Pollinator Morphology Research Articles

Putting the puzzle together: the relationship between floral characters and pollinator morphology determines pollination mode in the fig-fig wasp mutualism.

The diversification of angiosperms has largely been attributed to adaptive radiation of their pollination and mating systems, which are relevant drivers of the macroevolution processes. The fig (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) interaction is an example of obligate mutualism. Passive and active pollination modes have been associated with morphological traits in both partners. However, more information is required to assess the relationship between floral traits and pollination modes, particularly in Neotropical Ficus species. This study evaluates the morphological traits of figs and fig wasps regarding pollination modes in species belonging to Neotropical Ficus sections (three species each of Americanae and Pharmacosycea). Pollination mode was identified by floral morphology, anther/ovule ratio, and specialized structures fig wasps use for pollen transport (pollen pocket and coxal combs). Fig species in sect. Americanae are actively pollinated because pistillate flowers form a synstigma, present anther/ovule ratios <0.11, and their pollinator Pegoscapus fig wasps have pollen pockets and coxal combs. In contrast, species in sect. Pharmacosycea have free pistillate flowers, with anther/ovule ratios >0.27; they are pollinated by Tetrapus wasps, which lack specialized structures to carry pollen. Each species of Ficus was associated with a single morphospecies of fig wasp. The results support previous contributions that consider reciprocal morphological traits between fig species and their pollinating wasps as evidence of a close co-evolutionary history.

A hurricane alters pollinator relationships and natural selection on an introduced island plant

AbstractNovel relationships between the floral morphology of introduced plants and the trophic morphology of native pollinators have been hypothesized to cause strong natural selection on both parties, but evidence for such selection is rare. We capitalized on a natural disturbance to examine selection on an introduced plant,Heliconia wagneriana, on the island of Dominica, before and after Hurricane Maria. Prior to the hurricane, femaleAnthracothorax jugularishummingbirds, which have longer bills than males, were the main visitor toH. wagneriana, and directional selection on corolla length was insignificant. After the hurricane, shorter‐billed maleA. jugulariswere the main visitor toH. wagneriana. The absence of trait matching between a short‐billed pollinator and a long‐flowered plant resulted in directional selection for shorter flowers because males preferentially visited plants with shorter flowers. The amount of nectar removed by maleA. jugulariswas negatively associated with flower length, with flowers &gt;53 mm containing nearly five times the nectar than flowers &lt;53 mm. We estimate a roughly 75% decrease in the population size ofA. jugularis, and results suggest the heaviest mortality occurred among short‐billed male hummingbirds and larger‐bodied individuals of both sexes, which would have higher nectar requirements and the most difficulty obtaining nectar. Our results indicate that hurricanes may alter relationships between plants and pollinators and that lack of trait matching resulting from such disturbances may lead to selection on both plant and pollinator.

Floral traits of mammal-pollinated Mucuna macrocarpa (Fabaceae): Implications for generalist-like pollination systems.

Floral traits are adapted by plants to attract pollinators. Some of those plants that have different pollinators in different regions adapt to each pollinator in each region to maximize their pollination success. Mucuna macrocarpa (Fabaceae) limits the pollinators using its floral structure and is pollinated by different mammals in different regions. Here, we examine the relationships between floral traits of M. macrocarpa and the external morphology of mammalian pollinators in different regions of its distribution. Field surveys were conducted on Kyushu and Okinawajima Island in Japan, and in Taiwan, where the main pollinators are the Japanese macaque Macaca fuscata, Ryukyu flying fox Pteropus dasymallus, and red‐bellied squirrel Callosciurus erythraeus, respectively. We measured the floral shapes, nectar secretion patterns, sugar components, and external morphology of the pollinators. Results showed that floral shape was slightly different among regions and that flower sizes were not correlated with the external morphology of the pollinators. Volume and sugar rate of nectar were not significantly different among the three regions and did not change throughout the day in any of the regions. However, nectar concentration was higher in Kyushu than in the other two regions. These results suggest that the floral traits of M. macrocarpa are not adapted to each pollinator in each region. Although this plant limits the number of pollinators using its flower structure, it has not adapted to specific mammals and may attract several species of mammals. Such generalist‐like pollination system might have evolved in the Old World.

