Florivore impacts on plant reproductive success and pollinator mortality in an obligate pollination mutualism

Florivores are present in many pollination systems and can have direct and indirect effects on both plants and pollinators. Although the impact of florivores are commonly examined in facultative pollination mutualisms, their effects on obligate mutualism remain relatively unstudied. Here, we used experimental manipulations and surveys of naturally occurring plants to assess the effect of florivory on the obligate pollination mutualism between yuccas and yucca moths. Yucca filamentosa (Agavaceae) is pollinated by the moth Tegeticula cassandra (Lepidoptera: Prodoxidae), and the mutualism also attracts two florivores: a generalist, the leaf-footed bug Leptoglossus phyllopus (Hemiptera: Coreidae), and a specialist, the beetle Hymenorus densus (Coleoptera: Tenebrionidae). Experimental manipulations of leaf-footed bug densities on side branches of Y. filamentosa inflorescences demonstrated that feeding causes floral abscission but does not reduce pollen or seed production in the remaining flowers. Similar to the leaf-footed bugs, experimental manipulations of beetle densities within individual flowers demonstrated that beetle feeding also causes floral abscission, but, in addition, the beetles also cause a significant reduction in pollen availability. Path analyses of phenotypic selection based on surveys of naturally occurring plants revealed temporal variation in the plant traits important to plant fitness and the effects of the florivores on fitness. Leaf-footed bugs negatively impacted fitness when fewer plants were flowering and leaf-footed bug density was high, whereas beetles had a positive effect on fitness when there were many plants flowering and their densities were low. This positive effect was likely due to adult beetles consuming yucca moth eggs while having a negligible effect on floral abscission. Together, the actions of both florivores either augmented the relationship of plant traits and fitness or slightly weakened the relationship. Overall, the results suggest that, although florivores are always present during flowering, the impact of florivores on phenotypic selection in yuccas is strongly mitigated by changes in their densities on plants from year to year. In contrast, both florivores consistently influenced pollinator larval mortality through floral abscission, and H. densus beetles additionally via the consumption of pollinator eggs.     

Nonadditive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus

Flower herbivory and pollination have been described as interactive processes that influence each other in their effects on plant reproductive success. Few studies, however, have so far examined their joint effects in natural populations. In this paper we evaluate the influence of flower damage and pollination by the hummingbird Oreotrochilus leucopleurus on the fecundity of the Andean monkey flower Mimulus luteus. We performed a 2×2 factorial experiment, with artificial clipping of lower petals and selective exclusion of the hummingbird as main factors. In spite of the relatively low proportion (27.5%) of the variance in seed production accounted for by the full factorial model, artificial damage and hummingbird exclusion, as well as their interaction, were highly significant, indicating nonadditive effects of factors on plant fecundity. In the presence of hummingbirds, undamaged flowers had a seed production that was 1.7-fold higher than for damaged flowers, suggesting that the effect of flower damage on female reproductive success occurs probably as a consequence of hummingbird discrimination against damaged corollas. This result indicates that the impact of flower herbivory on plant fecundity was contingent on the presence or absence of hummingbirds, suggesting that pollinators may indirectly select for undamaged and probably resistant flower phenotypes. A second interaction effect revealed that undamaged flowers produced 78.5% more seeds in the absence of rather than in the presence of O. leucopleurus, raising the question of the ecological mechanism involved. We suggest that the strong territorial behavior exhibited by the bee Centris nigerrima may confine the foraging activities of the remaining bee species to safe sites within exclosures. Overall, our results provide evidence that hummingbird pollination and flower herbivory have interdependent effects on M. luteus fecundity, which indicates that it will be difficult to predict their ecological and evolutionary consequences unless interactions are analyzed in an integrated form.     

