Seed production in a threatened Aloe is not affected by bird exclusion or population size

Small populations of many plant species have been shown to exhibit ecological Allee effects. These effects are expected to be pronounced in plants which are obligate outcrossers and rely on pollinators which forage preferentially in larger populations with greater nectar availability. We examined the breeding and pollination systems, level of pollen limitation and seed production in populations of a threatened “ornithophilous” species, Aloe pruinosa. Experimental hand-pollinations showed that A. pruinosa is genetically self-incompatible and thus an obligate outcrosser. Experimental exclusion of birds from inflorescences did not affect seed production, suggesting that insects are effective pollinators. Supplemental hand-pollinations in several populations showed that seed production in A. pruinosa is not pollen limited. Further, there were no significant relationships between population size and any measure of reproductive success in this Aloe species. Small populations of A. pruinosa are thus viable in terms of pollination processes and should be protected from more direct threats, such as habitat alteration.     

A trade-off in stand size effects in the reproductive biology of a declining tropical conifer Callitris intratropica

Because wind pollination is inefficient over longer distances, plants dependent on it may suffer Allee effects (lower individual reproductive fitness with lower density). However, at higher density, individual reproductive fitness may suffer because of intraspecific competition. We investigate density-dependent effects, via stand size, on cone and seed production and seed germinability in a conifer endemic to tropical Australia. Callitris intratropica R.T. Baker & H.G. Smith is an obligate-seeding tree that often occurs in monodominant stands embedded within savannas and on the fringes of monsoon forests. We found that isolated trees (50–300 m from stands) were taller, of broader profile, and produced approximately twice the number of cones (~407 cones per tree) as those in large stands (~173 cones per tree), suggesting that monodominance generates intraspecific competition. The number of seeds per cone (27 seeds) was not related to stand size. However, a contrasting effect in which seed germinability was higher in large stands (~20 vs. <10 % in small stands) was approximately compensatory and consistent with an Allee effect of wind pollination. The net effect of an approximately even trade-off between cone production and seed germinability was that there was neither an Allee or density-dependent effect of stand size on fitness, measured as the number of germinable seeds per tree. Nevertheless, because the likelihood of cross-fertilisation declines with distance, the ability of C. intratropica to persist as very isolated individuals may be limited.     

Density-dependent seed set in the Haleakala silversword: evidence for an Allee effect

Plant species may be subject to Allee effects if individuals experience a reduction in pollination services when populations are small or sparse. I examined temporal variation in reproductive success of the monocarpic Haleakala silversword (Argyroxiphium sandwicense subsp. macrocephalum) over five years, to determine if plants flowering out of synchrony with most of the population (i.e., in low flowering years) exhibited lower percent seed set than synchronously-flowering plants (i.e., those flowering in high flowering years). Through two pollination experiments conducted over multiple years, I also measured pollen limitation and self-incompatibility in this species. The number of flowering plants varied greatly among years, as did reproductive success. Percent seed set was significantly correlated with the number of plants flowering annually, such that plants flowering in high flowering years (1997 and 2001) exhibited significantly higher percent seed set than did plants flowering in low flowering years (1998-2000). In the 3-year pollen limitation study, plants flowering asynchronously were pollen-limited, whereas plants flowering synchronously were not. This species is strongly self-incompatible. Results of this study demonstrate that the Haleakala silversword experiences reduced reproductive success in low flowering years, and suggest that this Allee effect is pollinator-mediated. Allee effects in plants are an understudied yet potentially important force with implications for the population dynamics and conservation of rare species.     

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.     

Testing for ecological and genetic Allee effects in the invasive shrub Senna didymobotrya (Fabaceae)

For an introduced plant species to become invasive, it must be able to reproduce even in initially small populations. We tested for Allee effects (reduced reproductive performance of individuals in small populations) in the nonclonal, buzz-pollinated shrub Senna didymobotrya in its invasive range in South Africa. The species is self-compatible, but we found that in its invasive range in South Africa it requires pollinators to set seed. Nearly all stigmas (90%) received pollen, but natural fruit set was very low (3-20%). Pollen receipt and fruit set were not significantly correlated with population size. We thus found no evidence for an ecological Allee effect arising from pollen limitation in small populations. Offspring seedling performance, measured in terms of stem volume and leaf area, was also not significantly correlated with the number of plants in the source population, indicating that genetic Allee effects, such as inbreeding depression, are either absent or of such a small magnitude that they would be unlikely to limit further spread of S. didymobotrya in South Africa.     