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

The occurrence and extent of multiple paternity is an important component of variation in plant mating dynamics. However, links between pollinator activity and multiple paternity are generally lacking, especially for plant species that attract functionally diverse floral visitors. In this study, we separated the influence of two functionally distinct floral visitors (hawkmoths and solitary bees) and characterized their impacts on multiple paternity in a self-incompatible, annual forb, Oenothera harringtonii (Onagraceae). We also situated pollinator-mediated effects in a spatial context by linking variation in multiple paternity to variation in plant spatial isolation. We documented pronounced differences in the number of paternal sires as function of pollinator identity: on average, the primary pollinator (hawkmoths) facilitated mating with nearly twice as many pollen donors relative to the secondary pollinator (solitary bees). This effect was consistent for both isolated and nonisolated individuals, but spatial isolation imposed pronounced reductions on multiple paternity regardless of pollinator identity. Considering that pollinator abundance and pollen dispersal distance did not vary significantly with pollinator identity, we attribute variation in realized mating dynamics primarily to differences in pollinator morphology and behaviour as opposed to pollinator abundance or mating incompatibility arising from underlying spatial genetic structure. Our findings demonstrate that functionally distinct pollinators can have strongly divergent effects on polyandry in plants and further suggest that both pollinator identity and spatial heterogeneity have important roles in plant mating dynamics.

A spur-ious inference: Pollination is not more specialized in long-spurred than in spurless species in Diascia-Rediviva mutualisms

Plant species occupy a continuum from extreme generalization to extreme specialization in terms of the number and type of pollinator species they utilize, often irrespective of the number of available pollinator species. It is largely unclear what floral traits determine the level of specialization. Here we study interactions between co-flowering oil-producing Diascia species and oil-collecting Rediviva bee species at a site in the Cape Floristic Region of South Africa to quantify the level of specialization and identify the traits that mediate plant-pollinator interactions. Four Rediviva species, encompassing a two-fold difference in foreleg-length, all visited two Diascia species, which differed eight-fold in spur length, but the longest and shortest-legged bee species most frequently and preferentially visited long-spurred and short-spurred Diascia species, respectively. A third Rediviva species, with forelegs of intermediate length, visited both species and did not discriminate between Diascia species. Previously, most Diascia species were thought to share similar cues for pollinator attraction, however, our study shows that species-specific floral cues filter poorly-matching Rediviva species and enable partitioning of the local Rediviva assemblage by co-occurring Diascia species. Assessments of seed set following single visits by pollinators revealed no difference in per-visit effectiveness among Rediviva species, suggesting that morphological matching does not necessarily affect pollen deposition efficiency and that variation in female reproductive success determined by matching between flower and pollinator morphology is an unlikely driver of spur-length evolution in Diascia. Further, our study raises the intriguing possibility that the nature of reward presentation in the long-spurred D. ‘floribunda’ may even counteract specialization for exclusive pollination by long-legged species, and, thus, the unidirectional evolution of spur length fundamental to the co-evolutionary arms races assumed to have driven the evolution of elongated spurs.

Intraspecific divergence and convergence of floral tube length in specialized pollination interactions.

Floral tubes are often thought to be a consequence of adaptive specialization towards pollinator morphology. We explore floral tube length evolution within Tritoniopsis revoluta (Iridaceae), a species with considerable geographical tube length variation. We ask whether tube lengths of T. revoluta populations are associated with pollinator proboscis lengths, whether floral divergence occurs in the presence of different pollinators and whether floral convergence occurs between distantly related populations pollinated by the same pollinator. Finally, we ask whether tube length evolution is directional. Shifts between morphologically different pollinators were always associated with shifts in floral morphology, even when populations were very closely related. Distantly related populations had similar tube lengths when they were pollinated by the same pollinator. Shifts in tube length tended to be from short to long, although reversals were not infrequent. After correcting for the population-level phylogeny, there was a strong positive, linear relationship between floral tube length and pollinator proboscis length, suggesting that plants are functionally specialized on different pollinators at different sites. However, because tube length evolution in this system can be a bidirectional process, specialization to the local pollinator fauna is unlikely to result in evolutionary or ecological dead-ends such as canalization or range limitation.

