New frontiers in competition for pollination.

BACKGROUND Co-flowering plant species frequently share pollinators. Pollinator sharing is often detrimental to one or more of these species, leading to competition for pollination. Perhaps because it offers an intriguing juxtaposition of ecological opposites - mutualism and competition - within one relatively tractable system, competition for pollination has captured the interest of ecologists for over a century. SCOPE Our intent is to contemplate exciting areas for further work on competition for pollination, rather than to exhaustively review past studies. After a brief historical summary, we present a conceptual framework that incorporates many aspects of competition for pollination, involving both the quantity and quality of pollination services, and both female and male sex functions of flowers. Using this framework, we contemplate a relatively subtle mechanism of competition involving pollen loss, and consider how competition might affect plant mating systems, overall reproductive success and multi-species interactions. We next consider how competition for pollination might be altered by several emerging consequences of a changing planet, including the spread of alien species, climate change and pollinator declines. Most of these topics represent new frontiers whose exploration has just begun. CONCLUSIONS Competition for pollination has served as a model for the integration of ecological and evolutionary perspectives in the study of species interactions. Its study has elucidated both obvious and more subtle mechanisms, and has documented a range of outcomes. However, the potential for this interaction to inform our understanding of both pure and applied aspects of pollination biology has only begun to be realized.

[1]  D. Ackerly,et al.  Plant-pollinator interactions and the assembly of plant communities. , 2008, Trends in ecology & evolution.

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

[3]  L. Bobisud,et al.  Pollinator constancy and survival of rare species , 2004, Oecologia.

[4]  H. Sahli,et al.  Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae). , 2007, American journal of botany.

[5]  Teja Tscharntke,et al.  Mass flowering crops enhance pollinator densities at a landscape scale , 2003 .

[6]  Jane Memmott,et al.  Global warming and the disruption of plant-pollinator interactions. , 2007, Ecology letters.

[7]  C. Galen,et al.  Interspecific pollen transfer as a mechanism of competition: Consequences of foreign pollen contamination for seed set in the alpine wildflower, Polemonium viscosum , 1989, Oecologia.

[8]  B. Schmid,et al.  Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). , 2002, American journal of botany.

[9]  R. Mitchell,et al.  Competition for Pollination Between an Invasive Species (Purple Loosestrife) and a Native Congener , 2002 .

[10]  J. Thomson When Is It Mutualism? , 2003, The American Naturalist.

[11]  Ola Jennersten,et al.  Competition for bumblebee visitation between Melampyrum pratense and Viscaria vulgaris with healthy and Ustilago-infected flowers , 1991, Oecologia.

[12]  N. Waser,et al.  CHAPTER 10 – The Adaptive Nature of Floral Traits: Ideas and Eviaence , 1983 .

[13]  M. Sazima,et al.  Pollination and reproductive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. , 2004, Annals of botany.

[14]  M. Aizen,et al.  How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. , 2009, Annals of botany.

[15]  P. Feinsinger ECOLOGICAL INTERACTIONS BETWEEN PLANTS AND HUMMINGBIRDS IN A SUCCESSIONAL TROPICAL COMMUNITY , 1978 .

[16]  T. Laverty Plant interactions for pollinator visits: a test of the magnet species effect , 1992, Oecologia.

[17]  A. Lack COMPETITION FOR POLLINATORS AND EVOLUTION IN CENTAUREA , 1976 .

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

[19]  Brosi A. Bradley,et al.  Might Flowers of Invasive Plants Increase Native Bee Carrying Capacity? Intimations From Capitol Reef National Park, Utah , 2008 .

[20]  M. Burd,et al.  Pollination decays in biodiversity hotspots. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  T. Tscharntke,et al.  Bumblebees experience landscapes at different spatial scales: possible implications for coexistence , 2006, Oecologia.

[22]  T. Tscharntke,et al.  Pollination, seed set and seed predation on a landscape scale , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  Ørjan Totland,et al.  How does climate warming affect plant-pollinator interactions? , 2009, Ecology letters.

[24]  M. R. Dudash RELATIVE FITNESS OF SELFED AND OUTCROSSED PROGENY IN A SELF‐COMPATIBLE, PROTANDROUS SPECIES, SABATIA ANGULARIS L. (GENTIANACEAE): A COMPARISON IN THREE ENVIRONMENTS , 1990, Evolution; international journal of organic evolution.

[25]  L. W. Macior CO‐EVOLUTION OF PLANTS AND ANIMALS — SYSTEMATIC INSIGHTS FROM PLANT‐INSECT INTERACTIONS , 1971 .