Pollen limitation and Allee effect related to population size and sex ratio in the endangered Ottelia acuminata (Hydrocharitaceae): implications for conservation and reintroduction

Small populations may suffer more severe pollen limitation and result in Allee effects. Sex ratio may also affect pollination and reproduction success in dioecious species, which is always overlooked when performing conservation and reintroduction tasks. In this study, we investigated whether and how population size and sex ratio affected pollen limitation and reproduction in the endangered Ottelia acuminata, a dioecious submerged species. We established experimental plots with increasing population size and male sex ratio. We observed insect visitation, estimated pollen limitation by hand‐pollinations and counted fruit set and seed production per fruit. Fruit set and seed production decreased significantly in small populations due to pollinator scarcity and thus suffered more severe pollen limitation. Although frequently visited, female‐biased larger populations also suffered severe pollen limitation due to few effective visits and insufficient pollen availability. Rising male ratio enhanced pollination service and hence reproduction. Unexpectedly, pollinator preferences did not cause reduced reproduction in male‐biased populations because of high pollen availability. However, reproductive outputs showed more variability in severe male‐biased populations. Our results revealed two component Allee effects in fruit set and seed production, mediated by pollen limitation in O. acuminata. Moreover, reproduction decreased significantly in larger female‐biased populations, increasing the risk of an Allee effect.     

Differential effect of inter- and intraspecific competition on the performance of invasive and native Taraxacum species

Inter- and intraspecific competitive abilities are significant determinants of invasive success and the ecological impact of non-native plants. We tested two major hypotheses on the competitive ability of invasive species using invasive (Taraxacum officinale) and native (T. platycarpum) dandelions: differential interspecific competitive ability between invasive and native species and the kin recognition of invasive species. We collected seeds from two field sites where the two dandelion species occurred nearby. Plants were grown alone, with kin (plants from the same maternal genotype) or strangers (plants from different populations) of the same species, or with different species in a growth chamber, and the performance at the early developmental stage between species and treatments was compared. The invasive dandelions outcompeted the native dandelions when competing against each other, although no difference between species was detected without competition or with intraspecific competition. Populations of native species responded to interspecific competition differently. The effect of kinship on plant performance differed between the tested populations in both species. A population produced more biomass than the other populations when grown with a stranger, and this trend was manifested more in native species. Our results support the hypothesis that invasive plants have better competitive ability than native plants, which potentially contributes to the establishment and the range expansion of T. officinale in the introduced range. Although kin recognition is expected to evolve in invasive species, the competitive ability of populations rather than kinship seems to affect plant growth of invasive T. officinale under intraspecific competition.     

Allee effects limit population viability of an annual plant

ABSTRACT Allee effects may be experienced by plants when populations are too small or isolated to receive sufficient pollinator services to replace themselves. This article reports experimental data from an annual herb, Clarkia concinna, documenting that small patches suffered reproductive failure due to lack of effective pollination when critical thresholds of isolation were exceeded. In contrast, sufficiently large patches attracted pollinators regardless of their degree of isolation. These data accord with data on patch extinctions showing that small and isolated patches have a higher extinction rate than do large patches and with observations showing chronically low reproductive success in such patches prior to extinction. While not conclusively demonstrating that Allee effects cause extinction in small and isolated patches, the data are suggestive. Although threshold effects have been postulated in several mathematical models of population viability, this is the first report of data from natural populations that display the occurrence of such thresholds. These results have implications for the management of endangered plants, which often are restricted to isolated, small populations, as well as suggesting a potential limit to spatial spread in plant populations dependent on animal vectors for reproduction.     

