Reproductive biology and conservation implications of three endangered snapdragon species (Antirrhinum, Plantaginaceae)

About 32% of Antirrhinum species are considered to be endangered; however, no field studies have focused on their reproductive biology. In this work, several aspects of the reproductive biology (flowering phenology, floral biology, breeding system) and potential limits on seed quantity and quality (pollen limitation, inbreeding depression) were studied in natural populations of three endangered species of the genus (Antirrhinum charidemi, Antirrhinum subbaeticum, Antirrhinum valentinum). Results disclose that all three species need insect visitors for seed production since fruit set after autonomous self-pollination was lower than under hand cross-pollination. A. charidemi and A. valentinum were mainly self-incompatible, whereas A. subbaeticum was self-compatible but herkogamous. Supplementary pollination in open-pollinated flowers only increased fruit set and seed set relative to controls in a given population of A. valentinum. Preliminary data on inbreeding depression at early life-cycle stages of the self-compatible A. subbaeticum revealed that the cumulative level was low. Despite the three species being closely related and sharing many ecological characteristics, they show different mating systems, and different factors limit seed quantity and quality. Thus, caution should be taken when making a common conservation plan for a group of closely related taxa.     

Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands

The aim of this study was to investigate effects of introduced honey bees (Apis mellifera) on native pollination interactions of Echium wildpretii ssp. wildpretii in the sub-alpine desert of Tenerife. We selected two study populations, one dominated by honey bees, while the other was visited by many native insects. During peak activity period of insects, nectar was nearly completely depleted in flowers of the first, but not the latter population. Thus, a high abundance of honey bees may have suppressed visitation by native animals due to exploitative competition. Honey bees stayed longer and visited more flowers on the same inflorescence than native bees, thus potentially promoting self-pollination of the plants. Level of seed set and viability was similar in the two study populations. However, we cannot rule out long-term changes in genetic population structure due to changes in gene-flow patterns caused by foraging behaviour of honey bees vs. native flower-visitors.     

Andromonoecy in <Emphasis Type="Italic">Gynandropsis gynandra</Emphasis> (L.) Briq. (Cleomaceae) and effects on fruit and seed production

Spider plant (Gynandropsis gynandra) is a traditional leafy vegetable widespread in sub-Saharan Africa and tropical Asia that is also valued for its medicinal properties. Developing a breeding program for the species requires detailed knowledge of its phenology, floral morphology and pollination system. This study investigates the effects of floral morphology and pollination mechanisms on the reproductive success in G. gynandra. The experiments were conducted in two locations in Benin. A split-plot design was used with four randomized complete blocks. Three accessions were randomly assigned to the whole plots and five treatments including natural self-pollination, hand self-pollination, geitonogamy, open pollination and hand cross-pollination were randomized over the sub-plots. We observed that individual plant exhibited 70% of staminate (male) flowers and 30% of hermaphrodite flowers. G. gynandra was andromonoecious. Open pollination and hand cross-pollination led to higher fruit and seed set. Natural self-pollination and hand self-pollination resulted in lower fruit and seed production. G. gynandra is a self-compatible and predominantly out-crossing species. Cross-pollination resulted in a significant increase in fruit set. This study set the ground for the development of improved cultivars in G. gynandra.     

Effects of fragmentation on pollinator abundance and fruit set of an abundant understory palm in a Mexican tropical forest

Tropical forest fragmentation affects both biodiversity and plant reproductive success when small, isolated fragments sustain a reduced diversity or abundance of pollinators. Fragmentation-related effects have been poorly investigated in the case of palms, an important structural and functional component of tropical forests. We examined the relationships between fragment size and diversity and abundance of flower visitors, and palm reproduction, by quantifying the arthropod fauna associated to inflorescences of the palm Astrocaryum mexicanum, and its fruit set, in fragments of different size. The sample yielded a total of 228,772 arthropods (10 orders, 60 species). Coleoptera was the predominant group (?50% of the species), followed by Hymenoptera (20%), while the remaining (30%) was distributed among the other eight orders. We found a predominance of pollinating insects (Coleoptera-Nitidulidae), representing 85% of all visitors. Pollinator abundance was negatively affected by fragmentation, with a 4.2-fold average difference between small (<35 ha) and large (114-700 ha) fragments. However, fruit set was relatively high (?0.7) and not affected by fragmentation during three reproductive seasons. This could be explained because small fragments retained remarkably high numbers of pollinators (1191.4/inflorescence) and by the high abundance of palms (and flowers) in fragments. Further research is needed, however, to assess if fragmentation restricts pollinator movements to plants within the fragments, leading to a reduction in genetic variation of the progeny present in forest remnants.     

Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania

Exotic plant invasions threaten ecological communities world-wide. Some species are limited by a lack of suitable pollinators, but the introduction of exotic pollinators can facilitate rapid spread. In Tasmania, where many non-native plants are naturalised, exotic honeybees (Apis mellifera) and bumblebees (Bombus terrestris) have become established. We determined how these species affect the pollination of Lupinus arboreus, an invasive, nitrogen-fixing shrub, which is rarely visited by native pollinators. The proportion of flowers setting seed and the number of ovules fertilised per flower were positively related to the visitation rates of both exotic bee species. There was no effect of bee visitation rates on the proportion of seeds aborted prior to maturity, possibly due to post-fertilisation environmental constraints. We conclude that the spread of B. terrestris may not alter the fecundity of L. arboreus because of the pollination service provided by A. mellifera, and discuss potential interactions between these two bee species.     

Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae)

In plants, understanding the interactions between breeding systems and pollination ecology may enable us to predict the impacts of rarity. We used a comparative approach to test whether rarity is associated with reproductive biology in two closely-related species pairs. This system has been recently altered by changes in fire regimes and the introduction of European honeybees. More than 35% of flowers matured fruits in the common species after natural-pollination compared to <20% of flowers in the rare species. All species were obligate outcrossers in each of the study populations, but only the two rare species were pollen-limited, having significantly lower fruit-set on open-pollinated flowers than those cross-pollinated by hand (mean ± SE; 0.18 ± 0.02 vs. 0.42 ± 0.05; p < 0.001). Native bees (Leioproctus species) and introduced honeybees (Apis mellifera) visited all species. The native bees visited fewer flowers within a plant and moved greater distances between plants while foraging than honeybees, so the native bees are expected to be more effective in promoting outcrossing. While honeybees were the most frequent visitors to flowers of all species, native bees made more visits to common than rare species (0.65 ± 0.20 vs. 0.20 ± 0.09). Our results suggest that the poorer reproductive success in rare Persoonia species is associated with lower pollinator effectiveness, which is exacerbated by frequent fires and introduced honeybees. If this is a causal relationship, this may increase the probability of extinction in populations of these species.     

Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands

We examined visiting patterns of pollinators of Betonica officinalis L. (Lamiaceae) in experimentally fragmented calcareous grasslands and corresponding control plots at two study sites (Movelier and Nenzlingen) in the north-western Swiss Jura mountains. Fragments (1.5×1.5 m) were isolated by a 5-m wide strip of frequently mown vegetation while the control plots were situated in the adjacent undisturbed vegetation. The most common pollinator, the bumblebee Bombus veteranus (Apidae), visited fragments 53.7% less frequently than control plots. Furthermore, a change in foraging behaviour of Bombus veteranus was observed. In fragments the bumblebees visited more inflorescences, flew longer total visiting distances and the visiting time per patch tended to be higher than in control plots. The distribution of angles between arrival and departure direction (turning angles) differed from a uniform distribution in fragments but not in control plots. The increased directionality of bumblebee flight might be due to a decrease in floral rewards. Our results show that small-scale habitat fragmentation can affect plant pollination at two levels both relevant for plant fitness. First, lower visitation rates indicate a limitation of pollinators which might result in reduced seed set of the pollinated plant. Second, changes in pollinator behaviour might reduce pollen dispersal among flowers, increase inbreeding and hence reduce genetic variability in populations of this bumblebee pollinated plant.     

