Comparative pollination biology of Venezuelan columnar cacti and the role of nectar-feeding bats in their sexual reproduction

The floral biology, reproductive system, and visitation behavior of pollinators of four species of columnar cacti, Stenocereus griseus, Pilosocereus moritzianus, Subpilocereus repandus, and Subpilocereus horrispinus, were studied in two arid zones in the north of Venezuela. Our results support the hypothesis that Venezuelan species of columnar cacti have evolved toward specialization on bat pollination. Additional information on the floral biology of a fifth species, Pilosocereus lanuginosus, was also included. All species showed the typical traits that characterize the pollination syndrome of chiropterophily. All species but Pilosocereus moritzianus were obligate outcrossers. Nectar and pollen were restricted to nocturnal floral visitors. Two species of nectar-feeding bats, Leptonycteris curasoae Miller and Glossophaga longirostris Miller, were responsible for practically all the fruit set in these cacti. Frequency of bat visitation per flower per night was highly variable within and between species of cactus, with average frequencies varying between 27 and 78 visits/flower/night. In general terms, the pattern of floral visitation through the night was significantly correlated with the pattern of nectar production and nectar sugar concentration for all species of cactus. Under natural pollination, fruit:flower ratios varied from 0.46 in Subpilocereus repandus to 0.76 in Stenocereus griseus. The efficiency of bat pollination in terms of seed:ovule ratio was high in all species, varying between 0.70 and 0.94.     

Genetic population structure and mobility of two nectar-feeding bats from Venezuelan deserts: inferences from mitochondrial DNA

Glossophaga longirostris and Leptonycteris curasoae are nectar-feeding bats associated with arid zones in northern South America. Despite their close phylogenetic relationship, sympatric condition and niche similarities, morphological and ecological evidence suggest that these species differ in dispersal capabilities. Using mitochondrial DNA, we tested the hypothesis that these species exhibit different levels of population structure that are congruent with their particular movement capabilities. We sequenced a section of the control region of mtDNA for 41 G. longirostris and 42 L. curasoae from 11 zones in Venezuela. Population subdivision in G. longirostris (FST = 0.725) was considerably higher than in L. curasoae (FST = 0.167). L. curasoae individuals shared haplotypes at greater distances (812 km) than G. longirostris (592 km). Our results offer preliminary evidence for one of two possible scenarios, either greater mobility in L. curasoae or a higher degree of female philopatry in G. longirostris.     

The Diet and Reproductive Schedules of Leptonycteris curasoae curasoae and Glossophaga longirostris elongata (Chiroptera: Glossophaginae) on Curaçao

Two bat species, Leptonyrteris curasoae and Glossophaga longirostris, are the principal pollinators of at least two of the three species of columnar cacti that grow on the semiarid island of Curaçao, Netherlands Antilles. I examined the importance of the cacti in the diets of the bats and found that 85–91 percent of their diet samples contained cactus pollen and seeds. At least 43 percent of the samples from each species contained cactus pollen andlor seeds exclusively. Leptonycteris curasoae consumes nectar and pollen of Ceiba pentandra and Agave spp. at the beginning of the dry season and G. longirostris also consumes a few other plant products in the wet season, but both bat species depend nutritionally on cacti. Female bats give birth to one pup per year, and the periods of parturition and lactation in each species correspond to peaks in the reproductive phenology of the two most abundant columnar cactus species. From personal observations and a review of the literature, I determined that bats were unlikely to fly to the mainland to feed, although L. curasoae may do so. I conclude that the interdependence of bats and cacti is suggestive of coevolution, and that columnar cacti are critical for the survival and persistence of nectar-feeding bats on Curaçao.     