Limitations to reproductive output and genetic rescue in populations of the rare shrub Grevillea repens (Proteaceae)

Background and Aims

When conserving rare plant species, managers are often faced with small and/or isolated populations displaying low levels of sexual reproduction and genetic variation. One option for reinvigorating these populations is the introduction of genetic material from other sites, but in some cases fitness may be reduced as a result of outbreeding depression. Here the pollination biology of the rare shrub Grevillea repens is studied across its natural range and reproductive responses following cross-pollination among populations are examined to determine factors that may be limiting sexual reproduction and the potential for genetic rescue.

Methods

Pollen manipulation treatments (self-, autogamous self-, cross- and open pollination) were applied to flowers to examine the breeding system and fruit and seed production in five populations of G. repens. Pollen production, presentation and viability were investigated and interpopulation crosses of increasing genetic distance performed among the populations.

Key Results

The study species is self-incompatible and displayed very low natural seed set over two seasons, due partly to low pollen viability in one of the populations. Within-population crossing increased fruit and seed production at some sites, indicating pollinator limitation. Interpopulation crosses further increased reproductive output in one population, suggesting mate limitation, and for this site there was a positive relationship between genetic distance among populations and the size of genetic rescue benefits. However, in other populations there was a decrease in fruit and seed set with increasing genetic distance.

Conclusions

The results highlight that management strategies involving interpopulation crosses can improve reproductive output in small, isolated populations of rare plants, but guidelines need to be developed on a population by population basis.Key words: Grevillea repens, Proteaceae, genetic rescue, pollination ecology, self-incompatibility, breeding system, interpopulation cross, outbreeding depression, pollinator limitation, mate limitation, resource limitation     

Effects of floral herbivory on foraging behaviour of bumblebees and female reproductive success in Pedicularis gruina (Orobanchaceae)

The effects of floral herbivores on floral traits may result in alterations in pollinator foraging behaviour and subsequently influence plant reproductive success. Fed-upon plants may have evolved mechanisms to compensate for herbivore-related decreased fecundity. We conducted a series of field experiments to determine the relative contribution of floral herbivores and pollinators to female reproductive success in an alpine herb, Pedicularis gruina, in two natural populations over two consecutive years. Experimental manipulations included bagging, hand supplemental, geitonogamous pollination, and simulated floral herbivory. Bumblebees not only avoided damaged flowers and plants but also decreased successive visits of flowers in damaged plants, and the latter may reduce the level of geitonogamy. Although seed set per fruit within damaged plants was higher than that in intact plants, total seed number in damaged plants was less than that in intact plants, since floral herbivory-mediated pollinator limitation led to a sharp reduction of fruit set. Overall, the results suggest that resource reallocation within inflorescences of damaged plants may partially compensate for a reduction in seed production. Additionally, a novel finding was the decrease in successive within-plant bumblebee visits following floral herbivory. This may increase seed quantity and quality of P. gruina since self-compatible species exhibit inbreeding depression. The patterns of compensation of herbivory and its consequences reported in this study give an insight into the combined effects of interactions between floral herbivory and pollination on plant reproductive fitness.     

Allee effects within small populations of Aconitum napellus ssp. lusitanicum, a protected subspecies in northern France

Plants growing at low density can suffer from Allee effects as a result of pollen limitation. Previous studies of Allee effects have focused on the effects of variation among populations in size or density on reproduction. Here, the effects of plant distribution within populations on fitness components are explored in a rare plant, Aconitum napellus ssp. lusitanicum, and ecological and genetic mechanisms underlying these effects are identified. To detect pollen limitation, seed production was compared under natural versus hand-supplemented pollinations on inflorescences of different sizes in natural patches differing both in flower density and in isolation from other patches. Germination rate and juvenile survival of seeds produced in low- and high-density patches were also compared. Pollen-supplemented flowers always produced more seeds than open-pollinated flowers, especially among small plants and plants growing at low density. Offspring produced in low-density patches exhibited lower fitness that those produced in high-density patches. This could have been caused by post-fertilization mechanisms, including inbreeding depression or differential maternal resource allocation. These results show that Allee effects on fitness components (ecological and genetic Allee effects) occur within A. napellus populations at different spatial scales. The spatial distribution of plants seems to be a crucial factor affecting reproductive output and fitness.     

