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.     

Reproductive ecology of <Emphasis Type="Italic">Agave colorata</Emphasis>: the importance of nectar-feeding bats and the germination consequences of self-pollination

Agave colorata is a paniculate agave distributed along the migratory route of the nectar-feeding bat Leptonycteris yerbabuenae. In this paper, we evaluate the importance of nectar-feeding bats in the reproduction of A. colorata in a population in Sonora, Mexico, and describe the germination consequences of self-pollination. We estimated abundance using five plots and set pollination treatments to evaluate the importance of bats. We recorded 14.8?±?6.8 plants/400 m², with a bimodal size distribution. Flowers are protandrous and visited mainly (>?20 visits/plant/30 min) by L. yerbabuenae. Pollination exclusion experiments showed that flowers excluded from diurnal visitors had maximum fruit set values (0.49?±?0.42), while the autonomous self-pollination treatment had the lowest value (0.03?±?0.06). Similarly, the greatest number of viable seeds per fruit was recorded in the diurnal exclusion treatment, while the greatest number of empty seeds was observed in the self-pollination treatment. Fruit set values among untreated plants varied from 32 to 54%, with a mean value of 41.8%. Seeds derived from self-pollination had a narrower window of opportunity for germination compared to seeds derived from nocturnal pollination. Self-pollinated seeds had lower germination, rate of germination or lag time in response to light, osmotic potential and heat shock treatments, compared to other pollination treatments, revealing an inbreeding cost. Overall, our results show that L. yerbabuenae is the likely major pollinator of the studied A. colorata population. However, under pollinator limitation A. colorata may produce seeds by autonomous self-pollination, at a cost expressed as lower germination.     

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.     

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.     

Reproductive biology of Pachira aquatica Aubl. (Malvaceae: Bombacoideae): a tropical tree pollinated by bats,sphingid moths and honey bees

We investigated the reproductive biology, including the floral biology, pollination biology, breeding system and reproductive success, of Pachira aquatica, a native and dominant tropical tree of fresh water wetlands, throughout the coastal plain of the Gulf of Mexico. The flowers present nocturnal anthesis, copious nectar production and sugar concentration (range 18–23%) suitable for nocturnal visitors such as bats and sphingid moths. The main nocturnal visitors were bats and sphingid moths while bees were the main diurnal visitors. There were no differences in legitimate visitation rates among bats, moths and honey bees. Bats and honey bees fed mainly on pollen while moths fed on nectar, suggesting resource partitioning. Eight species of bats carried pollen but Leptonycteris yerbabuenae is probably the most effective pollinator due to its higher pollen loads. The sphingid moths Manduca rustica, Cocytius duponchel and Eumorpha satellitia were recorded visiting flowers. Hand pollination experiments indicated a predominant outcrossing breeding system. Open pollination experiments resulted in a null fruit set, indicating pollen limitation; however, mean reproductive success, according to a seasonal census, was 17 ± 3%; these contrasting results could be explained by the seasonal availability of pollinators. We conclude that P. aquatica is an outcrossing species with a pollination system originally specialized for bats and sphingid moths, which could be driven to a multimodal pollination system due to the introduction of honey bees to tropical America.     

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.     

Reproductive biology and the process of domestication of the columnar cactus Stenocereus Stellatus in Central Mexico

Pollination biology, breeding system, and floral phenology of the columnar cactus Stenocereus stellatus were studied in wild, wild managed in situ and cultivated populations of central Mexico, in order to examine whether these aspects have been modified under domestication and whether they determine reproductive barriers between wild and manipulated individuals. Individuals of both wild and manipulated populations are self-incompatible, indicating that artificial selection has not modified the breeding system. Their pollination biology is also similar. Anthesis is mainly nocturnal, with a peak of nectar production between 0200 and 0400 when the stigma presents maximum turgidity. Nocturnal visitors are the effective pollinators. Nearly 75% of flowers exposed for nocturnal pollination set fruit, while none of the flowers exposed for diurnal pollination produced fruits. The bats Leptonycteris curasoae, L. nivalis, and Choeronycteris mexicana (Glossophaginae) are the most likely pollinators, and their time of foraging is synchronized with the time of nectar production and stigma receptivity in S. stellatus. Bats potentially move pollen over a considerable distance, so there is apparently no spatial isolation to prevent pollen exchange between wild and cultivated populations. Phenological studies showed that there are also no apparent temporal barriers. However, manual cross pollination failed between some domesticated and wild phenotypes, suggesting that gene flow between wild and cultivated populations might be limited by pollen incompatibility.     

Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis

Three species of nectar-feeding bats migrate from tropical and subtropical Mexico into the Sonoran and Chihuahuan deserts during the spring and summer months. We examined geographic and seasonal changes in the diet of one migrant species, Leptonycteris curasoae, using carbon stable isotope techniques to determine the relative importance of C3 and CAM (Cactaceae, Agavaceae) plants in its diet. We also examined the diet of a non-migratory nectar-feeding bat, Glossophaga soricina, from southern Mexico using the same techniques. We found that L. curasoae feeds extensively or exclusively on CAM plants during migration and in the northern part of its range and feeds mostly on C3 plants in southern Mexico. This bat is a year-round resident on Baja California where it is a CAM specialist. The non-migrant G. soricina feeds mostly on C3 plants year-round. Phenological data suggest that certain species of columnar cacti and at least one group of paniculate Agaves on the Mexican mainland provide a spatio-temporally predictable nectar corridor along which nectarivorous bats may migrate in the spring and fall, respectively. Different flowering schedules of Agaves in Baja California appear to promote year-round dietary specialization and perhaps non-migratory behavior in nectar-feeding bats living there.     

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.     

Geographic variation in the breeding system and the evolutionary stability of trioecy in Pachycereus pringlei (Cactaceae)

The Sonoran Desert columnar cactus Pachycereus pringlei has a geographically variable, non-hermaphroditic breeding system. It is trioecious (separate males, females and hermaphrodites) in the northern two-thirds of its range in Sonora, Mexico, and in the southern three-quarters of its range in Baja California, Mexico, and is gynodioecious (separate females and hermaphrodites) elsewhere. Trioecy occurs near known maternity roosts of its major pollinator, the nectar-feeding bat Leptonycteris curasoae; gynodioecy occurs>50km from known bat roosts. The observed geographic patterns cannot be explained by limited gene flow or by the geographic distributions of diurnal avian pollinators. Our field observations plus a theoretical analysis suggest that the abundance of chiropteran pollinators plays an important role in the maintenance of trioecy in this plant. Under pollinator limitation, trioecy can be a stable breeding system in this species. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Contribution of diurnal and nocturnal insects to the pollination of Jatropha curcas (Euphorbiaceae) in southwestern China

Jatropha curcas L. (Euphorbiaceae) is being increasingly planted worldwide, but questions remain regarding its pollination biology. This study examined the contribution of diurnal and nocturnal insects to the pollination of monoecious J. curcas, through its floral biology, pollination ecology, and foraging behavior of potential pollinators. Nectar production of both male and female flowers peaked in the morning, declined in the afternoon, and rapidly bottomed during the night in all of their anthesis days. The diurnal visitors to the flowers of J. curcas are bees and flies, and the nocturnal visitors are moths. Flowers received significantly more visits by diurnal insects than by nocturnal insects. Through bagging flowers during night or day or both or exclusion, we compared fruit and seed production caused by diurnal and nocturnal pollinators. Both nocturnal and diurnal visitors were successful pollinators. However, flowers exposed only to nocturnal visitors produced less fruits than those exposed only to diurnal visitors. Thus, diurnal pollinators contribute more to seed production by J. curcas at the study site.     

Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators

The aim of this study was to analyse the reproductive biology of Echinopsis terscheckii, a species endemic to northwest Argentina that has nocturnal flowers. We expected that this species had a generalised pollination system, with moths and diurnal visitors as the primary pollinators. To test this, we studied the floral biology, breeding system and floral visitors of this species and the effectiveness of nocturnal and diurnal visitors. Floral biology was defined based on floral morphology, floral cycle and nectar production of the flowers. The breeding system and relative contributions of diurnal and nocturnal visitors to fruit and seed set were analysed through field experiments. E.?terscheckii flowers opened at sunset and closed the following day. The peak of nectar production occurred at midnight. Flowers were determined to be self-incompatible. Moths, bees and birds were identified as floral visitors. Moths were the most frequent visitors at night, whereas bees were the most frequent visitors during the day. Fruit production by diurnal pollinators was less than that by nocturnal pollinators; among all floral visitors, moths were the most effective pollinators. We have demonstrated for the first time that moths are the primary pollinators of columnar cacti of the genus Echinopsis. Our results suggest that moths might be important pollinators of columnar cactus species with nocturnal flowers in the extra-tropical deserts of South America.     

The evolution of bat pollination: a phylogenetic perspective

Background

Most tropical and subtropical plants are biotically pollinated, and insects are the major pollinators. A small but ecologically and economically important group of plants classified in 28 orders, 67 families and about 528 species of angiosperms are pollinated by nectar-feeding bats. From a phylogenetic perspective this is a derived pollination mode involving a relatively large and energetically expensive pollinator. Here its ecological and evolutionary consequences are explored.

Scope and Conclusions

This review summarizes adaptations in bats and plants that facilitate this interaction and discusses the evolution of bat pollination from a plant phylogenetic perspective. Two families of bats contain specialized flower visitors, one in the Old World and one in the New World. Adaptation to pollination by bats has evolved independently many times from a variety of ancestral conditions, including insect-, bird- and non-volant mammal-pollination. Bat pollination predominates in very few families but is relatively common in certain angiosperm subfamilies and tribes. We propose that flower-visiting bats provide two important benefits to plants: they deposit large amounts of pollen and a variety of pollen genotypes on plant stigmas and, compared with many other pollinators, they are long-distance pollen dispersers. Bat pollination tends to occur in plants that occur in low densities and in lineages producing large flowers. In highly fragmented tropical habitats, nectar bats play an important role in maintaining the genetic continuity of plant populations and thus have considerable conservation value.     

Generalized and complementary pollination system in the Andean cactus Echinopsis schickendantzii

The considerable floral diversity present in the cactus family has often been associated with the specificity of its pollinators. However, many cactus pollination systems are generalized as their flowers are pollinated by a wide spectrum of animals. For example, cactus species with white flowers, nocturnal anthesis and extended floral cycles would present generalized pollination systems in which both nocturnal and diurnal visitors could be effective pollinators. In this article, we tested this hypothesis by studying the pollination biology of Echinopsis schickendantzii, an Andean cactus with sphingophilous flowers. In addition, we evaluated whether the cactus’s pollination system is complementary or redundant regarding the relative contributions of nocturnal and diurnal pollinators. Specifically, we studied the floral cycle, the reproductive system and the pollination effectiveness of floral visitors. The flowers of E. schickendantzii are self-incompatible; they opened at crepuscule and have an extended floral cycle. Moths were frequent visitors at night, whereas bees were frequent visitors during the day; both were effective pollinators of the cactus. Our results indicated that the flowers of this species present phenotypic, functional and ecological generalization, and their fruit set is determined by the contributions of both pollinator functional groups, i.e., they have complementary pollination systems. These results support the hypothesis that cacti in the extra-tropical deserts of South America have generalized pollination systems.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.     

