Resource competition triggers the co-evolution of long tongues and deep corolla tubes

Background

It is normally thought that deep corolla tubes evolve when a plant''s successful reproduction is contingent on having a corolla tube longer than the tongue of the flower''s pollinators, and that pollinators evolve ever-longer tongues because individuals with longer tongues can obtain more nectar from flowers. A recent model shows that, in the presence of pollinators with long and short tongues that experience resource competition, coexisting plant species can diverge in corolla-tube depth, because this increases the proportion of pollen grains that lands on co-specific flowers.

Methodology/Principal Findings

We have extended the model to study whether resource competition can trigger the co-evolution of tongue length and corolla-tube depth. Starting with two plant and two pollinator species, all of them having the same distribution of tongue length or corolla-tube depth, we show that variability in corolla-tube depth leads to divergence in tongue length, provided that increasing tongue length is not equally costly for both species. Once the two pollinator species differ in tongue length, divergence in corolla-tube depth between the two plant species ensues.

Conclusions/Significance

Co-evolution between tongue length and corolla-tube depth is a robust outcome of the model, obtained for a wide range of parameter values, but it requires that tongue elongation is substantially easier for one pollinator species than for the other, that pollinators follow a near-optimal foraging strategy, that pollinators experience competition for resources and that plants experience pollination limitation.     

Pollination in Lilium sargentiae (Liliaceae) and the first confirmation of long‐tongued hawkmoths as a pollinator niche in Asia

The geographical distribution of pollinators is an important factor determining the biogeographical pattern of floral evolution and diversification. In Africa, a guild of plant species has converged in a floral syndrome for pollination by long‐tongued hawkmoths (predominantly Agrius convolvuli). It is hypothesized that such floral convergence could track the geographical distribution of long‐tongued hawkmoths, so it may not be confined to Africa. We investigated the pollination biology of Lilium sargentiae E. H. Wilson, which is endemic to China and exhibits traits suggestive of long‐tongued hawkmoth pollination. Lilium sargentiae was visited by A. convolvuli as well as small beetles (Nitidulidae) but pollination was mostly or totally effected by the moth. It was consistent with other hawkmoth‐pollinated plants in terms of floral tube length, nectar traits, tepal reflectance, and scent composition. We present the first experimental evidence for the hypothesis proposed above and for hawkmoth pollination in the widespread and ornamentally and economically important genus Lilium L. in a natural habitat. Our findings imply that long‐tongued hawkmoths (especially the extremely widespread A. convolvuli) as a distinctive pollinator niche may have underlain the evolution of long‐tubed (>8 cm) flowers across different continents.     

Reproductive biology of two Himalayan alpine gingers (Roscoea spp., Zingiberaceae) in China: pollination syndrome and compensatory floral mechanisms

According to the concept of pollination syndromes, floral traits reflect specialisation to a particular pollinator or set of pollinators. However, the reproductive biology of endemic, and often specialised, plants may require increased attention as climate change accelerates worldwide. Species of Roscoea endemic to the Himalayan region have striking orchid-like flowers with long corolla tubes, suggesting pollination by long-tongued insects. Until now, the reproductive biology of species of Roscoea has been poorly documented. We investigated the floral biology, breeding system and pollination ecology of R. cautleoides and R. humeana, from Hengduan Mountains, a global biodiversity hotspot in southwest China. We also tested whether floral longevity increases pollination success. Pollination experiments showed that the two species were self-compatible and depended on insects for fruit production. Over several flowering seasons we did not observe any potential pollinators with long tongues that matched the corolla tube visiting flowers in centres of distribution. The principal pollinators observed were pollen-collecting generalist bees, with low visitation frequencies. In general, members of the ginger family are characterised by short-lived (usually 1 day) flowers, but flowers of R. cautleoides and R. humeana last 8 and 6 days, respectively. Removing stigmas decreased fruit set in both study populations. Our results suggest that the original pollinators may have been long-tongued insects that are now absent from the Chinese Himalayas because habitats have responded to climate change. However, long-lived and self-compatible flowers, coupled with the presence of generalist pollinators, are traits that have allowed these gingers to reproduce and continue to persist in the alpine habitats.     