The presence of heterospecific males causes an Allee effect

The Allee effect is a positive causal relationship between any component of fitness and population density or size. Allee effects strongly affect the persistence of small or sparse populations. Predicting Allee effects remains a challenge, possibly because not all causal mechanisms are known. We hypothesized that reproductive interference (an interspecific reproductive interaction that reduces the fitness of the species involved) can generate an Allee effect. If the density of the interfering species is constant, an increase in the population of the species receiving interference may dilute the per capita effect of reproductive interference and may generate an Allee effect. To test this hypothesis, we examined the effect of heterospecific males on the relationship between per capita fecundity and conspecific density in Callosobruchus chinensis and C. maculatus. Of the two species, only C. maculatus females suffer reproductive interference from heterospecific males. Only C. maculatus, the species susceptible to reproductive interference, demonstrated an Allee effect, and only when heterospecific males were present. In contrast, C. chinensis, the species not susceptible to reproductive interference, demonstrated no Allee effect regardless of the presence of heterospecific males. Our results show that reproductive interference in fact generated an Allee effect, suggesting the potential importance of interspecific sexual interactions especially in small or sparse populations, even in the absence of a shared resource. It may be possible to predict Allee effects produced by this mechanism a priori by testing reproductive interference between closely related species.     

The influence of an invasive plant species on the pollination success and reproductive output of three riparian plant species

Besides competition for abiotic resources, an increasing number of studies show evidence of the effects of invasive species on the pollination success and reproductive output of indigenous species. We studied the effect of the invasive Impatiens glandulifera Royle on the process of reproduction in the indigenous Lythrum salicaria L. and Alisma plantago-aquatica L. and the naturalized Oenothera biennis L. The latter three species (target species) were transplanted into pots and placed in invaded and non-invaded areas. During flowering season of each of these species, we measured species composition and abundance of pollinators, pollinator behaviour, pollen deposition and female reproductive output of the target species. Competitive effects were found for L. salicaria, in which fewer pollinator species and number of foraging individuals were observed, and also, lower pollen deposition and seed set were measured in these invaded populations. In contrast, the reproductive success of A. plantago-aquatica and O. biennis was not affected by the presence of I. glandulifera. Our data indicate that when invasive and indigenous species show a large overlap in pollinator community, which is the case for I. glandulifera and L. salicaria, competition between these species can occur. When both species have a different pollinator community, pollination success and reproductive output is not affected, even when the indigenous populations are densely and abundantly invaded.     

Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae)

Habitat fragmentation may result in plant populations that are less attractive to pollinators and thus susceptible to reduced reproductive output due to pollination limitation. Pollination limitation was investigated in three Missouri populations of Oenothera macrocarpa, a hawk-moth-pollinated, perennial herb. The populations represented extremes in size and habitat quality. Following supplemental pollination, mean fertilization success (proportion of ovules fertilized) across populations increased from 24.3 to 44.8% and mean seed set (proportion of ovules that matured into seed) increased from 14.7 to 27.9%. These increases were statistically significant in two of the three populations. Failure to achieve 100% fertilization and seed set following supplementation indicates that other factors, in addition to pollination, were limiting to female reproductive success. Fruit set was pollination limited in only one population. Fruits matured with as few as one seed, suggesting that fruit set was not resource limited. The degree of pollination limitation was greatest in the most disturbed population. The population located in the highest-quality habitat was not significantly pollination limited. This suggests that pollination limitation is occurring, at least in part, because of reduced pollinator activity in degraded habitats.     