The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior

Interactions between a plant species (Corydalis caseana), a bumble bee nectar robber (Bombus occidentalis), and a bumble bee pollinator (B. appositus) were studied. There were no significant differences between naturally robbed and unrobbed flowers in fruit set or mean seed set per fruit. Plots of C. caseana plants were subjected to treatments of robbing and no robbing using commercially available colonies of B. occidentalis. Robbers did not pollinate the flowers. Pollinator behavior was observed to determine (1) the number of bees attracted to each plot, (2) the number of inflorescences visited in a plot, (3) the number of flowers visited on each inflorescence, and (4) the distance flown between inflorescences. There were no significant differences in the number of inflorescences visited per bee or the number of flowers visited per inflorescence per bee when robbed and unrobbed treatments were compared. Of the parameters measured, only distance flown between inflorescences differed in the robbed and the unrobbed treatments. Bees flew significantly further between inflorescences in the robbed plots than in the unrobbed plots. The results indicate that the nectar robbers have no negative effect on fruit set or seed set in C. caseana and that they may cause increased pollen flow distances by changing the behavior of the pollinator.     

Effects of nectar-robbing on plant reproduction and evolution

The relationship between plant and pollinator is considered as the mutualism because plant benefits from the pollinator’s transport of male gametes and pollinator benefits from plant’s reward. Nectar robbers are frequently described as cheaters in the plant-pollinator mutualism, because it is assumed that they obtain a reward (nectar) without providing a service (pollination). Nectar robbers are birds, insects, or other flower visitors that remove nectar from flowers through a hole pierced or bitten in the corolla. Nectar robbing represents a complex relationship between animals and plants. Whether plants benefit from the relationship is always a controversial issue in earlier studies. This paper is a review of the recent literatures on nectar robbing and attempts to acquire an expanded understanding of the ecological and evolutionary roles that robbers play. Understanding the effects of nectar robbers on the plants that they visited and other flower visitors is especially important when one considers the high rates of robbing that a plant population may experience and the high percentage of all flower visitors that nectar robbers make to some species. There are two standpoints in explaining why animals forage on flowers and steal nectar in an illegitimate behavior. One is that animals can only get food in illegitimate way because of the mismatch of the morphologies of animals’ mouthparts and floral structure. The other point of view argues that nectar robbing is a relatively more efficient, thus more energy-saving way for animals to get nectar from flowers. This is probably associated with the difficulty of changing attitudes that have been held for a long time. In the case of positive effect, the bodies of nectar robbers frequently touch the sex organs of plants during their visiting to the flowers and causing pollination. The neutral effect, nectar robbers’ behavior may destruct the corollas of flowers, but they neither touch the sex organs nor destroy the ovules. Their behavior does not affect the fruit sets or seed sets of the hosting plant. Besides the direct impacts on plants, nectar robbers may also have an indirect effect on the behavior of the legitimate pollinators. Under some circumstances, the change in pollinator behavior could result in improved reproductive fitness of plants through increased pollen flow and out-crossing. __________ Translated from Acta phytoecologiaca Sinica, 2006, 30(4): 695–702 [译自: 植物生态学报]     

The effects of plant density upon pollination success, reproductive effort and fruit parasitism in Cistus ladanifer L. (Cistaceae)

Human activity often causes a decline in the local density of plant populations. Below some critical lower density, populations may suffer a progressive decline in reproductive success because of the difficulties associated with finding suitable mates. Therefore, to conserve endangered plant species it is necessary to understand in greater detail how changes in population density affect different determinants of plant reproductive success. We simultaneously recorded individual plant pollination success, reproductive effort and fruit parasitism in three populations of Cistus ladanifer L. in eastern Portugal. Pollination success declined significantly as distance to the nearest conspecific increased (p<0.001). However, reproductive effort and fruit parasitism showed the opposite pattern (both p<0.001). On average, plants farther than 1 m from their nearest conspecific suffered from three times more fruit parasitism compared to plants closer to a conspecific. Overall, net female reproductive output decreased as nearest neighbor distance rose (p<0.001). Thus, isolated plants were able to compensate only partially for reduced pollination success through increased reproductive effort. We conclude that management plans for plant populations should recognize that reproductive success is the accumulated result of several different processes, which may each respond to plant density in different ways.     