Resource availability, population dynamics and diet of the nectar-feeding bat Leptonycteris curasoae in Guaymas, Sonora, Mexico

Nectar-feeding bats play important roles in the pollination of columnar cacti. Migratory bats such as Leptonycteris curasoae are vulnerable to extinction due to their migratory behavior and cave-roosting habit. The conservation of migratory bats requires the identification and protection of key roosting sites and their floral resources. In this paper we describe the availability of resources, the population dynamics and the diet of L. curasoae in the Guaymas region, and its diet at three additional sites in coastal Sonora, Mexico. Our results indicate that L. curasoae is a seasonal resident in the Guaymas area, with local occupation of around 4 months. Seasonal occupation seems to be determined by the availability of flowers and fruits of columnar cacti as peak abundance and peak availability coincide in time. The analyses of fecal and fur samples revealed that columnar cacti constitute the major food source during their seasonal occupation of coastal Sonora. The frequency of pollen from Agave and Bombacaceae in fecal samples was generally low but increased in importance in lower latitudes. Our results suggest that the availability of resources provided by columnar cacti determine seasonal occupation of L. curasoae in Sonora. Given that we detected newborns in the studied colony, we suggest active cave protection for the conservation of the maternity roosting site in Guaymas, Sonora, Mexico.     

Pollination biology of two columnar cacti (Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala) in the Tehuacan Valley,central Mexico

We document the pollination biology and mating systems of Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala, two Mexican giant columnar cacti. These two species form mixed forests in the western Tehuacan Valley, Mexico. The flowers of both N. mezcalaensis and N. macrocephala exhibit nocturnal anthesis, are self-incompatible, and are pollinated primarily by three species of nectar-feeding bats (Choeronycteris mexicana, Leptonycteris curasoae, and Leptonycteris nivalis). Neobuxbaumia mezcalaensis is androdioecious, a breeding system that appears to be uncommon among Cactaceae. Neobuxbaumia macrocephala is hermaphroditic. We hypothesize that columnar cacti show a geographical dichotomy in floral biology specialization that probably can be related to predictability in pollinator abundance.     

Estudio Fenológico de Cactíceas en el Enclave Seco de la Tatacoa,Colombia1

A one‐year phenological study of three columnar cacti, Stenocereus griseus (Haw.) Britton & Rose, Pilosocereus sp., Cereus hexagonus (L.) Mill., and a decumbent cactus Monvillea cf. smithiana (Britton & Rose) Backeberg., was carried out in the Andean arid region of La Tatacoa, Colombia. Pollinators and/or dispersers of the cacti species also were studied monthly, and fecal samples were collected for the identification of pollen and seeds. The flowering of all species was prolonged and showed bimodal, multimodal, or irregular patterns. Fruiting in all species also was prolonged and followed flowering with a lag of less than two months. Although there were no simple correlations between rainfall and flowering or fruiting, flower production during the dry season was higher for 5. griseus, while Pilosocereus sp. and C. hexagonus showed higher flower production during the wet season. Fruit production was also seasonal, with higher production during the wet season for 5. griseus and C. hexagonus. The patterns of flowering and fruiting in M. cf. smithiana showed no relationships with dry and wet seasons. The bats Glossophaga longirostris, Carollia perspicillata, Sturnira lilium, the birds Melanerpes rubricapillus (Picidae) and Mimus gilvus (Mimidae), and moths of the family Sphingidae, were identified as pollinators and/or fruit consumers of these cacti species.     

Effectiveness of bats as pollinators of Stenocereus stellatus (Cactaceae) in wild, managed in situ, and cultivated populations in La Mixteca Baja, central Mexico

Stenocereus stellatus is an endemic, self-incompatible, columnar cactus found in central Mexico where many of its wild populations have been fragmented. As an economically important species of fruit-producing cactus, S. stellatus occurs in wild, managed in situ, and cultivated populations. The objectives of this study were to determine the effective pollinators of S. stellatus, to compare pollinator visits and reproductive parameters among the three types of populations, and to determine if nectar feeding-bats are moving among populations. Effective pollinators were the nectarivorous bats Choeronycteris mexicana, Leptonycteris curasoae, and L. nivalis. Fewer total visits per flower per night and fewer visits by Choeronycteris were observed in cultivated populations, while the opposite pattern was observed for Leptonycteris. One aggressive interaction was filmed in which Choeronycteris was physically displaced by Leptonycteris, and Choeronycteris visits were significantly affected by Leptonycteris visits. Cultivated populations received more pollen grains and had more fruit set. Variation in pollinator visits between different populations and the consequent effects on reproductive success were likely a result of competition between bat species, and differences in foraging and in sensitivity of bat species to human populations. Three marked L. curasoae traveled 15 km from their roosting site to their foraging area, and one visited cultivated and managed populations, suggesting that this species may be particularly important in moving pollen among populations.     