[26]  A. Snow,et al.  Commercialization of Transgenic Plants: Potential Ecological Risks , 1997 .

[27]  J. Free Dandelion as a Competitor to Fruit Trees for Bee Visits , 1968 .

[28]  L. Harder Behavioral responses by bumble bees to variation in pollen availability , 1990, Oecologia.

[29]  Luciano Cagnolo,et al.  Uniting pattern and process in plant-animal mutualistic networks: a review. , 2009, Annals of botany.

[30]  D. Campbell,et al.  The Mechanism of Competition for Pollination between Two Forest Herbs , 1985 .

[31]  R. Mitchell,et al.  Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). , 2009, American journal of botany.

[32]  S. Weller,et al.  The evolution of wind pollination in angiosperms , 2002 .

[33]  D. Levin,et al.  An Analysis of Interspecific Pollen Exchange in Phlox , 1967, The American Naturalist.

[34]  K. Armitage,et al.  Climate change is affecting altitudinal migrants and hibernating species. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  L. Johnson,et al.  From horticultural plantings into wild populations: movement of pollen and genes in Lobelia cardinalis , 2008, Plant Ecology.

[36]  I. Washitani,et al.  Heterostylous morph differences in pollen transfer and deposition patterns in Primula sieboldii on a visitation by a queen bumblebee, measured with a semi‐natural experimental system , 2002 .

[37]  P. Feinsinger,et al.  Effects of indiscriminate foraging by tropical hummingbirds on pollination and plant reproductive success: experiments with two tropical treelets (Rubiaceae) , 1988, Oecologia.

[38]  Honor C. Prentice,et al.  Gene Flow and Introgression from Domesticated Plants into Their Wild Relatives , 1999 .

[39]  Claire Kremen,et al.  Modelling pollination services across agricultural landscapes. , 2009, Annals of botany.

[40]  John Connolly,et al.  What is wrong with replacement series? , 1988, Trends in ecology & evolution.

[41]  M. Geber,et al.  CHAPTER 6 Pollinator responses to plant communities and implications for reproductive character evolution , 2006 .

[42]  J. Dushoff,et al.  Native bees provide insurance against ongoing honey bee losses. , 2007, Ecology Letters.

[43]  L. Real,et al.  Effective mutualism between sequentially flowering plant species , 1979, Nature.

[44]  D. Schemske Floral Convergence and Pollinator Sharing in Two Bee‐Pollinated Tropical Herbs , 1981 .

[45]  W. B. Watt,et al.  Nectar resource use by Colias butterflies , 1974, Oecologia.

[46]  P. Feinsinger Effects of plant species on each other's pollination: Is community structure influenced? , 1987, Trends in ecology & evolution.

[47]  James Regetz,et al.  Landscape effects on crop pollination services: are there general patterns? , 2008, Ecology letters.

[48]  A. Traveset,et al.  Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands , 2005 .

[49]  B. Rathcke CHAPTER 12 – Competition and Facilitation among Plants for Pollination , 1983 .

[50]  J Memmott,et al.  The structure of a plant-pollinator food web. , 1999, Ecology letters.

[51]  L. Cavieres,et al.  The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities , 2008 .

[52]  D. Campbell Multiple paternity in fruits of Ipomopsis aggregata (Polemoniaceae). , 1998, American journal of botany.

[53]  J. Ghazoul Floral diversity and the facilitation of pollination , 2006 .

[54]  D. Campbell POLLEN AND GENE DISPERSAL: THE INFLUENCES OF COMPETITION FOR POLLINATION , 1985, Evolution; international journal of organic evolution.

[55]  M. Vilà,et al.  High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. , 2008, Annals of botany.

[56]  J. Free Insect pollination of crops , 1970 .

[57]  G. Whitney THE REPRODUCTIVE BIOLOGY OF RASPBERRIES AND PLANT‐POLLINATOR COMMUNITY STRUCTURE , 1984 .

[58]  Michele R. Dudash,et al.  A model and lexicon for pollen fate , 1994 .

[59]  M. Zimmerman REPRODUCTION IN POLEMONIUM: COMPETITION FOR POLLINATORS' , 1980 .

[60]  M. Potts,et al.  Character displacement among bat-pollinated flowers of the genus Burmeistera: analysis of mechanism, process and pattern , 2007, Proceedings of the Royal Society B: Biological Sciences.

[61]  Gary Paul Nabhan,et al.  The Forgotten Pollinators , 1996 .

[62]  T. Ricketts Tropical Forest Fragments Enhance Pollinator Activity in Nearby Coffee Crops , 2004 .