Diurnal and nocturnal pollination of Marginatocereus marginatus (Pachycereeae: Cactaceae) in Central Mexico

BACKGROUND AND AIMS: Chiropterophillous and ornithophillous characteristics can form part of a single reproductive strategy in plants that have flowers with diurnal and nocturnal anthesis. This broader pollination strategy can ensure seed set when pollinators are scarce or unpredictable. This appears to be true of hummingbirds, which presumably pollinate Marginatocereus marginatus, a columnar cactus with red nocturnal and diurnal flowers growing as part of dense bat-pollinated columnar cacti forests in arid regions of central Mexico. The aim of this study was to study the floral biology of M. marginatus, and evaluate the effectiveness of nocturnal vs. diurnal pollinators and the contribution of each pollinator group to overall plant fitness. METHODS: Individual flower buds were marked and followed to evaluate flower phenology and anthesis time. Flowers and nectar production were measured. An exclusion experiment was conducted to measure the relative contribution of nocturnal and diurnal pollinators to seed set. KEY RESULTS: Marginatocereus marginatus has red hermaphroditic flowers with nocturnal and diurnal anthesis. The plant cannot produce seeds by selfing and was pollinated during the day by hummingbirds and during the night by bats, demonstrating that both pollinator groups were important for plant reproduction. Strong pollen limitation was found in the absence of one of the pollinator guilds. CONCLUSIONS: Marginatocereus marginatus has an open pollination system in which both diurnal and nocturnal pollinators are needed to set seeds. This represents a fail-safe pollination system that can ensure both pollination, in a situation of low abundance of one of the pollinator groups (hummingbirds), and high competition for nocturnal pollinators with other columnar cacti that bloom synchronously with M. marginatus in the Tehuacan Valley, Mexico.     

First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae)

Background and Aims

Bromeliaceae is a species-rich neotropical plant family that uses a variety of pollinators, principally vertebrates. Tillandsia is the most diverse genus, and includes more than one-third of all bromeliad species. Within this genus, the majority of species rely on diurnal pollination by hummingbirds; however, the flowers of some Tillandsia species show some characteristics typical for pollination by nocturnal animals, particularly bats and moths. In this study an examination is made of the floral and reproductive biology of the epiphytic bromeliad Tillandsia macropetala in a fragment of humid montane forest in central Veracruz, Mexico.

Methods

The reproductive system of the species, duration of anthesis, production of nectar and floral scent, as well as diurnal and nocturnal floral visitors and their effectiveness in pollination were determined.

Key Results

Tillandsia macropetala is a self-compatible species that achieves a higher fruit production through outcrossing. Nectar production is restricted to the night, and only nocturnal visits result in the development of fruits. The most frequent visitor (75 % of visits) and the only pollinator of this bromeliad (in 96 % of visits) was the nectarivorous bat Anoura geoffroyi (Phyllostomidae: Glossophaginae).

Conclusions

This is the first report of chiropterophily within the genus Tillandsia. The results on the pollination biology of this bromeliad suggest an ongoing evolutionary switch from pollination by birds or moths to bats.     

Relative importance of diurnal and nocturnal pollinators for reproduction in the early spring flowering shrub Stachyurus praecox (Stachyuraceae)

Generalized pollination systems may be favored in early spring flowering plants, as during this period pollinator activity is unpredictable. Many previous studies have concentrated on the importance of diurnal visitors in pollination, and consequently, information on the contribution of nocturnal visitors to pollination in early spring is limited. This study was conducted to evaluate the relative importance of diurnal and nocturnal pollinators in the early spring flowering dioecious shrub Stachyurus praecox (Stachyuraceae), in two temperate forests in central Japan. Visitors to the female and male flowers were observed during day and night, and their relative contributions to seed set were compared. The pollinator observations revealed that the diurnal and nocturnal insects visited both male and female flowers, and that the main flower visitors were diurnal small bees and flies as well as nocturnal settling moths. The diurnal and nocturnal flower visitors also acted as pollinators, as the pollen grains of S. praecox were attached to the insects collected from the female flowers. Pollination experiments demonstrated that the contributions of diurnal pollinators to the seed set were higher than those of the nocturnal pollinators. The results of this study indicate that S. praecox has a generalized pollination system, comprising both diurnal insects and nocturnal settling moths. Although the roles of diurnal insects are more important in the pollination of S. praecox, nocturnal settling moths may have a complementary role in early spring.