Effects of nectar-robbing on plant reproduction and evolution

The relationship between plant and pollinator is considered as the mutualism because plant benefits from the pollinator's transport of male gametes and pollinator benefits from plant's reward.Nectar robbers are frequently described as cheaters in the plant-pollinator mutualism,because it is assumed that they obtain a reward (nectar) without providing a service (pollination).Nectar robbers are birds,insects,or other flower visitors that remove nectar from flowers through a hole pierced or bitten in the corolla.Nectar robbing represents a complex relationship between animals and plants.Whether plants benefit from the relationship is always a controversial issue in earlier studies.This paper is a review of the recent literatures on nectar robbing and attempts to acquire an expanded understanding of the ecological and evolutionary roles that robbers play.Understanding the effects of nectar robbers on the plants that they visited and other flower visitors is especially important when one considers the high rates of robbing that a plant population may experience and the high percentage of all flower visitors that nectar robbers make to some species.There are two standpoints in explaining why animals forage on flowers and steal nectar in an illegitimate behavior.One is that animals can only get food in illegitimate way because of the mismatch of the morphologies of animals'mouthparts and floral structure.The other point of view argues that nectar robbing is a relatively more efficient,thus more energy-saving way for animals to get nectar from flowers.This is probably associated with the difficulty of changing attitudes that have been held for a long time.In the case of positive effect,the bodies of nectar robbers frequently touch the sex organs of plants during their visiting to the flowers and causing pollination.The neutral effect,nectar robbers' behavior may destruct the corollas of flowers,but they neither touch the sex organs nor destroy the ovules.Their behavior does not affect the fruit sets or seed sets of the hosting plant.Besides the direct impacts on plants,nectar robbers may also have an indirect effect on the behavior of the legitimate pollinators.Under some circumstances,the change in pollinator behavior could result in improved reproductive fitness of plants through increased pollen flow and out-crossing.     

Effects of nectar theft by flower mites on hummingbird behavior and the reproductive success of their host plant, Moussonia deppeana (Gesneriaceae)

Hummingbird flower mites are transported in the nares of hummingbirds and may compete with them by "robbing" nectar secreted by the host plants. We have shown that Tropicoseius sp. flower mites consume almost half the nectar secreted by the long-lived, protandrous flowers of Moussonia deppeana (Gesneriaceae) pollinated by Lampornis amethystinus (Trochilidae). In this paper, we ask whether mimicking nectar consumption of flower mites alters some aspects of hummingbird foraging patterns, and, if so, how this affects host plant seed production. We observed hummingbirds foraging on (a) plants in which nectar was removed from the flowers and then filled with a sugar solution to half the volume of nectar simulating nectar consumption by flower mites, and (b) plants where nectar was removed and then filled with the sugar solution up to normal nectar volumes. Flower mites were excluded from both groups of plants to control for mite activity. Hummingbirds made fewer but longer visits to plants and revisited more the flowers with nectar removal than those without the treatment. We then conducted a pollination experiment on pistillate flowers using a stuffed L. amethystinus hummingbird to evaluate the effect of pollination intensity (number of bill insertions into one flower) on seed production. Flowers with more insertions produced significantly more seeds than those flowers that received fewer insertions. We conclude that the simulation of nectar consumption by hummingbird flower mites can influence the behavior of the pollinator, and this may positively affect seed production.     

The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant

Pollen fate can strongly affect the genetic structure of populations with restricted gene flow and significant inbreeding risk. We established an experimental population of inbred and outbred Silene latifolia plants to evaluate the effects of (i) inbreeding depression, (ii) phenotypic variation and (iii) relatedness between mates on male fitness under natural pollination. Paternity analysis revealed that outbred males sired significantly more offspring than inbred males. Independently of the effects of inbreeding, male fitness depended on several male traits, including a sexually dimorphic (flower number) and a gametophytic trait (in vitro pollen germination rate). In addition, full-sib matings were less frequent than randomly expected. Thus, inbreeding, phenotype and genetic dissimilarity simultaneously affect male fitness in this animal-pollinated plant. While inbreeding depression might threaten population persistence, the deficiency of effective matings between sibs and the higher fitness of outbred males will reduce its occurrence and counter genetic erosion.     