Pollination ecology of Stenocereus queretaroensis (Cactaceae), a chiropterophilous columnar cactus, in a tropical dry forest of Mexico

Flowers of columnar cacti are animal-pollinated, often displaying a chiropterophylic syndrome. This study examined if the columnar cactus Stenocereus queretaroensis, a tropical species endemic to western Mexico, is bat-pollinated, by studying its pollination biology and the foraging behavior of potential pollinators. Flowers were produced in winter through spring, peaking in April. Anthesis was nocturnal, and stigma and anther turgidity began around 2200 hours. Production of nectar secretion and highest sugar concentration and energy supply were nocturnal, peaking between 2200 and 2400 hours. Manual auto-pollination and exclusion experiments showed that self-pollination yielded no fruits, while nocturnal pollinators resulted in high fruit set and seed set compared to diurnal pollination treatments. The nectar-feeding bat Leptonycteris curasoae (Phyllostomidae) was the main nocturnal pollinator with the highest effective pollination. Peak bat visitation coincided with peaks in nectar production. The high abundance of L. curasoae throughout the 4-yr study, suggests that it is a seasonally reliable pollinator for this columnar cactus. While pollination syndromes have been increasingly called into question in recent years, this study suggests that at least for this system, there is a fairly close fit between pollinator and pollination syndrome.     

Population genetic structure of Venezuelan chiropterophilous columnar cacti (Cactaceae)

We conducted allozyme surveys of three Venezuelan self-incompatible chiropterophilous columnar cacti: two diploid species, Stenocereus griseus and Cereus repandus, and one tetraploid, Pilosocereus lanuginosus. The three cacti are pollinated by bats, and both bats and birds disperse seeds. Population sampling comprised two spatial scales: all Venezuelan arid zones (macrogeographic) and two arid regions in northwestern Venezuela (regional). Ten to 15 populations and 17-23 loci were analyzed per species. Estimates of genetic diversity were compared with those of other allozyme surveys in the Cactaceae to examine how bat-mediated gene dispersal affects the population genetic attributes of the three cacti. Genetic diversity was high for both diploid (P(s) = 94.1-100, P(p) = 56.7-72.3, H(s) = 0.182-0.242, H(p) = 0.161-0.205) and tetraploid (P(s) = 93.1, P(p) = 76.1, H(s) = 0.274, H(p) = 0.253) species. Within-population heterozygote deficit was detected in the three cacti at macrogeographic (F(IS) = 0.145-0.182) and regional (F(IS) = 0.057-0.174) levels. Low genetic differentiation was detected at both macrogeographic (G(ST) = 0.043-0.126) and regional (G(ST) = 0.009-0.061) levels for the three species, suggesting substantial gene flow among populations. Gene exchange among populations seems to be regulated by distance among populations. Our results support the hypothesis that bat-mediated gene dispersal confers high levels of genetic exchange among populations of the three columnar cacti, a process that enhances levels of genetic diversity within their populations.     

沈阳地区气传致敏花粉探讨

本文报道在沈阳地区1965—1985年间于空气中间断收集大气花粉5年,共收花粉玻片1100张,花粉45780粒,属于24科37属或种。其中9种(或属)超过千粒,为优势种类花粉。每年沈阳市大气中花粉出现两个高峰,一个为春季(四、五月),另一个为夏秋季(七八月)。通过长期观察发现,花粉种类和数量每年虽有不同,伹差异不大,唯有豚草花粉消长明显。大气中花粉种类及数量的变化往往受到气温、国家有关绿化政策以及社会风气的影响。花粉与过敏症关系十分密切,我们采用17种花粉制成浸液为病人皮试和治疗。皮试结果阳性率最高的为蒿属花粉,其次为其它夏秋花粉,春季花粉阳性率不高,致敏性不强。用花粉浸液对过敏症者进行免疫治疗,收到一定的疗效。     

Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora

In the tropical dry forest of the central Pacific coast of Mexico the pollination and reproductive success of the bombacaceous tree Ceiba grandiflora was negatively affected by habitat disruption. Two of the three bat species that function as effective pollinators for this species ( Glossophaga soricina and Musonycteris harrisoni) visited flowers found in trees in disturbed habitats significantly less than trees found in undisturbed habitats. A similar pattern was observed for the effective bat pollinator, Leptonycteris curasoae; however the difference was not significant. The three nectarivorous bats that functioned as effective pollinators of C. grandiflora also visited flowers to exclusively feed on pollen by biting or pulling off an anther (see Fig. S1 of Electronic Supplementary Material). The number of pollen grains deposited on stigmas from flowers in undisturbed areas was significantly greater than from flowers in disturbed habitats. The greater visitation rate and the greater number of pollen grains deposited on flowers from trees in undisturbed forest resulted in a significantly greater fruit set for trees in these areas. Our study demonstrates the negative effect that habitat disruption has on bat pollinators in tropical dry forest ecosystems and documents the negative consequences for the plants they pollinate.     

Studies on Atmosphere Spores and Pollen and Their Influences on the Sporopollen Assemblages in the Sediments of Huanghai Sea

Totally, 321 grains of spores and pollens which consist of 23 genera and species, were collected from the atmosphere over Huanghai Sea during the survey in 1978–1979. It has been found that the amount of spores and pollen in the atmosphere was high in spring, lower in autumn and the lowest in summer and winter. The content of arboreal pollens amount to 74%, with 23% of herbaceous pollens and SM of spores. By comparing the spores and pollens in the atmosphere with those in the marine sedments it was revealed that they were well correlated but the former influences distinctly to the distribution of the latter, thus making a high content of herbaceous pollens in the sporopollen distributions in the marine sediments nearshore area and high content of arboreal pollens in area far from the coast.     

Banksia pollen in the diet of Australian mammals

Mammals are frequent visitors to flowers in some Australian plant communities Nectar is usually considered to be the food sought, because pollen is thought to be of low digestibility This study compared the abilities of four non-flying mammal species to extract the protoplasts from Banksia pollen grains and quantified the amount of pollen in the diets of the species over 16 months All four species were capable of extracting the protoplast from a large proportion of the pollen grains that they ingested the mean percentage of empty Banksia pollen grains in the faeces ranged from 37% to 66% Banksia pollen was a major component in the faecal samples from two species, Cercartetus nanus and Petaurus breviceps , between March and October It occasionally comprised a large proportion of Amechmus stuartti faeces but was rare in the faeces of Rattus fuscipes Other major components of faeces included invertebrates and plant material other than pollen and fungal spores As the four mammal species tested were all from separate families and all capable of extracting the protoplast from a large proportion of the pollen grains, it is concluded that the extraction of pollen protoplasts by mammals may be widespread and may require no special adaptations     

Specialization clines in the pollination systems of agaves (Agavaceae) and columnar cacti (Cactaceae): A phylogenetically controlled meta-analysis

The biogeography of plant-animal interactions is a novel topic on which many disciplines converge (e.g., reproductive biology, biogeography, and evolutionary biology). Narrative reviews have indicated that tropical columnar cacti and agaves have highly specialized pollination systems, while extratropical species have generalized systems. However, this dichotomy has never been quantitatively tested. We tested this hypothesis using traditional and phylogenetically informed meta-analysis. Three effect sizes were estimated from the literature: diurnal, nocturnal, and hand cross-pollination (an indicator of pollen limitation). Columnar cactus pollination systems ranged from purely bat-pollinated in the tropics to generalized pollination, with diurnal visitors as effective as nocturnal visitors in extratropical regions; even when phylogenetic relatedness among species is taken into account. Metaregressions identified a latitudinal increase in pollen limitation in columnar cacti, but this increase was not significant after correcting for phylogeny. The currently available data for agaves do not support any latitudinal trend. Nectar production of columnar cacti varied with latitude. Although this variation is positively correlated with pollination by diurnal visitors, it is influenced by phylogeny. The degree of specificity in the pollination systems of columnar cacti is heavily influenced by ecological factors and has a predictable geographic pattern.     