Morphology, Diet and Flower‐visiting by Phyllostomid Bats in Cuba

AbstractPollinator morphology can play an important role in structuring plant–pollinator relationships and a pollinator's morphology may be associated with aspects of its diet. We examined the relationship between morphology and the partitioning of flower‐based food resources for five species of flower‐visiting Cuban bats: Artibeus jamaicensis, Brachyphylla nana, Erophylla sezekorni, Monophyllus redmani and Phyllonycteris poeyi. We analyzed cranial traits and body size to assess differences among species with respect to morphological specializations. We also collected dietary data from guano and used acoustic monitoring to assess bat activity at flowers. We found evidence that bats partition floral resources, but we found no direct evidence that plants were limiting resources for the bats. Morphological similarity among bat species did not predict dietary overlap. Rather it was associated with phylogenic relationships among some species. Species with different morphological specialization for flower‐visiting consumed resources and visited food plants at different frequencies.

Matching floral and pollinator traits through guild convergence and pollinator ecotype formation.

Pollinator landscapes, as determined by pollinator morphology/behaviour, can vary inter- or intraspecifically, imposing divergent selective pressures and leading to geographically divergent floral ecotypes. Assemblages of plants pollinated by the same pollinator (pollinator guilds) should exhibit convergence of floral traits because they are exposed to similar selective pressures. Both convergence and the formation of pollination ecotypes should lead to matching of traits among plants and their pollinators. We examined 17 floral guild members pollinated in all or part of their range by Prosoeca longipennis, a long-proboscid fly with geographic variation in tongue length. Attractive floral traits such as colour, and nectar properties were recorded in populations across the range of each species. The length of floral reproductive parts, a mechanical fit trait, was recorded in each population to assess possible correlation with the mouthparts of the local pollinator. A multiple regression analysis was used to determine whether pollinators or abiotic factors provided the best explanation for variation in floral traits, and pollinator shifts were recorded in extralimital guild member populations. Nine of the 17 species were visited by alternative pollinator species in other parts of their ranges, and these displayed differences in mechanical fit and attractive traits, suggesting putative pollination ecotypes. Plants pollinated by P. longipennis were similar in colour throughout the pollinator range. Tube length of floral guild members co-varied with the proboscis length of P. longipennis. Pollinator shifts have resulted in geographically divergent pollinator ecotypes across the ranges of several guild members. However, within sites, unrelated plants pollinated by P. longipennis are similar in the length of their floral parts, most probably as a result of convergent evolution in response to pollinator morphology. Both of these lines of evidence suggest that pollinators play an important role in selecting for certain floral traits.

The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae)

One of the most powerful drivers of speciation in plants is pollinator-mediated disruptive selection, which leads to the divergence of floral traits adapted to the morphology and behavior of different pollinators. Despite the widespread importance of this speciation mechanism, its genetic basis has been explored in only a few groups. Here, we characterize the genetic basis of pollinator-mediated divergence of two species in genus Ipomopsis, I. guttata and I. tenuifolia, using quantitative trait locus (QTL) analyses of floral traits and other variable phenotypes. We detected one to six QTLs per trait, with each QTL generally explaining small to modest amounts of the phenotypic variance of a backcross hybrid population. In contrast, flowering time and anthocyanin abundance (a metric of color variation) were controlled by a few QTLs of relatively large effect. QTLs were strongly clustered within linkage groups, with 26 of 37 QTLs localized to six marker-interval 'hotspots,' all of which harbored pleiotropic QTLs. In contrast to other studies that have examined the genetic basis of pollinator shifts, our results indicate that, in general, mutations of small to modest effect on phenotype were involved. Thus, the evolutionary transition between the distinct pollination modes of I. guttata and I. tenuifolia likely proceeded incrementally, rather than saltationally.