Evidence for pollen limitation of a native plant in invaded communities

Animal-pollinated invasive species have frequently been demonstrated to outcompete native species for pollinator attention, which can have detrimental effects on the reproductive success and population dynamics of native species. Many animal-pollinated invasive species exhibit showy flowers and provide substantial rewards, allowing them to act as pollinator ‘magnets’, which, at a large scale, can attract more pollinators to an area, but, at a smaller scale, may reduce compatible pollen flow to local native species, possibly explaining why most studies detect competition. By performing pollen limitation experiments of populations in both invaded and uninvaded sites, we demonstrate that the invasive plant Lythrum salicaria appears to facilitate, rather than hinder, the reproductive success of native confamilial Decodon verticillatus, even at a small scale, in a wetland habitat in southeastern Ontario. We found no evidence for a magnet species effect on pollinator attraction to invaded sites. Germination experiments confirmed that seeds from invaded sites had similar germination rates to those from uninvaded sites, making it unlikely that a difference in inbreeding was masking competitive effects. We describe several explanations for our findings. Notably, there were no differences in seed set among populations at invaded and uninvaded sites. Our results underscore the inherent complexity of studying the ecological impacts of invasive species on natives.     

Population size, pollination and reproductive success in two endangered Genista species

Habitat fragmentation often leads to small and isolated plant populations as well as decreased habitat quality. These processes can fundamentally disrupt the interactions between plants and pollinators and decrease reproductive success. This concerns especially self-incompatible, non-clonal species that depend on pollination for successful reproduction.In two rare and endangered heathland plant species, Genista anglica and G. pilosa, we examined pollination and reproduction in relation to population size. Eight populations of G. anglica and ten populations of G. pilosa were surveyed in the vicinity of Bremen, NW-Germany. We counted the visits of pollinators (honeybees, bumblebees, and other insects) and determined the reproductive output of the observed shoots.Contrary to our expectation to find increased pollinator visitation rates in larger populations of both Genista species, the number of flower-visiting insects was unrelated to the number of flowering shoots. Increasing shoot length had a positive and increasing temperature a negative impact on the number of visiting honeybees and bumblebees. Despite the general absence of population size effects on pollinator numbers, the number of fruits and seeds in G. anglica increased with increasing population size. Fruit and seed set in G. pilosa were negatively related to the number of ‘other insects’. Our field observations showed that larger populations of both Genista species flowered earlier than smaller populations and much earlier than reported in the literature. Flowering in large populations therefore tends to coincide less well with pollinator abundance, and this may cause a disruption of the temporal coincidence between flowering phenology and pollinator activity.     

Number of conspecifics and reproduction in the invasive plant Eschscholzia californica (Papaveraceae): is there a pollinator‐mediated Allee effect?

The component Allee effect has been defined as ‘a positive relationship between any measure of individual fitness and the number or density of conspecifics’. Larger plant populations or large patches have shown a higher pollinator visitation rate, which may give rise to an Allee effect in reproduction of the plants. We experimentally tested the effect of number of conspecifics on reproduction and pollinator visitation in Eschscholzia californica Cham., an invasive plant in Chile. We then built patches with two, eight and 16 flowering individuals of E. californica (11 replicates per treatment) in an area characterised by dominance of the study species. We found that E. californica exhibits a component Allee effect, as the number of individuals of this species has a positive effect on individual seed set. However, individual fruit production was not affected by the number of plants examined. Pollinator visitation rate was also independent of the number of plants, so this factor would not explain the Allee effect. This rate was positively correlated with the total number of flowers in the patches. We also found that the number of plants did not affect the seed mass or proportion of germinated seeds in the patches. Higher pollen availability in patches with 16 plants and pollination by wind could explain the Allee effect. The component Allee effect identified could lead to a weak demographic Allee effect that might reduce the rate of spread of E. californica. Knowledge of this would be useful for management of this invasive plant in Chile.     

Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus <Emphasis Type="Italic">Cirsium</Emphasis> (Asteraceae)

Previous studies have examined an association between reproductive success and pollination biology of rare versus widespread species through pair-wise comparisons of native and invasive congeners or rare and common congeners. To determine the importance of reproductive success and pollination biology for an invasive thistle, Cirsium vulgare, we compared it in its invaded range to five, co-occurring native Cirsium species that range from rare to common. Native study species include C. fontinale var. fontinale, C. andrewsii, C. brevistylum, C. occidentale, and C. quercetorum. We compared all species’ reproductive success, insect visitation rate and composition, autonomous self-pollination, and level of pollen limitation in multiple populations. Species differed in their reproductive success; the invasive C. vulgare produced more flower heads per plant than most native species. C. vulgare attracted more visitors than its congeners. In addition, reproductive success and insect visitation significantly varied between populations within species, mainly due to aphid infestation in one population of C. occidentale. Unlike the rare species (C. fontinale and andrewsii), C. vulgare did not require a pollinator for high-levels of seed production. The remaining native species set fewer seeds than C. vulgare without a pollinator. However, differences in insect visitation and autonomous self-pollination did not lead to differences in pollen limitation across species or between populations. This result suggests that factors other than pollination biology determine the difference in reproductive success of these species. However, high levels of autonomous self-pollination and generalist insect visitation may allow the invasive C. vulgare to easily establish new populations from low numbers of propagules. Our study provides one contrast that should build towards a larger comparative analysis to examine general patterns in the relationship between reproductive success, pollination biology, rare and invasive species, and our ability to predict biological invasions in introduced species.     

Pollination efficiency and reproductive patterns in relation to local plant density,population size,and floral display in the rewarding Listera ovata (Orchidaceae)

Pollination efficiency and reproductive success vary strongly among populations of most animal‐pollinated plant species, depending on their size and local density, whereas individual plants within populations experience varying levels of reproductive output as a result of differences in floral display. Although most orchid species have been shown to be severely pollination limited, few studies have investigated the impact of the above‐mentioned factors on pollination success and reproduction, especially in rewarding species. In this study, the impact of population size, local density of flowering plants, and floral display on the rates of pollinia export and fruit production was investigated in 13 natural populations of the rewarding terrestrial orchid Listera ovata. In addition, an emasculation experiment was set up to examine how floral display and local density of flowering plants affected the relative importance of cross‐ vs. geitonogamous pollination in determining fruit set. In the studied populations, pollination efficiency, pollen removal, and fruit set increased with increasing population size until a threshold value of 30–40 flowering plants was reached, above which pollination efficiency and reproductive output decreased again. On average, plants with large floral displays showed higher proportional pollinia removal and fruit set compared with smaller plants. Fruit production was also significantly and positively related to local plant density, whereas emasculation did not affect the relationship between local plant density and fruit set, suggesting that geitonogamous pollination did not affect the outcome of female function. The results of this study are discussed in the light of the flowering mechanism of the species and its generalized pollination system. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 157 , 713–721.     

Pollination ecology of Gentianella uliginosa, a rare annual of the Dutch coastal dunes

The pollination ecology of Gentianella uliginosa , a rare annual in The Netherlands, was studied in three relatively small coastal dune populations. In all populations, the species was fully self-compatible: manual self pollination resulted in a seed set of 92–94%. Autofertility was also high (seed set of caged, unhandled flowers 80–85%). The homogamous flowers were visited by Bombus pascuorum , which collected nectar and transported pollen sternotribically. Differences among populations in bumblebee visitation rate did not affect natural seed set. In one plot, seed set following natural pollination was lower than after manual selñng, and as high as after spontaneous selñng. As flowers here were also visited frequently, this might be due to pollen limitation through heterospecific pollen competition. Support for this hypothesis was derived from another population, where seed set after natural pollination was lower in a plot dominated by co-flowering Mentha aquatica than in a plot with few Mentha. However, differences in water availability might also have caused this. In one population, seed sets of the cross pollination and spontaneous selfing treatments were lower than those of the manual selñng and natural pollination treatments. Whether the low outcrossing success can be attributed to small differences in the treatment of the experimental plants or to outcrossing depression remains unclear. We conclude that this annual species is most likely a predominant selfer. Its high autofertility is probably an adaptation to its wet dune slack habitat, where reproductive assurance may be important to cope with unpredictable fluctuations in water table, summer droughts and pollinator service.