Predicting reproductive success of insect- versus bird-pollinated scattered trees in agricultural landscapes

Scattered trees are set to be lost from agricultural landscapes within the next century without sustained effort to increase recruitment. Thus, understanding the reproductive dynamics of scattered tree populations will be critical in determining how they can contribute to population restoration. The distance between conspecifics should be a key predictor of reproductive success, as more isolated trees are expected to receive fewer pollinator visits and experience increased transfer of self-pollen during longer pollinator foraging bouts. Further, isolation effects should be greater in species with less mobile pollinators. Here we contrast the effects of plant isolation on reproductive success of two species of eucalypt “paddock trees”, Eucalyptus camaldulensis and Eucalyptus leucoxylon, with insect- and bird-pollination, respectively. Seed production was not affected by tree isolation in either the insect- or bird-pollinated species and once outliers were removed, neither was there an effect on germination rate. As somatic mutations may bias outcrossing rate estimates, we initially screened our microsatellite markers for mutations but found no variation in microsatellite profiles throughout the canopy of trees. Individual outcrossing rates did not decline with increasing tree isolation in either the insect- or bird-pollinated species, though there was considerable variation in these rates at large distances, suggesting that pollination becomes unreliable with increasing tree isolation. We found that pollination distances have likely increased in tree species in agricultural landscapes, and that this may be facilitated by introduced honeybees in the case of E. camaldulensis. We therefore suggest that even isolated trees of these species produce seed of sufficient quantity and quality to contribute to population restoration.     

Agricultural insect pest compromises survival of two endemic Braya (Brassicaceae)

Agro-ecosystems support a vast array of non-native insects, but the potential of these insects to invade and degrade natural ecosystems is largely unknown. Plutella xylostella L. (diamondback moth) is a global agricultural pest that is not native to North America. It feeds on members of the Brassicaceae family, including the endangered Braya longii (Fernald) (Long’s braya) and threatened B. fernaldii (Abbe) (Fernald’s braya) which are endemic to the limestone barrens of Newfoundland, Canada. The immigration of P. xylostella from overwintering sites in the United States to this rare natural ecosystem was monitored with pheromone traps between 2003 and 2005. After their mass immigration in early summer, females lay eggs on an average of 30% of the B. longii and 16% of the B. fernaldii population. Larval feeding reduces the mean seed output of infested plants by 60%, from 10.8 to 4.3 seeds/fruit, and damages 26% of their leaves. There are residual and long-term effects of this herbivory, as many dead braya had higher numbers of eggs, and subsequent leaf and fruit damage one to three years before they died. High summer air temperatures and low precipitation allowed this pest to become multivoltine, resulting in additive damage to braya individuals. Presently, insufficient attention is directed to the impacts of agricultural pests on native ecosystems and rare host plants; hence, there is a need for both the conservation and agricultural communities to cooperate in mitigating the impacts of these pests on native biodiversity.     

Commercialized European bumblebee can cause pollination disturbance: An experiment on seven native plant species in Japan

Non-native pollinator species are now widely utilized to facilitate pollination of agricultural crops. Evaluation of the ecological risk of alien pollinators is necessary because they could have a large impact on native ecosystems through disturbing native plant-pollinator interactions. We conducted a greenhouse experiment to examine the impact of the non-native commercialized European bumblebees, Bombus terrestris, on the pollination success of seven Japanese bumblebee-pollinated plant species. Plants were exposed to three groups of bumblebees: native bumblebee(s) only (NATIVE treatment); the alien bee only (ALIEN) and a mix of the two (MIX). ALIEN treatment had negative effects on fruitset and/or fruit quality of five plants, including self-incompatible and compatible, herb and woody, and queen- and worker-pollinated species. The negative effects were caused by a decrease in legitimate flower visitation due to (1) physical inaccessibility to nectary in deep-corolla flowers by the alien bee with insufficient tongue length and, (2) biased flower preference between short-corolla flowers. Fruitset tended to decrease drastically for the self-incompatible species while fruit quality decreased moderately for the self-compatible species. Effects of MIX were not intermediate between NATIVE and ALIEN in most plant species, and caused pollination success to vary in an unpredictable manner amongst plant species, probably due to interaction between native and alien bees. This non-linear relationship between plants’ pollination success and the relative density of the alien suggests that the alien bee can disturb pollination of a plant species even when only representing a small fraction of the total pollinator community.     

