to maintain stability in the fig–fig pollinator mutualism.     

Longevity, early emergence and body size in a pollinating fig wasp--implications for stability in a fig-pollinator mutualism

1. Fig trees (Ficus) are pollinated only by agaonid wasps, whose larvae also gall fig ovules. Each ovule develops into either a seed (when pollinated) or a wasp (when an egg is also laid inside) but not both. 2. Ovipositing wasps (foundresses) favour ovules near the centre of the enclosed inflorescence (syconium or 'fig'), leaving ovules near the outer wall to develop into seeds. This spatial stratification of wasps and seeds ensures reproduction in both partners, and thereby enables mutualism persistence. However, the mechanism(s) responsible remain(s) unknown. 3. Theory shows that foundresses will search for increasingly rare inner ovules and ignore outer ovules, as long as ovipositing in outer ovules is sufficiently slow and/or if inner ovules confer greater fitness to wasps. The fig-pollinator mutualism can therefore be stabilized by strong time constraints on foundresses and by offspring fitness gradients over variation in ovule position. 4. Female fig wasps cannot leave their galls without male assistance. We found that females in outer ovules were unlikely to be released. Inner ovules thus have added value to foundresses, because their female offspring are more likely to mate and disperse. 5. For those offspring that did emerge, gall position (inner/outer) and body size did not influence the order in which female pollinators exited syconia, nor did early emerging wasps enjoy increased life spans. 6. We also found that the life spans of female wasps nearly doubled when given access to moisture. We suggest that conflict resolution in the fig-pollinator mutualism may thus be influenced by tropical seasonality, because wasps may be less able to over-exploit ovules in dry periods due to time constraints.     

Yeasts associated with pollinating bees and flower nectar

A study of the yeast flora of 328 honey stomachs from 7 different pollinating bee species, and 342 flower nectar samples of 9 different flower species yielded 766 yeast isolates composed of 16 genera and 47 species. Most of the yeast species from both the sources belonged to the genusCandida, while the most frequently isolated yeasts wereDekkera intermedia from honey stomach andCandida blankii from flower nectar. Among the honey bees,Xylocopa sp., and among flowers,Citrus medica, yielded the highest number of yeast species. Nineteen species of yeasts belonging to 9 genera were common to both the sources.     

Sex and pollen: the role of males in stabilising a plant-seed eater pollinating mutualism

Some plants are exclusively pollinated by an insect whose larvae feed on their seeds. The net outcome of a single visit for the plant depends on the number of ovules fertilised by the visitor, the number of eggs laid, and the number of seeds eaten by each larva. Unlike other known plant-seed eater pollinating mutualisms, the globeflower-globeflower fly mutualism (Trollius europaeus-Chiastocheta spp.) is unique in that not only females but also males visit flowers, and both sexes are potential pollinators. I analysed the relative efficiency of Chiastocheta males versus females in transporting pollen and fertilising globeflower ovules. I show that there is no sex-specific morphological adaptation or behaviour to enhance pollen collection and transportation in Chiastocheta flies, and that males contribute to pollination. However, because of their smaller body size, males transport significantly less pollen than females. Less seeds are produced after a visit from a male than after a visit from a female. A single female visit contributes to about 12% of total seed production, and a single male visit to only 5.4%. Females tend to spend more time inside the flower than males, and the number of ovules fertilised is significantly correlated with the time insects spent inside the closed corolla. The lower efficiency of ovule fertilisation by a male's single visit is compensated for by the higher rate of flower visitation by males: a flower receives about twice as many visits from males as from females during a time unit. The contribution of males to pollination is of major importance with respect to understanding the evolutionary stability of the globeflower-globeflower fly mutualism, as males satiate pollen requirement of flowers, masking the antagonistic effect of ovipositing females.     