Relative contributions to seed production by floral visitors of slickspot peppergrass, Lepidium papilliferum (Brassicaceae)

Assessing the relative contributions to seed production made by different types of floral visitors is fundamental to understanding the evolution of floral morphology and the influence that particular pollinator taxa have on plant fitness and reproduction. This 3-year study examined the pollinator activity and the seed production in three populations of Lepidium papilliferum, a threatened mustard endemic to sagebrush-steppe habitat in southwest Idaho. Relative amounts of time visitor taxa spent foraging on flowers, visitation rates (number of flowers visited per unit time during a foraging bout), and pollination effectiveness (fruit set per single visit to a virgin flower) were recorded for each of 12 insect taxa that visited L. papilliferum flowers. Relative contributions to seed production were calculated as the product of relative interaction frequencies (the relative number of flowers visited by each taxon—the “quantity” component of pollination) and pollination effectiveness (fruit set per single visit to a virgin flower—the “quality” component of pollination). Despite the superiority of some insect taxa in terms of pollination effectiveness, estimates of relative pollinator contributions to seed production were influenced primarily by an insect taxon’s interaction frequency with flowers. Pollinator assemblages varied widely both spatially and temporally, which suggest that L. papilliferum is not under strong selective pressure to shift from its generalist pollination strategy toward greater specialization. For this threatened plant, reliance on a diverse assemblage of insect pollinators may serve as an important buffer against disruption in reproductive success caused by fluctuations in population sizes of individual pollinator taxa.     

Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations

Pollination success of deceptive orchids is affected by the density and distribution of nectar providing plant species and overall plant density. Here we extended the framework of how plant density can affect pollination to examine how it may promote the success of plant intraspecific cheaters. We compared hawkmoth behaviour in two native populations of Petunia axillaris, where we simultaneously offered rewarding and manually depleted P. axillaris. We asked whether pollinator foraging strategies change as a function of plant density and whether such changes may differentially affect nectarless plants. We observed the first choice and number of flowers visited by pollinators and found that in the dense population, pollinators visited more flowers on rewarding plants than on nectar-depleted plants. In the sparse population, such discrimination was absent. As we found no differences in nectar volume between plants of the two populations, the observed differences in plant density may be temporal. We reason that if differences were more permanent, an equivalent of the remote habitat hypothesis prevails: in a sparse population, cheating plants benefit from the absence of inter- and intraspecific competitors because pollinators tend to visit all potential resources. In a denser population, a pollinator’s optimal foraging strategy involves more selectivity. This would cause between-plant competition for pollinators in a pollinator-limited context, which applies to most hawkmoth-pollinated systems. We propose that nectar-provisioning of plants can be density-dependant, with cheaters able to persist in low density areas.     

Is the timing of scent emission correlated with insect visitor activity and pollination in long‐spurred Satyrium species?

Plants are expected to emit floral scent when their pollinators are most active. In the case of long‐tubed flowers specialised for pollination by crepuscular or nocturnal moths, scent emissions would be expected to peak during dawn. Although this classic idea has existed for decades, it has rarely been tested quantitatively. We investigated the timing of flower visitation, pollination and floral scent emissions in six long‐spurred Satyrium species (Orchidaceae). We observed multiple evening visits by pollinaria‐bearing moths on flowers of all study species, but rarely any diurnal visits. The assemblages of moth pollinators differed among Satyrium species, even those that co‐flowered, and the lengths of moth tongues and floral nectar spurs were strongly correlated, suggesting that the available moth pollinator fauna is partitioned by floral traits. Pollinarium removal occurred more frequently during the night than during the day in four of the six species. Scent emission, however, was only significantly higher at dusk than midday in two species. Analysis of floral volatiles using gas chromatography coupled with mass spectrometry yielded 168 scent compounds, of which 112 were species‐specific. The scent blends emitted by each species occupy discrete clusters in two‐dimensional phenotype space, based on multivariate analysis. We conclude that these long‐spurred Satyrium species are ecologically specialised for moth pollination, yet the timing of their scent emission is not closely correlated with moth pollination activity. Scent composition was also more variable than expected from a group of closely related plants sharing the same pollinator functional group. These findings reveal a need for greater understanding of mechanisms of scent production and their constraints, as well as the underlying reasons for divergent scent chemistry among closely related plants.     