Plight of the bumble bee: Pathogen spillover from commercial to wild populations

Pathogen spread or ‘spillover’ can occur when heavily infected, domestic hosts interact with closely-related wildlife populations. Commercially-produced bumble bees used in greenhouse pollination often have higher levels of various pathogens than wild bumble bees. These pathogens may spread to wild bees when commercial bees escape from greenhouses and interact with their wild counterparts at nearby flowers. We examined the prevalence of four pathogens in wild bumble bee populations at locations near and distant to commercial greenhouses in southern Ontario, Canada. Bumble bees collected near commercial greenhouses were more frequently infected by those pathogens capable of being transmitted at flowers (Crithidia bombi and Nosema bombi) than bees collected at sites away from greenhouses. We argue that the spillover of pathogens from commercial to wild bees is the most likely cause of this pattern and we discuss the implications of such spillover for bumble bee conservation.     

Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory

In fragmented landscapes plant species are often confined to remnants of formerly more widespread habitats, with many of their populations being small and isolated. This study experimentally examined the effects of population size and isolation on pollination, herbivory and reproductive success in the forest herb Phyteuma spicatum (Campanulaceae). In an experiment in which population size and isolation were manipulated using plants from the same origin, population size positively affected pollinator visitation, but did not alter the generally high levels of herbivory. As a result, seed production was higher in large populations. Conversely, plants originating from 14 natural populations of varying size and degree of isolation did not differ in reproductive success when grown in the same environment, suggesting similar attractiveness to pollinators and reproductive potential. The intensity of herbivory, however, was higher in progeny of small populations, at least in terms of the proportion of biomass removed. In both experiments, there were no effects of population isolation. The results suggest (1) that small population size decreases reproductive success via direct negative effects on plant-pollinator interactions, (2) that this pattern is not offset by herbivory, but (3) that herbivory enforces fragmentation effects on pollination by further reducing the number of flowering individuals and (4) that habitat fragmentation may influence plant fitness by affecting plant response to herbivory. The effects of habitat fragmentation on plant populations in present-day landscapes are thus complex, illustrating the need for more integrated studies in conservation biology that take into account both mutualistic and antagonistic plant-animal interactions.     

Comparative demography of a rare species in Florida scrub and road habitats

Anthropogenic habitats can offer opportunities for expansion of rare species. The federally listed herb Hypericum cumulicola is virtually restricted to natural gaps within fire-maintained Florida scrub, but also occurs within and along sandy roads traversing scrub. To test the hypothesis that sandy roads provide suitable habitat for H. cumulicola, we compared the demographic performance of scrub and road populations at the Lake Wales Ridge State Forest and Archbold Biological Station in south-central Florida. Twice a year in February and August 1997-2006, we assessed recruitment and survival; annually in August we also measured maximum height and estimated reproductive output of tagged individuals. Scrub population dynamics were more stable than road populations. Recruitment increased with rainfall in scrub populations, but not always in road populations. Compared with scrub populations, road populations were weedier, with more variable life spans, earlier flowering, and higher fecundity. Germination rates did not differ between individuals from different habitats, but varied depending on simulated weather conditions. The weedier life history may reflect a divergent selective environment (and perhaps an evolutionary and ecological trap). Alternatively, adaptive plasticity in H. cumulicola may allow the species to maintain populations in anthropogenic habitats that can serve as refugia for fire-suppressed scrub populations.     