Testing hypotheses for genealogical discordance in a rainforest lizard

Genealogical discordance, or when different genes tell distinct stories although they evolved under a shared history, often emerges from either coalescent stochasticity or introgression. In this study, we present a strong case of mito‐nuclear genealogical discordance in the Australian rainforest lizard species complex of Saproscincus basiliscus and S. lewisi. One of the lineages that comprises this complex, the Southern S. basiliscus lineage, is deeply divergent at the mitochondrial genome but shows markedly less divergence at the nuclear genome. By placing our results in a comparative context and reconstructing the lineages' demography via multilocus and coalescent‐based approximate Bayesian computation methods, we test hypotheses for how coalescent variance and introgression contribute to this pattern. These analyses suggest that the observed genealogical discordance likely results from introgression. Further, to generate such strong discordance, introgression probably acted in concert with other factors promoting asymmetric gene flow between the mitochondrial and nuclear genomes, such as selection or sex‐biased dispersal. This study offers a framework for testing sources of genealogical discordance and suggests that historical introgression can be an important force shaping the genetic diversity of species and their populations.     

Can andromonoecy explain low fruit : flower ratios in the Proteaceae?

There are several possible explanations for the low fruit: flower ratios commonly observed in the Australian Proteaceae—some proximate and others ultimate. One of these, namely that some flowers on a plant are functionally male (andromonoecy), has recently received considerable attention. However, the term andromonoecy appears to have been misused in the pollination ecology literature. In this note, we clarify the use of the terms andromonoecy and androgyny, and suggest that they should be applied with care, only after it is clear that the flowers lack ovules or that they possess dysfunctional gynoecia. These terms should not be applied to post-fertilization events which result in ovule abortion. Further, we review the current evidence for andromonoecy or androgyny in the Proteaceae, especially the genus Banksia , and present the results of studies on two additional Banksia species, B. spinulosa and B. ericifolia. The evidence so far fails to provide support for widespread andromonoecy in this genus as an explanation for low fruit: flower ratios.     

Flower-strip agri-environment schemes provide diverse and valuable summer flower resources for pollinating insects

The diversity and abundance of insect pollinators are declining. This decline reduces the potential ecosystem services of pollination for wild and cultivated plants. Specific agri-environment schemes (AES) are subsidised to support and conserve biodiversity in farmlands. In Belgium, the pollinator flower-strips AES, strips of flower-rich hay meadows, has been promoted as a potential scheme to increase pollinator abundance and diversity, even if their effectiveness has not been locally evaluated. The main objective of this research is to assess the capacity of pollinator-strip AES to provide flower-resources to diverse pollinators. During 2 years, we monthly measured the availability of flower resources (pollen and nectar) produced on four flower-strips surrounded by intensive farming in Belgium. We counted and identified insects that visited these flowers, and we constructed the plant–insect interactions networks. The pollinator-strip AES presented a mix of both sown and spontaneous plant species. The ten sown plant species were all present, even after 8 years of strip settings. Three of them, Centaurea jacea, Lotus corniculatus, and Daucus carota were mainly visited for nectar collection, and a spontaneous non-sown species, Trifolium repens, had a key role in providing high-quality pollen to insects. Most of the observed flower-visiting insects belonged to common species of Hymenoptera and Diptera. All are considered highly efficient pollinators. The Belgian pollinator flower-strips are effective AES that provide flower resources to pollinators, mainly during summer and support pollination services. Nevertheless, spring and autumn flower resources remain poor and could reduce the strips’ effectiveness for supporting long-term insect diversity.     

Mating system and sex ratios of a pollinating fig wasp with dispersing males

Recent studies have used sex ratios to quantify the mating systems of organisms, the argument behind it being that more female-biased sex ratios are an indication of higher local mate competition, which goes hand-in-hand with higher levels of inbreeding. Although qualitative tests of the effects of mating systems on sex ratios abound, there is a dearth of studies that quantify both the mating system and the sex ratio. I use a colour dimorphism with a simple Mendelian inheritance to quantify the mating system of an unusual fig-pollinating wasp in which males disperse to obtain matings on non-natal mating patches. In qualitative agreement with initial expectations, the sex ratios of single foundresses are found to be higher than those of regular species. However, by quantifying the mating system, it is shown that the initial expectation is incorrect and this species' sex ratio is a poor predictor of its mating system (it underestimates the frequency of sib-mating). The species has a very high variance in sex ratio suggesting that excess males can simply avoid local mate competition (and hence a lowered fitness to their mother) by dispersing to other patches.     