Effects of ants on the reproductive success of Euphorbia cyparissias and associated pathogenic rust fungi

Ants are common visitors to the flowers of Euphorbia cyparissias , and also often forage on E. cyparissias stems that are infected by rust fungi of the species complex Uromyces pisi . These fungi sterilise their host, produce nectar and require insects for their sexual reproduction. Our objective was to determine whether ant visits enhance the sexual reproduction of either E. cyparissias or the rust fungi. Uromyces pisi is known to be obligately outcrossing, whereas a breeding system experiment established that E. cyparissias can self, but sets more seeds when outcrossed. We used insect exclusion experiments to test whether ants fertilise the rust fungi and to determine whether ants are pollinators of E. cyparissias . These experiments showed that insect pollination is necessary for seed set and that ants can pollinate the flowers. However, ants do not fertilise the rust fungi.     

Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability

Background and Aims

Mating system is a primary determinant of the ecological and evolutionary dynamics of wild plant populations. Pollen limitation and loss of self-incompatibility genotypes can both act independently to reduce seed set and these effects are commonly observed in fragmented landscapes. This study used a simulation modelling approach to assess the interacting effects of these two processes on plant reproductive performance and population viability for a range of pollination likelihood, self-incompatibility systems and S-allele richness conditions.

Methods

A spatially explicit, individual-based, genetic and demographic simulation model parameterized to represent a generic self-incompatible, short-lived perennial herb was used to conduct simulation experiments in which pollination probability, self-incompatibility type (gametophytic and sporophytic) and S-allele richness were systematically varied in combination to assess their independent and interacting effects on the demographic response variables of mate availability, seed set, population size and population persistence.

Key Results

Joint effects of reduced pollination probability and low S-allele richness were greater than independent effects for all demographic response variables except population persistence under high pollinator service (>50 %). At intermediate values of 15–25 % pollination probability, non-linear interactions with S-allele richness generated significant reductions in population performance beyond those expected by the simple additive effect of each independently. This was due to the impacts of reduced effective population size on the ability of populations to retain S alleles and maintain mate availability. Across a limited set of pollination and S-allele conditions (P = 0·15 and S = 20) populations with gametophytic SI showed reduced S-allele erosion relative to those with sporophytic SI, but this had limited effects on individual fecundity and translated into only modest increases in population persistence.

Conclusions

Interactions between pollen limitation and loss of S alleles have the potential to significantly reduce the viability of populations of a few hundred plants. Population decline may occur more rapidly than expected when pollination probabilities drop below 25 % and S alleles are fewer than 20 due to non-additive interactions. These are likely to be common conditions experienced by plants in small populations in fragmented landscapes and are also those under which differences in response between gameptophytic and sporophtyic systems are observed.     

Age at pollination modifies relative male and female reproductive success in a monoecious fig tree

