Does the morphological fit between flowers and pollinators affect pollen deposition? An experimental test in a buzz‐pollinated species with anther dimorphism

Abstract Some pollination systems, such as buzz‐pollination, are associated with floral morphologies that require a close physical interaction between floral sexual organs and insect visitors. In these systems, a pollinator's size relative to the flower may be an important feature determining whether the visitor touches both male and female sexual organs and thus transfers pollen between plants efficiently. To date, few studies have addressed whether in fact the “fit” between flower and pollinator influences pollen transfer, particularly among buzz‐pollinated species. Here we use Solanum rostratum, a buzz‐pollinated plant with dimorphic anthers and mirror‐image flowers, to investigate whether the morphological fit between the pollinator's body and floral morphology influences pollen deposition. We hypothesized that when the size of the pollinator matches the separation between the sexual organs in a flower, more pollen should be transferred to the stigma than when the visitor is either too small or too big relative to the flower. To test this hypothesis, we exposed flowers of S. rostratum with varying levels of separation between sexual organs, to bumblebees (Bombus terrestris) of different sizes. We recorded the number of visits received, pollen deposition, and fruit and seed production. We found higher pollen deposition when bees were the same size or bigger than the separation between anther and stigma within a flower. We found a similar, but not statistically significant pattern for fruit set. In contrast, seed set was more likely to occur when the size of the flower exceeded the size of the bee, suggesting that other postpollination processes may be important in translating pollen receipt to seed set. Our results suggest that the fit between flower and pollinator significantly influences pollen deposition in this buzz‐pollinated species. We speculate that in buzz‐pollinated species where floral morphology and pollinators interact closely, variation in the visitor's size may determine whether it acts mainly as a pollinator or as a pollen thief (i.e., removing pollen rewards but contributing little to pollen deposition and fertilization).

[1]  M. Vallejo‐Marín,et al.  High incidence of pollen theft in natural populations of a buzz-pollinated plant , 2015, Arthropod-Plant Interactions.

[2]  T. Itino,et al.  Altitudinal flower size variation correlates with local pollinator size in a bumblebee‐pollinated herb, Prunella vulgaris L. (Lamiaceae) , 2015, Journal of evolutionary biology.

[3]  A. Lou,et al.  Pollen limitation in invasive populations of Solanum rostratum and its relationship to population size , 2015 .

[4]  Achim Zeileis,et al.  Diagnostic Checking in Regression Relationships , 2015 .

[5]  T. Itino,et al.  Changes in pollinator fauna affect altitudinal variation of floral size in a bumblebee-pollinated herb , 2014, Ecology and evolution.

[6]  W. Armbruster,et al.  In the right place at the right time: Parnassia resolves the herkogamy dilemma by accurate repositioning of stamens and stigmas. , 2014, Annals of botany.

[7]  M. Vallejo‐Marín,et al.  Population Structure and Genetic Diversity of Native and Invasive Populations of Solanum rostratum (Solanaceae) , 2013, PloS one.

[8]  M. Vallejo‐Marín,et al.  Mating system in Mexican populations of the annual herb Solanum rostratum Dunal (Solanaceae). , 2013, Plant biology.

[9]  M. Vallejo‐Marín,et al.  What's the 'buzz' about? The ecology and evolutionary significance of buzz-pollination. , 2013, Current opinion in plant biology.

[10]  D. Goulson,et al.  Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers , 2012, Oecologia.

[11]  John C. Nash,et al.  Unifying Optimization Algorithms to Aid Software System Users: optimx for R , 2011 .

[12]  Antonio Gasparrini,et al.  Distributed Lag Linear and Non-Linear Models in R: The Package dlnm. , 2011, Journal of statistical software.

[13]  M. Vallejo‐Marín,et al.  Trait correlates and functional significance of heteranthery in flowering plants. , 2010, The New phytologist.

[14]  N. Waser,et al.  Size-specific interaction patterns and size matching in a plant-pollinator interaction web. , 2009, Annals of botany.