Pollination system of the Pilosocereus leucocephalus columnar cactus (tribe Cereeae) in eastern Mexico

It has been suggested that there is a geographic dichotomy in the pollination systems of chiropterophilous columnar cacti: in intra‐tropical areas they are pollinated almost exclusively by bats, whereas in extratropical areas they are pollinated by bats, birds and bees. However, currently the studies are clumped both taxonomically (mainly Pachycereeae species) and geographically (mainly in the Tehuacan Valley and the Sonoran Desert). This clumping limits the possibility of generalising the pattern to other regions or cactus tribes. Only four of the 36 chiropterophilous cacti in Pilosocereus have been studied. Despite the tropical distribution of two Pilosocereus species, bees account for 40–100% of their fruit set. We examined how specialised is the pollination system of P. leucocephalus in eastern Mexico. As we studied tropical populations, we expected a bat‐specialised pollination system. However, previous studies of Pilosocereus suggest that a generalised pollination system is also possible. We found that this cactus is mainly bat‐pollinated (bats account for 33–65% of fruit set); although to a lesser degree, diurnal visitors also caused some fruit set (7–15%). Diurnal visitors were more effective in populations containing honeybee hives. P. leucocephalus is partially self‐compatible (14–18% of fructification) but unable to set fruit without visitors. Despite the variation in pollination system, P. leucocephalus shows more affinity with other columnar cacti from tropical regions than with those from extratropical regions. Although we report here that a new species of tropical Pilosocereus is relatively bat‐specialised, this Cereeae genus is more flexible in its pollination system than the Pachycereeae genera.     

Shape and Size Modification of Recent Pollen Grains under Acetolysis

In this paper, the shape and size modification of recent pollen grains have been studied. 63 species of recent pollen grains that belongs to 55 genera, 26 families were observed before and after the acetolysis treatment with LM. The length of polar axis and equatorial axis and the thickness of exine were measured from about 20 pollen grains for each species (the thickness of exine were only measured for acetolysed pollen grains). The significance of shape and size modification was examined with the statistical method "ttest". From this investigati0n it can be concluded that: The pollen modification in size and shape 'was related to aperture type, pollen size, wall thickness and sculpture depth. Pantoporate, spheroidal pollens and small perporlate pollens usually change little in there size and shape after acetolysis. The size of colpate pollens was generally increased, or their shape changed. The size or shape change usually got bigger as the pollen size, wall thickness and sculpture depth became bigger and bigger. Oblate pollens were apter to change their size and shape than prolate pollens. The P/E ratio of most colpate pollens became a little bigger after acetolysis.     

北京城区气传花粉季节分布特征

研究北京城区气传花粉种类、数量及季节消长规律,为防治花粉症及建设合理城市绿地提供有效资料.应用Burkard采样器于2010年12月31日至2011年12月31日对北京城区气传花粉浓度进行监测,并对花粉浓度进行统计学分析.研究结果显示,2011年北京城区的花粉季节从3月20日起始,至10月18日截止,持续213d,占全年天数的58％;全年花粉含量月分布呈现两个高峰,第1个高峰为3-4月,主要花粉为木犀科、杨属、柳属等树木花粉,占全年花粉总量的30％;第2个高峰为8-9月,主要花粉为菊科、藜科及苋科等莠草花粉,占全年花粉总量的50％;2011年度北京城区最具代表性的气传花粉来自于菊科,比重占了收集到气传花粉的35％.研究结果还表明,秋季的气传花粉致敏性强,所以北京花粉症的高发季节主要集中在秋季,以8-9月为最高,其中有95％的病人在此期间出现花粉症症状.花粉浓度及飘散规律受当地植被状况及气候等多种因素影响,因此,北京城区空气中气传花粉飘散种类、数量及季节分布规律的调查结果,可以为本地区花粉症防治及绿化品种的选择提供可靠依据.     