A snake in paradise: Disturbance of plant reproduction following extirpation of bird flower-visitors on Guam

The introduction of an alien top predator, the brown treesnake (Boiga irregularis), has resulted in severe losses of native vertebrate populations in Guam. Among these are important pollinators and seed dispersers. This study is a first attempt to document cascading effects on vertebrate-pollinated native plant species in Guam. We investigated flower visitation, seed set and germination in two native plants, the mangrove tree Bruguiera gymnorrhiza and the forest tree Erythrina variegata var. orientalis. Both species are bird-pollinated. Studies were conducted on two Mariana islands, Guam (with high density of snakes) and Saipan (with nearly no snakes). Visitation rates by birds were high on Saipan, but zero on Guam. Insects and lizards visited flowers to a low extent on both islands. Only lizards were potential effective pollinators. Seed set of both species were significantly higher on Saipan compared to Guam, and for B. gymnorrhiza, seedling recruitment was significantly higher on Saipan. Hence, these bird-pollinated species appear highly dependent on bird visitors for reproduction. The eradication of flower-visiting birds by the invasive treesnake thus secondarily results in broken mutualistic interactions, which may, in turn, result in a lower recruitment of native plants. Thus, the treesnake affects not only potential prey species, but its effects cascade through the entire ecosystem on Guam. Conservation actions should be directed towards an improved recruitment (artificial pollination, planting) of the affected plant species.     

不同蜂传粉对设施桃果实生长发育和品质的影响

应用意大利蜜蜂和小峰熊蜂在北京平谷区果树试验站为设施桃传粉, 以研究2 种蜂的传粉行为对设施桃果实生长发育及其品质的影响。结果表明,应用小峰熊蜂授粉, 设施桃果实在整个发育过程中的果径增长速度显著高于意大利蜜蜂授粉的果实(P<0.05)。2 种蜂授粉的设施桃果实发育历期不同,小峰熊蜂授粉区的桃果实比意大利蜜蜂授粉区的果实提前7 d 左右成熟。桃的生理落果高峰在小峰熊蜂授粉区出现2 次,而在意大利蜜蜂授粉区出现3 次。在小峰熊蜂授粉区, 距离蜂箱不同距离之间的桃座果率基本一致; 而在意大利蜜蜂授粉区, 座果率随着与蜂箱距离的增大而明显降低。小峰熊蜂授粉区桃树的平均座果率略高于意大利蜜蜂授粉区, 但二者之间差异不显著(P>0.05)。经2 种蜂传粉的设施桃果实营养品质差异不显著(P>0.05), 但二者均明显优于人工授粉组(对照)。和意大利蜜蜂授粉的桃果实相比, 经小峰熊蜂传粉后的桃果实, 单果重高, 畸形果率低(P<0.05)。本研究认为中国本土小峰熊蜂为设施桃的传粉效率优于意大利蜜蜂。     

Potential of invasive and native solitary specialist bee pollinators to help restore the rare cowhorn orchid (Cyrtopodium punctatum) in Florida

Cyrtopodium punctatum is a rare epiphytic orchid in southern Florida, made rare by historical over-collection. We examined the potential pollination of this orchid by the recently naturalized orchid bee (Euglossa viridissima), recorded as a pollinator of the orchid in tropical America, and found that this orchid bee is not a pollinator of the plant. We sought to learn what is responsible for relatively heavy fruit set in a Fairchild Tropical Botanic Garden population of C. punctatum, and determined that the native oil-collecting bee, Centris errans, is the most important pollinator. C. punctatum flowers at Fairchild have 18 times the fruit set of flowers in Everglades National Park. The difference is probably due to the many species and individuals of oil-reward plants in the Malpighiaceae in the garden, compared to one uncommon native species in the park. Female C. errans visit these oil-reward flowers to obtain edible oils to provision their brood. Cyrtopodium flowers appear to mimic the oil-reward flowers of the Malpighiaceae to attract Centris bee pollinators, much as many Oncidium orchids do in tropical America. We recommend that Brysonima lucida, a rare native malpighiaceous shrub, and C. punctatum be planted together in Everglades National Park and other natural areas to attempt to increase C. errans pollination, to restore and enhance the long-term survival of the orchid. Planting model malpighiaceous plants to enhance Centris bee pollination may be a useful restoration tactic for other rare orchid mimics in the American tropics, including Atlantic Forest in Brazil.     