[63]  T. Mosquin Competition for pollinators as a stimulus for the evolution of flowering time , 1971 .

[64]  Anders Nielsen,et al.  Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb. , 2006, American journal of botany.

[65]  B. Heinrich BEE FLOWERS: A HYPOTHESIS ON FLOWER VARIETY AND BLOOMING TIMES , 1975, Evolution; international journal of organic evolution.

[66]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  P. Feinsinger,et al.  Competition among plants sharing hummingbird pollinators : laboratory experiments on a mechanism , 1991 .

[68]  F. G. Stiles Coadapted Competitors: The Flowering Seasons of Hummingbird-Pollinated Plants in a Tropical Forest , 1977, Science.

[69]  W. Armbruster,et al.  An experimental test for reproductive interactions between two sequentially blooming Saxifraga species (Saxifragaceae) , 1991 .

[70]  N. Waser,et al.  Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata , 1986, Oecologia.

[71]  M. V. Price,et al.  Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography. , 2008, Ecology.

[72]  D. Goulson,et al.  Decline and conservation of bumble bees. , 2008, Annual review of entomology.

[73]  Juan M Morales,et al.  Invasive Mutualists Erode Native Pollination Webs , 2008, PLoS biology.

[74]  L. Chittka,et al.  Successful invasion of a floral market , 2001, Nature.

[75]  J. Cresswell,et al.  Frequency-Dependent Selection and Adaptive Surfaces for Floral Character Combinations: The Pollination of Polemonium viscosum , 1991, The American Naturalist.

[76]  D. Schemske Time Budget and Foraging Site Preference of the Cinnamon Hummingbird in Costa Rica , 1975 .

[77]  P. Keddy,et al.  Competitive Effect and Response Rankings in 20 Wetland Plants: Are They Consistent Across Three Environments? , 1994 .

[78]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Michele R. Dudash,et al.  Fluorescent dye particles are good pollen analogs for hummingbird-pollinated Silene virginica (Caryophyllaceae) , 1996 .

[80]  J. Thomson Effects of stand composition on insect visitation in two-species mixtures of Hieracium [aurantiacum and Hieracium florentinum]. , 1978 .

[81]  L. Harder,et al.  THEORETICAL CONSEQUENCES OF HETEROGENEOUS TRANSPORT CONDITIONS FOR POLLEN DISPERSAL BY ANIMALS , 1998 .

[82]  S. Kephart The Partitioning of Pollinators among Three Species of Asclepias , 1983 .

[83]  Ø. Totland,et al.  Do alien plant invasions really affect pollination success in native plant species , 2007 .

[84]  J. D. Karron,et al.  FITNESS CONSEQUENCES OF MULTIPLE PATERNITY IN WILD RADISH, RAPHANUS SATIVUS , 1990, Evolution; international journal of organic evolution.

[85]  P. Lewis,et al.  Reproductive Traits and Male Fertility in Plants: Empirical Approaches* , 1993 .

[86]  M. V. Price,et al.  COMPONENTS OF PHENOTYPIC SELECTION: POLLEN EXPORT AND FLOWER COROLLA WIDTH IN IPOMOPSIS AGGREGATA , 1991, Evolution; international journal of organic evolution.

[87]  G. Nabhan,et al.  Services provided by pollinators , 1997 .

[88]  M. Whalen Reproductive Character Displacement and Floral Diversity in Solanum Section Androceras , 1978 .

[89]  L. Chittka,et al.  Flower Constancy, Insect Psychology, and Plant Evolution , 1999, Naturwissenschaften.

[90]  G. Stone,et al.  Partitioning of pollinators during flowering in an African Acacia community , 1998 .

[91]  James S. Clark,et al.  Plant migration and climate change , 1997 .

[92]  P. Petraitis Competitive Networks and Measures of Intransitivity , 1979, The American Naturalist.

[93]  S. Pickett,et al.  Changing perspectives in community dynamics: A reply to Waters. , 1990, Trends in ecology & evolution.

[94]  D. Winkler,et al.  A Matter of Timing , 2008, Science.

[95]  The collection of pollen by bees , 2000 .

[96]  B. Hocking,et al.  Insect-flower associations in the high Arctic with special reference to nectar' , 1968 .

[97]  Frederic E. Clements,et al.  Experimental pollination; an outline of the ecology of flowers and insects , 2009 .

[98]  K. Mauck,et al.  Experimental field comparison of native and non‐native maple seedlings: natural enemies, ecophysiology, growth and survival , 2007 .

[99]  W. Morris,et al.  Systematic increase in pollen carryover and its consequences for geitonogamy in plant populations , 1994 .