Plants that depend on a single species of insect pollinator must often contend with infrequent and unpredictable visitation. Prolongation of floral receptivity comes at the cost of reduced male and/or female reproductive success among older flowers. Fig trees (Ficus spp.) have a highly specific pollination symbiosis and individual inflorescences (syconia) that remain receptive for days or weeks. Reproductive success in monoecious fig trees involves production of both seeds and fig wasp offspring. We assessed whether the reproductive output of individual syconia changes with the length of time they waited for pollination, and whether the relative female and male reproductive success also changes. A pollination experiment was conducted in an SE Asian monoecious fig tree Ficus curtipes, in which receptive syconia were covered with mesh bags to exclude wasps and pollinated by single pollinators of this fig tree at their different receptive ages. When the syconia matured their size and contents were recorded. Seed quality was also assessed. The results showed that pollinators entered syconia that had been waiting for up to 36?days. The frequencies of abortions among syconia pollinated at different ages were low throughout. The number of un-utilised flowers increased progressively in older syconia. Seed production was highest in syconia entered on the first day of receptivity, whereas pollinator production peaked in syconia pollinated on day 12, then declined in older syconia. Consequently, overall reproductive efficiency declined with syconium age and floral sex allocation became more male-biased in older syconia. Older syconia also produced lighter seeds. These results suggest that un-pollinated syconia of F. curtipes can remain receptive for several weeks. This makes pollination of each syconium more likely, but at the cost of reduced productivity and with more ovules allocated to male function. However, the prolongation of floral receptivity has significance for the co-adaptation between syconia and fig wasps and for the evolution of the fig tree-fig wasp symbiosis.     

Effects of multiple competitors for pollination on bumblebee foraging patterns and Mimulus ringens reproductive success

When co‐occurring plant species overlap in flowering phenology they may compete for the service of shared pollinators. Competition for pollination may lower plant reproductive success by reducing the number of pollinator probes or by decreasing the quality of pollen transport to or from a focal species. Pair‐wise interactions between plants sharing pollinators have been well documented. However, relatively few studies have examined interactions for pollination among three or more plant species, and little is known about how the outcomes and mechanisms of competition for pollination may vary with competitor species composition. To better understand how the dynamics of competition for pollination may be influenced by changes in the number of competitors, we manipulated the presence of two competitors, Lythrum salicaria and Lobelia siphilitica, and quantified reproductive success for a third species, Mimulus ringens. Patterns of pollinator preference and interspecific transitions in mixed‐species arrays were significantly influenced by the species composition of competitor plants present. Both pair‐wise and three‐species competition treatments led to a similar ～ 40% reduction in Mimulus ringens seed set. However, the patterns of pollinator foraging we observed suggest that the relative importance of different mechanisms of competition for pollination may vary with the identity and number of competitors present. This variation in mechanisms of competition for pollination may be especially important in diverse plant communities where many species interact through shared pollinators.     

Effects of indiscriminate foraging by tropical hummingbirds on pollination and plant reproductive success: experiments with two tropical treelets (Rubiaceae)

Summary In cloud forest at Monteverde, Costa Rica, two common treelets (Palicourea lasiorrachis and Cephaelis elata, both Rubiaceae) depend simultaneously on one hummingbird population (Lampornis calolaema) for pollination. Both species are distylous and self-incompatible. In laboratory experiments, we examined possible effects of indiscriminate foraging by hummingbirds among flowers of both species, as observed in the field, on pollination of Palicourea. In each of 35 trials, captive L. calolaema probed 2 flowers from pin plants of Palicourea followed by 20 thrum flowers of the same species, with either 0, 2, or 10 Cephaelis flowers intervening. We assessed pollen transfer by staining and counting pin pollen tubes growing in thrum styles; counts of 0, 1, or 2 pollen tubes relate directly to seed output (0, 1, or 2 seeds per fruit, respectively). Intervening Cephaelis flowers sharply reduced pollen receipt by thrum flowers of Palicourea and reduced some aspects of pollen dispersal from pins as well, thereby curtailing maternal and paternal reproductive potential of Palicourea. Such effects of interspecific pollen loss on reproductive output may lead to strong competition among some, though not all, combinations of plant species pollinated by L. calolaema or of other plant combinations that share animal pollinators.     