Look and touch: multimodal sensory control of flower inspection movements in the nocturnal hawkmothManduca sexta

A crucial stage in the interaction between pollinators and plants is the moment of physical contact between them, known as flower inspection, or handling. Floral guides - conspicuous colour markings, or structural features of flower corollas - have been shown to be important in the inspecting behaviour of many insects, particularly in diurnal species. For the nocturnal hawkmoth Manduca sexta tactile input has an important role in flower inspection, but there is no knowledge about the use of visual floral guides in this behaviour. I carried out a series of experiments to first, evaluate the putative role of floral guides during flower inspection and second, to explore how simultaneous tactile and visual guides could influence this behaviour. Results show that visual floral guides affect flower inspection by M. sexta. Moths confine proboscis placement to areas of higher light reflectance regardless of their chromaticity, but do not appear to show movements in any particular direction within these areas. I also recorded inspection times, finding that moths can learn to inspect flowers more efficiently when visual floral guides are available. Additionally, I found that some visual floral guides can affect the body orientation that moths adopt while hovering in front of horizontal models. Finally, when presented with flower models offering both visual and tactile guides, the former influenced proboscis placement, whereas the latter controlled proboscis movements. Results show that innate inspection behaviour is under multimodal sensory control, consistent with other components of the foraging task. Fine scale inspection movements (elicited by diverse floral traits) and the tight adjustment between the morphology of pollinators and flowers appear to be adaptively integrated, facilitating reward assessment and effective pollen transfer.

Do floral traits of Strelitzia reginae limit nectar theft by sunbirds?

The shape of flowers frequently corresponds to the morphology of pollinators but some floral traits may also function to prevent non-pollinating flower visitors from stealing flower rewards. Despite the presence of such structures few studies have demonstrated their efficacy in limiting the nectar intake by nectar thieves. The flowers of Strelitzia reginae are regularly visited by sunbirds that do not effect pollination and act solely as nectar thieves. In this species, the nectary is covered by the convoluted bases of the petals (“nectar barriers”). In this study we investigate how non-pollinating sunbirds interact with these nectar barriers and whether nectar barriers play a role in limiting the amount of nectar sunbirds can steal. We quantified the volume of nectar that sunbirds consume while visiting flowers where nectar barriers were present and in flowers where these were experimentally removed. We found that sunbirds consume a median of 106.8 µl of nectar when visiting flowers with nectar barriers present and consumed a significantly greater volume of nectar (median = 158.03 µl) in flowers without nectar barriers. These results suggest that the convoluted petals that cover the nectary of S. reginae may function to reduce nectar theft but are likely to be more effective against insect nectar thieves. This is one of the first studies to quantitatively demonstrate the role of flower features that may function to limit nectar theft.

Plant–hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size

Floral phenotype and pollination system of a plant may be influenced by the abiotic environment and the local pollinator assemblage. This was investigated in seven plant-hummingbird assemblages on the West Indian islands of Grenada, Dominica and Puerto Rico. We report all hummingbird and insect pollinators of 49 hummingbird-pollinated plant species, as well as six quantitative and semi-quantitative floral characters that determine visitor restriction, attraction and reward. Using nonmetric multidimensional scaling analysis, we show that hummingbird-pollinated plants in the West Indies separate in floral phenotypic space into two gradients-one associated with the abiotic environment and another with hummingbird size. Plants pollinated by large, long-billed hummingbirds had flowers with long corolla tube, large amounts of nectar and showy orange-red colouration. These attracted few or no insect species, whereas plants pollinated by small, short-billed hummingbirds were frequently pollinated by insects, particularly lepidopterans. The separation of plants related to environmental factors showed that species in the wet and cold highlands produced large amounts of dilute nectar, possessed no or a weak odour, and were associated with few insects, particularly few hymenopterans, compared to plants in the dry and warm lowlands. The most specialised hummingbird-pollinated plants are found in the West Indian highlands where they are pollinated by mainly large, long-billed hummingbirds. At the other extreme, highly generalised plants growing in the dry and warm lowlands are pollinated by small, short-billed hummingbirds and numerous insect species. This illustrates that, even within the hummingbird-pollinated flora, pollination syndrome and the degree of specialisation may vary tremendously depending on pollinator morphology and environment.