Change of floral orientation affects pollinator diversity and their relative importance in an alpine plant with generalized pollination system,Geranium refractum (Geraniaceae)

Floral orientation may affect pollinator attraction and pollination effectiveness, and its influences may differ among pollinator species. We, therefore, hypothesized that, for plant species with a generalized pollination system, changes in floral orientation would affect the composition of pollinators and their relative contribution to pollination. Geranium refractum, an alpine plant with downward floral orientation was used in this study. We created upward-facing flowers by altering the flower angle. We compared the pollinator diversity, pollination effectiveness, and pollinator importance, as well as female reproductive success between flowers with downward- and upward-facing orientation. Results indicated that the upward-facing flowers were visited by a wider spectrum of pollinators (classified into functional groups), with higher pollinator diversity than natural flowers. Moreover, due to influences on visitation number and pollen removal, the pollinator importance exhibited by the main pollinator groups differed between flower types. Compared with natural flowers, the pollination contribution of principal pollinators (i.e., bumblebees) decreased in upward-facing flowers and other infrequent pollinators, such as solitary bees and muscoid flies, removed more pollen. Consequently, stigmatic pollen loads were lower in upward- than in downward-facing flowers. These findings reveal that floral orientation may affect the level of generalization of a pollination system and the relative importance of diverse pollinators. In this species, the natural downward-facing floral orientation may increase pollen transfer by effective pollinators and reduce interference by inferior pollinators.     

Pollinator individual‐based networks reveal the specialized plant–pollinator mutualism in two biodiverse communities

Generalization of pollination systems is widely accepted by ecologists in the studies of plant–pollinator interaction networks at the community level, but the degree of generalization of pollination networks remains largely unknown at the individual pollinator level. Using potential legitimate pollinators that were constantly visiting flowers in two alpine meadow communities, we analyzed the differences in the pollination network structure between the pollinator individual level and species level. The results showed that compared to the pollinator species‐based networks, the linkage density, interaction diversity, interaction evenness, the average plant linkage level, and interaction diversity increased, but connectance, degree of nestedness, the average of pollinator linkage level, and interaction diversity decreased in the pollinator individual‐based networks, indicating that pollinator individuals had a narrower food niche than their counterpart species. Pollination networks at the pollinator individual level were more specialized at the network level (H′₂) and the plant species node level (d′) than at the pollinator species‐level networks, reducing the chance of underestimating levels of specialization in pollination systems. The results emphasize that research into pollinator individual‐based pollination networks will improve our understanding of the pollination networks at the pollinator species level and the coevolution of flowering plants and pollinators.     

The influence of nectar production on hawkmoth behavior,self pollination,and seed production in Mirabilis multiflora (Nyctaginaceae)

Nectar is the most common floral reward that plants produce to attract pollinators. To determine the effect of nectar production on hawkmoth behavior, pollen movement, and reproductive success in Mirabilis multiflora, I manipulated nectar volumes and observed the subsequent foraging behavior of the hawkmoth Hyles lineata and the resulting pollen movement patterns. Individual hawkmoths visited significantly more flowers on plants with more nectar. The increase in flower visits significantly increased pollen deposition on stigmas and pollen removal from anthers when nectar volume was raised to twice the highest level found in nature. As hawkmoths visited flowers consecutively on a plant, the proportion of self pollen deposited on stigmas increased significantly and rapidly. Based on simulated hawkmoth visits, seed set was significantly reduced for flowers later in a visit sequence. A simple model combining these results predicts that the form of selection on nectar production varies depending on pollinator abundance. Using a multiple regression analysis a nearly significant (P < 0.08) effect of stabilizing selection was detected during a single season as predicted by the model for the prevailing hawkmoth abundance. Although increased nectar production may indirectly affect plant fitness by reducing resources available for other plant functions, the direct effect of high nectar production on pollinator behavior and self pollination may generally limit floral nectar production.     