[15]  Elisabeth Dévière,et al.  Analyzing linguistic data: a practical introduction to statistics using R , 2009 .

[16]  Y. Takami,et al.  Flower orientation enhances pollen transfer in bilaterally symmetrical flowers , 2009, Oecologia.

[17]  J. Thomson,et al.  Division of labour within flowers: heteranthery, a floral strategy to reconcile contrasting pollen fates , 2009, Journal of evolutionary biology.

[18]  Hong Liu,et al.  Solitary invasive orchid bee outperforms co-occurring native bees to promote fruit set of an invasive Solanum , 2009, Oecologia.

[19]  G. Kudo,et al.  Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees , 2008, Ecological Research.

[20]  W. Armbruster,et al.  Associations between floral specialization and species diversity: cause, effect, or correlation? , 2008, Evolutionary Ecology.

[21]  Qing‐Jun Li,et al.  The pollination ecology of Paraboea rufescens (Gesneriaceae): a buzz-pollinated tropical herb with mirror-image flowers. , 2006, Annals of botany.

[22]  S. Barrett,et al.  Experimental tests of the function of mirror-image flowers , 2005 .

[23]  A. Nicotra,et al.  High self-pollen transfer and low fruit set in buzz-pollinated Dianella revoluta (Phormiaceae) , 2004 .

[24]  C. Andrus Plant breeding systems , 1963, Euphytica.

[25]  J. Obeso A hierarchical perspective in allocation to reproduction from whole plant to fruit and seed level , 2004 .

[26]  S. Barrett,et al.  The Comparative Biology of Mirror‐Image Flowers , 2003, International Journal of Plant Sciences.

[27]  Dave Goulson,et al.  Bumblebees: Behaviour, Ecology, and Conservation , 2003 .

[28]  S. Barrett,et al.  Enantiostyly: Solving the puzzle of mirror-image flowers , 2002, Nature.

[29]  S. Barrett Evolution of sex: The evolution of plant sexual diversity , 2002, Nature Reviews Genetics.

[30]  S. Barrett,et al.  Sexual interference of the floral kind , 2002, Heredity.

[31]  A. Fetscher Resolution of male-female conflict in an hermaphroditic flower , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  J. Cresswell Stabilizing Selection and the Structural Variability of Flowers within Species , 1998 .

[33]  David W. Inouye,et al.  Techniques for Pollination Biologists , 1993 .

[34]  A. Montalvo RELATIVE SUCCESS OF SELF AND OUTCROSS POLLEN COMPARING MIXED‐ AND SINGLE‐DONOR POLLINATIONS IN AQUILEGIA CAERULEA , 1992, Evolution; international journal of organic evolution.

[35]  Thomas P. Clausen,et al.  POLLINATION OF DALECHAMPIA MAGNOLIIFOLIA (EUPHORBIACEAE) BY MALE EUGLOSSINE BEES , 1989 .

[36]  D. Roubik,et al.  Pollen Deposition and Removal by Bees Visiting Two Tree Species in Panama , 1987 .

[37]  D. G. Lloyd,et al.  The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy , 1986 .

[38]  S. Buchmann Buzz pollination in angiosperms. , 1983 .

[39]  R. Dulberger THE FLORAL BIOLOGY OF CASSIA DIDYMOBOTRYA AND C. AURICULATA (CAESALPINIACEAE) , 1981 .

[40]  A. Stephenson Flower and Fruit Abortion: Proximate Causes and Ultimate Functions , 1981 .

[41]  K. Bowers The Pollination Ecology of Solanum Rostratum (Solanaceae) , 1975 .

[42]  J. Harris,et al.  Observations on pollination of Solanum rostratum dunal and Cassia chamaecrista L. , 1902 .

[43]  J. Hannay Natural Selection and Natural Theology , 1883, Nature.

[44]  H. Müller Two Kinds of Stamens with Different Functions in the same Flower , 1881, Nature.