SELECTION TOWARD SHORTER FLOWERS BY BUTTERFLIES WHOSE PROBOSCES ARE SHORTER THAN FLORAL TUBES

Darwin's meticulous observations on the function of floral shape led to his famous prediction of a long-tongued pollinator, which he believed to be the evolutionary trigger for the long-spurred flowers of the Madagascar star orchid. Although tubular flowers are common, long tubes or spurs are an exception, suggesting that selection maintaining short flowers is widespread. Using the butterfly-pollinated carnation Dianthus carthusianorum and two butterfly species differing in proboscis length (Melanargia galathea and Inachis io) as model organisms, we experimentally demonstrate a reduction in pollinator efficiency with an increasing difference between proboscis length and floral tube length. Such a relationship is a prerequisite for the evolution of floral shape in response to pollinator morphology.

Pollinator shifts drive increasingly long nectar spurs in columbine flowers

Directional evolutionary trends have long garnered interest because they suggest that evolution can be predictable. However, the identification of the trends themselves and the underlying processes that may produce them have often been controversial. In 1862, in explaining the exceptionally long nectar spur of Angraecum sesquipedale, Darwin proposed that a coevolutionary 'race' had driven the directional increase in length of a plant's spur and its pollinator's tongue. Thus he predicted the existence of an exceptionally long-tongued moth. Though the discovery of Xanthopan morgani ssp. praedicta in 1903 with a tongue length of 22 cm validated Darwin's prediction, his 'race' model for the evolution of long-spurred flowers remains contentious. Spurs may also evolve to exceptional lengths by way of pollinator shifts as plants adapt to a series of unrelated pollinators, each with a greater tongue length. Here, using a species-level phylogeny of the columbine genus, Aquilegia, we show a significant evolutionary trend for increasing spur length during directional shifts to pollinators with longer tongues. In addition, we find evidence for 'punctuated' change in spur length during speciation events, suggesting that Aquilegia nectar spurs rapidly evolve to fit adaptive peaks predefined by pollinator morphology. These findings show that evolution may proceed in predictable pathways without reversals and that change may be concentrated during speciation.

A Pollination Ecology Study of Pedicularis Linnaeus (Orobanchaceae) in a Subalpine to Alpine Area of Northwest Sichuan, China

Pollination ecology and habitat preference of Pedicularis species were studied in a transitional zone between subalpine coniferous forests and alpine meadows in northwestern Sichuan of China. Pedicularis species exhibited apparent preferences for different microhabitats. Species with long rostrate and contorted galea were nectarless and their mean corolla tube length ranged from 7 to 50 mm while species without long rostrate and contorted galea produced nectar and their corolla tube length averaged from 8 to 18 mm. Bumblebees were the sole pollinators of the studied species and five bee species pollinated seven Pedicularis species with one species pollinating all the Pedicularis species. Pollinators that visited nectariferous species had longer tongues than those that visited nectarless species and they spent longer time on nectariferous than on nectarless species. All Pedicularis species except for P. rex subsp. lipskyana were pollinated by worker bees. Pedicularis rex subsp. lipskyana was pollinated nototribically by worker, male and queen bumblebees through stigmatic contact with residual pollen on the left side of the bee’s head. Morphology of pollinators, rather than pollinator species, may play the key role in diversification of Pedicularis. Microhabitats rather than pollination may be the separation barrier in propagation. Factors contributing to high diversity of Pedicularis need further study.

Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology

There has been much recent interest in explaining patterns of body size variation within species assemblages. One observation is that frequency distributions of species’ body size commonly exhibit a right‐skew, even on a logarithmic scale. Here we examine the species’ body size distributions in two assemblages of large Costa Rican moths. We find that neither adult Sphingidae or Saturniidae exhibit the classic log right‐skewed pattern. Furthermore, the species’ body size distributions in these two groups are markedly different, which we suggest is a result of differential selective pressures related to resource and mate acquisition. For Sphingidae, we show (1) that body size is positively correlated with tongue length, and (2) that the distribution of sphingid body sizes/tongue lengths closely matches the distribution of flower corolla tube depths in sphingid‐pollinated plants. Thus, morphological fitting between plants and pollinators seems to underlie the species’ body size distribution of this sphingid assemblage. We discuss the significance of these results in the context of current theory on mechanisms driving species’ body size distributions. Finally, we present an evolutionary hypothesis for the diversity of body sizes seen in this sphingid assemblage related to reciprocal interactions between plants and pollinators. This hypothesis can be tested within a rigorous phylogenetic framework, although a systematic phylogenetic analysis of Neotropical Sphingidae does not currently exist.