Flower reshaping in the transition to hummingbird pollination in Loasaceae subfam. Loasoideae despite absence of corolla tubes or spurs

Many angiosperm lineages present transitions from bee to hummingbird pollination. The flower design in most of these lineages includes either corolla tubes or nectar spurs, structures that commonly experienced an elongation with the acquisition of hummingbird pollination. It is proposed that this increases the fit between the bird head and flower structures, and isolates or partially blocks bees from the interaction. But can this transition occur if the ancestral flower design lacks tubes or spurs? Here we focus on the transition from bee to hummingbird pollination in the Loasaceae subfamily Loasoideae. Loasoideae flowers have radial corollas with separated petals; therefore, they do not display corolla tubes nor nectar spurs. These flowers also present a whorl of nectar scales and staminodes, unique to the subfamily, which is involved in flower–pollinator fit and in nectar harvesting. To explore flower shape adaptation to hummingbird pollination, we tested for correspondence between pollinators and flower shape in Loasoideae. In order to achieve this, we first compared the evolutionary history of flower phenotype and pollination mode, and then used stochastic character mapping and geometric-morphometric variables in a comparison of alternative evolutionary models. The results of our study suggest that the transition from bee to bird pollination was accompanied by changes in the shape of the staminodial complex, along with the evolution of relatively closed corollas. Moreover, while bird pollination seems to be the end point in the evolution of pollination syndromes in many angiosperm lineages, rodent pollinated flowers probably evolved from ancestral bird pollinated flowers in Loasoideae. Our findings suggest that the evolution of bird pollinated flowers from ancestral bee pollinated flowers does not require the presence of corolla tubes or spurs, and can take place as long as the flower design includes structures participating in flower–pollinator fit.     

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

Secondary contact and adaptation to local pollinator assemblages mediate geographical variation in corolla length in Isodon shikokianus

Adaptation to local pollination regimes and secondary contact of allopatrically differentiated populations with respect to pollination ecology may result in geographical variation in floral traits. We examined the contributions of these two processes in Isodon shikokianus, which showed remarkable geographical variation in corolla tube length in western Japan. Corolla tube length varied among 17 study populations located within a relatively narrow area, and covaried with altitude and distribution of two bumblebee pollinators with different tongue lengths: the longer corolla was found at lower altitudes where the long-tongued pollinator was more abundant, and vice versa. Additionally, bumblebee species preferentially visited flowers that fit their tongue lengths. Population genetic analysis based on 11 microsatellite loci revealed that populations with long and short corolla tubes constituted genetically distinct groups. Migration rates were low between the groups, but high within each group. These results indicate that two genetically differentiated groups made secondary contact and hybridized, and gene flow between the groups was limited. Thus, the geographical variation in corolla tube length in I. shikokianus may be a result of past allopatric differentiation and subsequent secondary contact of populations with different corolla tube lengths. The variation in corolla tube length within a narrow area may be maintained by selection owing to the altitudinally structured pollinator assemblages. Altitudinal differences in relative abundance of two pollinators and their assortative visitation with respect to corolla tube length may contribute to reproductive isolation between the two groups.     

Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context

Hawkmoths (Lepidoptera, Sphingidae) are considered important pollinators in tropical regions, but the frequency and degree of reciprocal specialization of interactions between hawkmoths and flowers remain poorly understood. Detailed observations at two sites in Kenya over a two‐year period indicate that adult hawkmoths are routinely polyphagous and opportunistic, regardless of their proboscis length. About 700 individuals of 13 hawkmoth species were observed visiting a wide range of plant species at the study sites, including 25 taxa that appear to be specifically adapted for pollination by hawkmoths. We estimate that 277 plant species in Kenya (c. 4.61% of the total angiosperm flora) are adapted for pollination by hawkmoths. Floral tube lengths of these plants have a bimodal distribution, reflecting the existence of two hawkmoth guilds differing in tongue length. Hawkmoths exhibited strongly crepuscular foraging patterns with activity confined to a 20‐min period at dusk and, in some cases, a similar period just before dawn. Corolla tube length appears to act as a mechanical filter as the longest‐tubed plants were visited by the fewest hawkmoth species and these were exclusively from the long‐tongued guild. Tube length showed a strong positive relationship with nectar volume, even after phylogenetic correction, which implies that plants with long corolla tubes are under selection to offer relatively large amounts of nectar to entice visits by polyphagous long‐tongued hawkmoths. Our study shows that diffusely co‐evolved pollination systems involving long‐tongued hawkmoths are clearly asymmetrical, with plants exhibiting a high degree of floral specialization, while hawkmoths exhibit polyphagous behaviour. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 199–213.     