Restructuring of a mutualism following introduction of Australian fig trees and pollinating wasps to Europe and the USA

Figs and fig-pollinating wasps are obligate mutualists that require each other to complete sexual reproduction. However, landscapers can establish populations of fig trees outside their native ranges by propagation through exported seeds, seedlings or cuttings. Once mature, these trees could be colonized by pollinating wasps and/or various non-pollinating wasps that also develop in figs. In recent decades, the Australian endemic Ficus rubiginosa has been planted widely in the Mediterranean region and in parts of the USA. Observation of ripe fruit production suggested that a pollination mutualism has been re-established by pollinating wasps colonizing trees in the plant’s introduced range. We therefore used sampling of pollinators from mainland Spain, Tenerife and California (USA) and molecular studies to characterize the restructured mutualism and compare it with the native range. In the native range, the plant is pollinated by five wasp species that form the Pleistodontes imperialis complex. However, all wasps in the introduced ranges belonged to just one of these species (P. imperialis sp. 1). Moreover, their mtDNA diversity was close to zero and the sequences clearly link them with the native southern population of this species. None of the?>?20 non-pollinating wasp species from the native range were found in the introduced ranges. In summary, the restructured mutualism has been dramatically simplified, lacking all non-pollinating wasps and all but one pollinator species from the native range. Moreover, the one pollinator species to establish successfully shows a drastic reduction in genetic diversity relative to its source population.     

Geographic and population variation in pollinating seed-consuming interactions between senita cacti (Lophocereus schottii) and senita moths (Upiga virescens)

Interspecific interactions can vary within and among populations and geographic locations. This variation can subsequently influence the evolution and coevolution of species interactions. We investigated population and geographic variation in traits important to pollinating seed-consuming interactions between the senita cactus (Lophocereus schottii) and its obligate pollinating moth (Upiga virescens), both of which are geographically restricted to the Sonoran Desert. Female moths actively pollinate senita flowers and oviposit onto flowers. Their larvae consume developing seeds and fruit of flowers pollinated by females. Traits important to this interaction include fruit set from moth pollination, fruit survivorship, and costs of fruit consumption by larvae. We studied these traits for five populations at two widely separated geographic locations. On average, 37% of flowers set fruit, 22% of flowers produced mature fruit, and larvae consumed 25% of immature fruit pollinated by female senita moths. Senita cactus and senita moth interactions were strongly mutualistic in all populations that we studied. Although one population had statistically lower fruit set and fruit production than the other four, all five populations were qualitatively similar in fruit production, costs, and patterns of fruit survivorship. Hand-pollination experiments suggested that fruit set was resource-limited in all but this one population. Apparent pollen limitation in the one population explains the quantitative differences in fruit set and fruit survivorship among the populations. As predicted by theory and exemplified by the senita mutualism, specialized and/or obligate interactions vary little among populations and geographic locations. Received: 5 March 1999 / Accepted: 25 June 1999     

Testing hypotheses for maternal effects in Daphnia magna

Maternal effects are widely observed, but their adaptive nature remains difficult to describe and interpret. We investigated adaptive maternal effects in a clone of the crustacean Daphnia magna, experimentally varying both maternal age and maternal food and subsequently varying food available to offspring. We had two main predictions: that offspring in a food environment matched to their mothers should fare better than offspring in unmatched environments, and that offspring of older mothers would fare better in low food environments. We detected numerous maternal effects, for example offspring of poorly fed mothers were large, whereas offspring of older mothers were both large and showed an earlier age at first reproduction. However, these maternal effects did not clearly translate into the predicted differences in reproduction. Thus, our predictions about adaptive maternal effects in response to food variation were not met in this genotype of Daphnia magna.     

Testing Cort-Fitness and Cort-Adaptation hypotheses in a habitat suitability gradient for roe deer