Reproductive constraints for the long-term persistence of fragmented Acacia dealbata (Mimosaceae) populations in southeast Australia

Fragmented and degraded vegetation characterises agricultural landscapes across southern Australian. Remnant vegetation within these regions performs a number of vital ecological and hydrological roles, but little is known about whether or how fragmentation is affecting the long-term persistence of these critical landscape elements. Acacias are a significant component of many remnant vegetation communities across Australia, forming numerous integral faunal and floral relationships. Here, reproductive output of 11 fragmented Acacia dealbata (Mimosaceae) populations from across the southern tablelands of New South Wales was assessed over 2 years to identify reproductive constraints associated with increasing vegetation fragmentation. Fertilization success is the major reproductive constraint, particularly in small populations, and probably reflects a self-incompatible reproductive strategy. During 2002 larger and more dense populations produced more legumes (p = 0.014 and <0.001, respectively) while in 2003 these two variables were associated with increased fertilization success (p = 0.004 and 0.017, respectively). There was also some suggestion that populations with fewer exotic species also experienced increased fertilization success (p = 0.055). Assessment of plant performance within populations suggests that consistent reproductive output of particular individuals within small populations may limit reproductive compatibility within these populations over time. The long-term persistence of many small A. dealbata populations may be jeopardised by low seed set, and limited recruitment and aging stands. Immediate steps are now required to ensure that these populations continue contributing to landscape function by augmenting populations, improving connectivity, and allowing disturbance events that will stimulate recruitment.     

Gardens benefit bees and enhance pollination in intensively managed farmland

The recent loss of pollinating insects and out-crossing plants in agricultural landscapes has raised concern for the maintenance of ecosystem services. Wild bees have been shown to benefit from garden habitats in urban and suburban areas. We investigated the effects of distance from garden habitats on wild bees and seed set of a native out-crossing plant Campanula persicifolia, in intensively managed agricultural landscapes in Southern Sweden. Bee abundance and species richness, as well as plant seed set, were higher closer to gardens (<15 m) than further away (>140 m). This highlights private gardens as a landscape wide resource for pollinators but also the lack of sufficient pollination of wild plants in contemporary agricultural landscapes.     

The role of floral biology and breeding system on the reproductive success of the narrow endemic Petrocoptis viscosa rothm. (Caryophyllaceae)

Morphological and functional characteristics of flowers may have major effects on their reproductive success. Here, we report a study on the characteristics of flowers of Petrocoptis viscosa, a herb species endemic to the northwest Iberian Peninsula, restricted to crevices in limestone outcrops, and currently occurring in only three populations within an area of less than 30 km². We also investigated the effects of pollen source on indicators of reproductive success. The results show that Petrocoptis viscosa flowers are well adapted to autogamy. Inbreeding depression (as determined by comparison of results obtained after selfing and outcrossing) was negligible for fruit production (δ=−0.05) and mean seed number (δ=−0.11), low for seed germination percentage (δ=0.08), but relatively high for mean seed weight (δ=0.23). The spatial structure and small size of population of Petrocoptis viscosa may mean that inbreeding is frequent in natural habitats. Adaptation of plants to autogamy may therefore be energetically beneficial (i.e. less wasted expenditure on rewards and flowers).     

Pollen-limited production of viable seeds in an endemic dwarf birch, Betula apoiensis, and incomplete reproductive barriers to a sympatric congener, B. ermanii

An endemic dwarf birch, Betula apoiensis, is critically endangered, and two populations of this species are restricted to the ridges of Mt. Apoi in Hokkaido, Japan. We observed the flowering phenology, pollen dispersal, and viable seed production and conducted pollination experiments in order to examine pollen limitation and hybridization with a sympatric congener, B. ermanii. B. apoiensis flowered earlier than B. ermanii but had a more variable flowering time among trees than B. ermanii. The female flowering of B. apoiensis temporally overlapped with the male flowering of B. ermanii as well as with that of B. apoiensis. Pollination experiments demonstrated that seed set and seed germination were higher in female flowers outcrossed than in those that were non-pollinated, selfed, hybridized with B. ermanii pollen, or pollinated naturally. A few selfed or hybrid seeds were filled and germinated, which indicates that self-incompatibility and reproductive barriers are not complete. Logistic regressions of local density of conspecific trees on natural seed set and seed germination were significantly positive. These results suggest that B. apoiensis is pollen-limited.