Speciation genes in the genus Petunia

A major innovation in angiosperms is the recruitment of animal pollinators as a means to enhance the efficiency and specificity of pollen transfer. The implementation of this reproductive strategy involved the rapid and presumably coordinated evolution of multiple floral traits. A major question concerns the molecular identity of the genetic polymorphisms that specify the phenotypic differences between distinct pollination syndromes. Here, we report on our work with Petunia, an attractive model system for quantitative plant genetics and genomics. From interspecific crosses, we obtained F2 plants that differed in the length of the floral tube or the size of the limb. We used these plants to study the behaviour of the hawkmoth pollinator, Manduca sexta. Plants with larger limbs were preferentially visited, consistent with the notion that flower size affects visibility under low light conditions. The moths also displayed an innate preference for shorter tubes. However, in those cases that flowers with long tubes were chosen, the animals fed for equal time. Thus, the perception of tube length may help the moths, early on, to avoid those plants that are more difficult to handle.     

Interaction frequency and per-interaction effects as predictors of total effects in plant–pollinator mutualisms: a case study with the self-incompatible herb <Emphasis Type="Italic">Linaria lilacina</Emphasis>

It is widely recognized that pollinators vary in their effectiveness in pollination mutualisms, due both to differences in flower–pollinator morphological fit as well as pollinator behaviour. However, pollination webs typically treat all interactions as equal, and we contend that this method may provide misleading results. Using empirical and theoretical data, we present the case study of a self-incompatible herb in which the number of flowers visited by a pollinator cannot be used as a surrogate for the total effect of a pollinator on a plant due to differences in per-visit effectiveness at producing seeds. In self-incompatible species, the relationship between interaction frequency and per-interaction effect may become increasingly negative as more flowers per plant are visited due to geitonogamous pollen transfer. We found that pollinators making longer bouts (i.e. visiting more flowers per plant visit) had an overall higher pollination success per bout. However, per-interaction effects tended to decrease as the bout progressed, particularly for pollinators that cause higher pollen deposition. Since the same interaction frequency may result from different combinations of number of bouts (plant visits) and bout length (flowers visited/bout), pollinators making repeatedly shorter bouts may contribute more to plant reproduction for the same number of flowers visited. Consequently, the magnitude of the differences in number of interactions of different insect types may be overridden by the magnitude of the differences in effectiveness as pollinators, even if the same pollinators consistently interact more frequently. We discuss two predictions regarding the validity of using interaction frequency as a surrogate for plant seed production (as a measure of total effect), depending on the degree of self-compatibility, plant size and floral display. We suggest that the role of interaction frequency must be tested for different species, environments, and across wider scales to validate its use as a surrogate for total effect in plant–pollinator networks.     

Pollinator-mediated selection on flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae)

Darwin's mechanistic model whereby selection favours plants with flower tubes that exceed the tongue length of the primary pollinator, was tested using unmanipulated plants of the hawkmoth-pollinated South African iris, Gladiolus longicollis. The study population was characterized by exceptionally large phenotypic variation in flower-tube length (range 56-129 mm). Directional selection on tube length was revealed by a significant positive relationship between this trait and both fruit and seed set. Selection was attributed to the effect of tube length on pollen receipt, as supplemental hand pollinations showed fruit and seed set in the population to be pollen limited. Indirect selection on tube length may also occur through the correlation of this trait with inflorescence height, although direct selection on the latter trait was significant only for seed set. The main pollinators at the study site were individuals of the large hawkmoth Agrius convolvuli that had tongue lengths of 85-135 mm. Other hawkmoths had tongues that were much too short to reach the nectar in G. longicollis flowers and seldom carried pollen of G. longicollis. Flowers with tubes shorter than the tongues of A. convolvuli are apparently not effectively pollinated because stigmas do not contact the moth's head effectively. This study demonstrates that selection may occur among plants with natural phenotypic variation in flower-tube length, and supports Darwin's model of pollinator-mediated selection.     