Maximisation of reproductive success by European orchidaceae under conditions of infrequent pollination

Summary The pollination biology of a group of European orchids (Dactylorhiza, Ophrys, Orchis, Platanthera, Goodyera, andSerapias species) are investigated, and their anthecological characteristics considered in relation to natural levels of reproductive success. Pollen ovule (P O) ratios of the European orchids surveyed range from 10 1 (Goodyera repens) to 24 1 (Platanthera chlorantha). Average pollen-load ovule ratios are consistently lower than P O ratios. Naturally occurring pollen loads range from 1 massula to >1 pollinium. Even the smallest pollen load is sufficient to stimulate embryogenesis in experimentally pollinatedDactylorhiza purpurella flowers, although more seeds are set with larger loads. Pollen tubes grow rapidly through the stylar canal and into the top of the ovary within 2 or 3 days of pollination, and grow down either side of the 3 parietal ridges in the ovary. Fertilisation occurs throughout the length of the ovary but its distribution is non-random, especially when pollen loads are limiting, with more seeds being set at the stylar end. All species ofDactylorhiza, Ophrys, andOrchis studied are highly self-compatible. In the absence of pollination,Ophrys andOrchis flowers remain open and fertile for at least 3 weeks. Pollinated flowers remain receptive to further pollinations for at least 8 days. Some fruits can even be obtained on selfing 20-day-old unpollinatedOrchis morio flowers. Excised pollinia retain germinability for a long time, up to 51 days inDactylorhiza purpurella. The arrival of pollen on the stigma hastens floral senescence, but post-pollination changes are relatively slow when compared with those reported for tropical orchid species. It is concluded that characteristics of the pollination biology of European orchids act to maximise reproductive success by (1) prolonging the opportunity for effective pollen deposition both pre- and post-pollination, (2) increasing the likelihood of widespread dispersal, (3) reducing pollen wastage, and (4) increasing seed quality by promoting some pollen competition. As most European orchids are xenogamous and require pollen to arrive on the stigma before seed can be set, reproductive maximisation is of particular adaptive advantage because many of them are infrequently visited by insects so that the probability of successful pollination can be very low.Abbreviations P O pollen ovule ratio - PL O pollen-load ovule ratio - FCR fluorochromatic reaction test     

Contrasting effects of plant population size on florivory and pollination

Changes in plant population size, induced by various forms of habitat degradation, can affect the performance of plants by altering their interactions with other organisms such as pollinators and herbivores. However, studies on plant reproductive response to variation in population size that simultaneously consider different interactions are rare. In this study, we examined (1) how levels of pollinator visitation and florivory vary with population size of a self-incompatible herb, Verbascum nigrum (Scrophulariaceae), (2) the relative effect of these two interactions on host seed set, and (3) whether the intensity of florivory influences pollinator visitation rate. The intensity of florivory increased, whereas pollinator visitation rate decreased with host population size. Although average seed production was negatively affected by the intensity of florivory, seed production was independent of population size. The direct negative effect of florivores on plant seed set was indirectly enforced by their negative effect on pollinator visitation rate. Our results emphasize the complexity of responses of different plant–animal interactions to plant population size. However, interactions involving specialized organisms are likely to disrupt first as plant population size decreases.     

The impact of flower-dwelling predators on host plant reproductive success

Flowers attract insects and so are commonly exploited as foraging sites by sit-and-wait predators. Such predators can be costly to their host plant by consuming pollinators. However, sit-and-wait predators are often prey generalists that also consume plant antagonists such as herbivores, nectar robbers and granivores, so may also provide benefits to their host plant. Here we present a simple, but general, model that provides novel predictions about how costs and benefits interact in different ecological circumstances. The model predicts that the ecological conditions in which flower-dwelling predators are found can generate either net benefits to their host plants, net costs to their host plants, or can have no effect on the fitness of their host plants. The net effect is influenced by the relative densities of mutualists and antagonists. The flower-dwelling predator has a strong positive effect on the plant if both the pollinators and the granivores are at high density. Further, the range of density combinations that yield a positive net outcome for the plant increases if the performance of pollinators is negatively density dependent, if the predator is only moderately effective at influencing flower visitor rates by its potential prey, and if pollinators are very effective. If plants of a given species find themselves consistently in conditions where they benefit from the presence of a predator then we predict that natural selection could favour the evolution of plant traits that increase the likelihood of predator recruitment and retention, especially where plants are served by highly effective pollinators.