Patterns of frugivory in the columnar cactus Pilosocereus leucocephalus

In the frugivory networks of many arid and semi‐arid Mesoamerican ecosystems, columnar cacti act as keystone species that produce fruits with a high content of water and nutrients attractive to numerous vertebrates. The aim of this investigation was to assess the fruit removal patterns of two guilds of frugivores on the fruits of the woolly torch Pilosocereus leucocephalus. We assessed fruit pulp removal in two ways: by estimating the consumption of seeds given the amount of pulp removed per visit and by estimating the percentage of pulp removal over time. We put exclosures on unripe, intact fruits to keep frugivores from removing material. Once ripe, we removed the exclosures and tracked animal visitation of 69 fruits using camera traps. We obtained a total of 2,162 hr of footage (14:47 hours of them with effective pulp removal). The highest number of visitors is that of diurnal species (n = 12, all birds) versus only four nocturnal (three bats, one rodent). The most effective species in pulp removal are birds. Bats play a modest role in frugivory of this cactus. The significance of this work is twofold: (a) birds and bats consume the fruit pulp of this cactus and likely disperse its seeds, and (b) although bats rank high in pulp removal effectiveness, birds as a guild far outweigh their importance in this system, as they are not only more frequent but also remove more pulp and seeds. Both groups are known to be important in cacti seed dispersal, and our findings are essential in understanding the population dynamics of the woolly torch and in elucidating its seed dispersal ecology.     

Geographic differentiation in the pollination system of the columnar cactus Pachycereus pecten -aboriginum

The pollination biology of the cactus Pachycereus pecten-aboriginum was studied in a tropical location in western Mexico (ca. 18° N latitude) to compare with data from a northern population (ca. 28° N latitude). Throughout this range, the nectar-feeding bat Leptonycteris curasoae is resident within the tropics but migratory in its northern range. The hypothesis was tested that if a predictable bat presence has been an important force in the evolution of pollination systems in columnar cacti, P. pecten-aboriginum will have a specialized pollination system within the tropics and a generalized pollination system in northern populations. In both areas, pollination experiments showed that P. pecten-aboriginum has a self-incompatible, hermaphroditic breeding system. In the tropical area, flowers open at night and close early in the morning. Nectar is secreted only during the night, and flowers are exclusively pollinated by three species of nectar-feeding bats, indicating a specialized pollination system. In contrast, anthesis and nectar secretion in northern populations occur during the night and day, allowing visitation and effective pollination by both nocturnal and diurnal pollinators. This study provides evidence of divergence mediated by pollinator predictability (resident vs. migrant), through shifts from short to long anthesis and nectar production periods from southern to northern populations.     

In vitro pollen germination in Hypericum perforatum L. and Hypericum rumeliacum Boiss

In vitro pollen germination and pollen tube growth investigations are valuable tools used in identification of the effects of environmental factors and genotypic differences on pollen viability, pollen germination and tube elongation. In this study pollen viability, in vitro pollen germination capacity, abnormality ratios and tube length in germinated pollens of Hypericum perforatum L. and H. rumeliacum Boiss. were investigated. Both of these species has spheroid-shaped and tricolporate pollen grains. The diameters of Hypericum perforatum and H. rumeliacum pollens were found as 24 +/- 3 microm and 19 +/- 2 microm, respectively. Pollen viability of H. perforatum and H. rumeliacum was found as 83% and 72%, respectively. The germination percentages were found as 12.85% for H. perforatum and 64.42% for H. rumeliacurm. Tube lengths in germinated pollens of both taxa were measured approximately as 95.25 +/- 38 microm in H. perforatum and 165.92 +/- 53 microm in H. rumeliacium 4 h after inoculation. In germinated pollen grains of H. perlbratum and H. rumeliacumn abnormality percentages were determined as 13.23% and 43.97%, respectively. In germinated pollens of these two species, highly significant (P < 0.00001) differences in in vitro germination percents and abnormality percents were observed. Abnormalities such as swollen tube tip, branched tube, spiralled tube and excessive tube formation were observed in pollen tubes. The results of this study showed that there were obvious differences in pollen germinability between these two species growing under the same environmental conditions.