According to the Cort-Fitness Hypothesis, higher stress levels (glucocorticoids) in vertebrates are correlated to lower fitness. However, recent studies have failed to validate this hypothesis. A proposed wider framework suggests that reproduction can be perceived as an overload adds up to other environmental challenges that individuals must adjust to. In this case, elevated glucocorticoids could help individuals to allocate resources to reproduction without comprising other functions, leading to the expectation of a positive cort-fitness relationship. This has been proposed as the Cort-Adaptation Hypothesis. Stress levels result from a complex interaction between the environment and the neuroendocrine system of animals. Accounting for physiological functions involved in how animals cope with their environment would help to clarify the relationship between glucocorticoids and animal performance. We used roe deer (Capreolus capreolus) inhabiting diverse habitats in the Iberian Peninsula to: i) test the Cort-Fitness and Cort-Adaptation hypotheses by indexing fitness using a comprehensive physiological approach which takes into account fundamental physiological functions and their trade-offs; and ii) evaluate the link between primary productivity and individuals' condition in a seasonal environment. We evaluated spatial and temporal variation in stress levels, reproductive hormone levels, nutritional status and immune function from fecal samples collected in 2010. Lower stress levels were related to better condition in non-reproductive seasons but not to higher primary productivity. In contrast, stress levels were always positively related to reproductive condition, which was better in most productive habitats. Summer and winter were the less productive seasons and the more challenging for the species in the habitat gradient studied. In winter, reproductive condition traded off against immune function being biased toward immune function in less productive habitats. In summer reduced primary productivity limited roe deer nutritional and immunological condition but not reproductive condition. Overall our results match both the Cort-Fitness and Cort-Adaptation Hypotheses.     

基于集合种群理论框架的榕树-榕小蜂互惠系统动力学模型

互惠共生指双方物种都能通过对方增加适合度的种间关系。榕树与榕小蜂的传粉关系是自然界中典型的互惠共生系统,这种互惠关系发生在榕果中,也就是榕果是种间作用的场所,榕小蜂在其中传粉和产卵。由此,可以把榕果看作榕小蜂的生境斑块,利用集合种群理论框架构建榕树与榕小蜂互惠关系的动力学模型,研究这个互惠系统的稳定性和续存条件。由于这里的生境斑块(榕果)的动态变化性(榕果产生和掉落),模型不同于传统的生境斑块固定不变的集合种群模型,增加了描述生境动态的维度。模型表明:(1)榕果产生率足够大(大于一个阈值)是榕树与榕小蜂互惠系统能够续存的必要条件;(2)榕树和榕小蜂互惠系统存在双稳态现象(Allee效应),这个互惠系统续存需要种群大小超过一个阈值,换言之,种群大小低于这个阈值时,系统必然灭绝;(3)榕果产生率增加使榕小蜂种群增加,但不会影响未被占据的榕果数量。我们的模型不但可用来研究榕树与榕小蜂互惠系统的动力学性质,而且也是集合种群理论斑块动态化的发展。     

Testing evolutionary hypotheses for DNA barcoding failure in willows

The goal of DNA barcoding is to enable the rapid identification of taxa from short diagnostic DNA sequence profiles. But how feasible is this objective when many evolutionary processes, such as hybridization and selective sweeps, cause alleles to be shared among related taxa? In this issue of Molecular Ecology, Percy et al. (2014) test the full suite of seven candidate plant barcoding loci in a broad geographic sample of willow species. They show exceptional plastid haplotype sharing between species across continents, with most taxa not possessing a unique barcode sequence. Using population genetic and molecular dating analyses, they implicate hybridization and selective sweeps, but not incomplete lineage sorting, as the historical processes causing widespread haplotype sharing among willow taxa. This study represents an exceptional case of how poorly barcoding can perform, and highlights methodological issues using universal organellar regions for species identification.     

Fruit to flower ratios and trade-offs in size and number

Summary Hermaphroditic flowering plants commonly produce many more flowers than fruits. To interpret this observation, I suggest an explanation based on trade-offs occurring between the size and the number of flowers and fruits that mature when resources are limiting. I make this suggestion concrete with the aid of a phenotypic model analysed using the ESS approach. The model includes resource allocations to male and female reproductive structures at the time of flowering and to fruit maturation. The formulation allows for non-linear relations between opportunities for fertility gain on the one hand and flower and fruit size and number on the other. Results of the model indicate that fewer fruits will be matured than flowers produced, even in the absence of previously suggested factors such as pollinator limitation and bet-hedging in the face of environmental variability. Model results emphasize the distinction between flower versus inflorescence contributions to male and female reproductive success. Analysis also shows that the fruit to flower ratio in hermaphroditic plants will be lower than that in female plants, in accord with broad taxonomic surveys. Finally, results obtained lead to empirically testable predictions about the relationship between flower size, fruit size and the fruit to flower ratio. Methods to test these predictions are discussed.