Selection on floral design in Polemonium brandegeei (Polemoniaceae): female and male fitness under hawkmoth pollination

Plant-pollinator interactions promote the evolution of floral traits that attract pollinators and facilitate efficient pollen transfer. The spatial separation of sex organs, herkogamy, is believed to limit sexual interference in hermaphrodite flowers. Reverse herkogamy (stigma recessed below anthers) and long, narrow corolla tubes are expected to promote efficiency in male function under hawkmoth pollination. We tested this prediction by measuring selection in six experimental arrays of Polemonium brandegeei, a species that displays continuous variation in herkogamy, resulting in a range of recessed to exserted stigmas. Under glasshouse conditions, we measured pollen removal and deposition, and estimated selection gradients (β) through female fitness (seeds set) and male fitness (siring success based on six polymorphic microsatellite loci). Siring success was higher in plants with more nectar sugar and narrow corolla tubes. However, selection through female function for reverse herkogamy was considerably stronger than was selection through male function. Hawkmoths were initially attracted to larger flowers, but overall preferred plants with reverse herkogamy. Greater pollen deposition and seed set also occurred in reverse herkogamous plants. Thus, reverse herkogamy may be maintained by hawkmoths through female rather than male function. Further, our results suggest that pollinator attraction may play a considerable role in enhancing female function.     

Effects of nectar-robbing on plant reproduction and evolution

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

The Pollinators of the Malagasy Star Orchids Angraecum sesquipedale,A. sororium and A. compactum and the Evolution of Extremely Long Spurs by Pollinator Shift

The pollination process of the extremely long-spurred orchids Angraecum sesquipedale and A. sororium is described and documented here for the first time. The pollinaria and viscidia load was examined in moths captured in central and south Madagascar. Visits to orchids by hawkmoths were rarely observed in the field and were therefore systematically recorded in large flight tents using a night-vision video technique and flashlight photography. Angraecum sesquipedale in Fort Dauphin is pollinated by Xanthopan morgani praedicta and A. sororium on Mt. Angavokely by Coelonia solani. By combining a deep nectar spur of extraordinary length with a protruding labellum functioning as a landing platform, these orchids overcome the moth's stereotypic swing-hovering flight thus enabling full insertion of the long tongue. Angraecum compactum in Forêt d'Ambohitantely is pollinated by both the shorter and longer-tongued forms of Panogena lingens which never swing-hover but is also exploited by X. morgani and C. solani with wastage of pollinaria. The duration of tongue insertion, nectar exploitation and tongue withdrawal were analyzed: legitimate and illegitimate visitors differ in their time budget and approach to the flower. Nectar volume, nectar level and sugar concentration of A. sesquipedale and A. sororium were compared with the nectar requirements of the pollinating hawkmoths. The evolution of very long spurs in these orchids is likely to have involved a series of pollinator shifts. The orchids adapted to different hawkmoth species with increasingly long tongues which primarily evolved to avoid predator attacks during visits to less specialized flowers. This “pollinator shift” model modifies the classical “coevolutionary race” model. The relevance of the taxon Angraecum bosseri Senghas is questioned.     

IS FLORAL SPECIALIZATION AN EVOLUTIONARY DEAD‐END? POLLINATION SYSTEM TRANSITIONS IN RUELLIA (ACANTHACEAE)

Pollination systems frequently reflect adaptations to particular groups of pollinators. Such systems are indicative of evolutionary specialization and have been important in angiosperm diversification. We studied the evolution of pollination systems in the large genus Ruellia. Phylogenetic analyses, morphological ordinations, ancestral state reconstructions, and a character mapping simulation were conducted to reveal key patterns in the direction and lability of floral characters associated with pollination. We found significant floral morphological differences among species that were generally associated with different groups of floral visitors. Floral evolution has been highly labile and also directional. Some specialized systems such as hawkmoth or bat pollination are likely evolutionary dead-ends. In contrast, specialized pollination by hummingbirds is clearly not a dead-end. We found evidence for multiple reverse transitions from presumed ancestral hummingbird pollination to more derived bee or insect pollination. These repeated origins of insect pollination from hummingbird-pollinated ancestors have not evolved without historical baggage. Flowers of insect-pollinated species derived from hummingbird-pollinated ancestors are morphologically more similar to hummingbird flowers than they are to other more distantly related insect-pollinated flowers. Finally, some pollinator switches were concomitant with changes in floral morphology that are associated with those pollinators. These observations are consistent with the hypothesis that some transitions have been adaptive in the evolution of Ruellia.