[100]  T. Callaghan,et al.  COMPARATIVE RESPONSES OF PHENOLOGY AND REPRODUCTIVE DEVELOPMENT TO SIMULATED ENVIRONMENTAL-CHANGE IN SUB-ARCTIC AND HIGH ARCTIC PLANTS , 1993 .

[101]  A. Traveset,et al.  Interspecific Pollen Transfer: Magnitude, Prevalence and Consequences for Plant Fitness , 2008 .

[102]  W. Wilson,et al.  When can two plant species facilitate each other's pollination? , 2004 .

[103]  J. Osborne,et al.  An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species , 2005, Molecular ecology.

[104]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[105]  H. Mooney,et al.  The evolutionary impact of invasive species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[106]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Jane Memmott,et al.  The impact of an alien plant on a native plant-pollinator network: an experimental approach. , 2007, Ecology letters.

[108]  Rebecca E. Irwin,et al.  Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions , 2004 .

[109]  S. Colla,et al.  Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson , 2008, Biodiversity and Conservation.

[110]  R. Vaillancourt,et al.  Gene flow between introduced and native Eucalyptus species , 2002, New Forests.

[111]  M. V. Price,et al.  Experimental studies of pollen carryover: effects of floral variability in Ipomopsis aggregata , 1984, Oecologia.

[112]  N. Waser Interspecific pollen transfer and competition between co-occurring plant species , 2004, Oecologia.

[113]  K. Lertzman Pollen transfer : processes and consequences , 1981 .

[114]  Harlan Lewis,et al.  Experimental Sympatric Populations of Clarkia , 1961, The American Naturalist.

[115]  R. Reader Competitive relationships of some bog ericads for major insect pollinators , 1975 .

[116]  W. Anderson,et al.  Competition for Pollinators between Simultaneously Flowering Species , 1970, American Naturalist.

[117]  H. Rusterholz,et al.  Effects of elevated CO2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands , 1998, Oecologia.

[118]  J. Thomson Spatial and Temporal Components of Resource Assessment by Flower-Feeding Insects , 1981 .

[119]  L. Harder,et al.  Pollen fates and the limits on male reproductive success in an orchid population , 2005 .

[120]  M. V. Price,et al.  EFFECTS OF EXPERIMENTAL WARMING ON PLANT REPRODUCTIVE PHENOLOGY IN A SUBALPINE MEADOW , 1998 .

[121]  C. Robertson The Philosophy of Flower Seasons, and the Phaenological Relations of the Entomophilous Flora and the Anthophilous Insect Fauna , 1895, The American Naturalist.

[122]  T. Ashman,et al.  Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[123]  M. Mangel,et al.  Mechanisms of pollen deposition by insect pollinators , 1995, Evolutionary Ecology.

[124]  Sarah S. Greenleaf,et al.  Bee foraging ranges and their relationship to body size , 2007, Oecologia.

[125]  M. Edwards,et al.  Floral Character Displacement Generates Assemblage Structure of Western Australian Triggerplants (Stylidium) , 1994 .

[126]  J. Cane The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields , 1997 .

[127]  N. Waser Competition for Hummingbird Pollination and Sequential Flowering in Two Colorado Wildflowers , 1978 .

[128]  S. Murphy The Determination of the Allelopathic Potential of Pollen and Nectar , 1992 .

[129]  D. Schemske,et al.  Flowering Ecology of Some Spring Woodland Herbs , 1978 .

[130]  K. Niklas,et al.  Pollination and Airflow Patterns Around Conifer Ovulate Cones , 1982, Science.

[131]  S. Naeem,et al.  Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem , 2003 .

[132]  L. Harder,et al.  Evolutionary Options for Maximizing Pollen Dispersal of Animal-Pollinated Plants , 1989, The American Naturalist.

[133]  D. Levin THE EFFECT OF COROLLA COLOR AND OUTLINE ON INTERSPECIFIC POLLEN FLOW IN PHLOX , 1969, Evolution; international journal of organic evolution.

[134]  P. Feinsinger,et al.  Interspecific Pollen Loss by Hummingbirds Visiting Flower Mixtures: Effects of Floral Architecture , 1995 .

[135]  J. Osborne,et al.  Nectar and flower production in Vicia faba L. (field bean) at ambient and elevated carbon dioxide , 1997 .

[136]  A. McGuire,et al.  EXPERIMENTAL ASSESSMENT OF REPRODUCTIVE INTERACTIONS BETWEEN SYMPATRIC ASTER AND ERIGERON (ASTERACEAE) IN INTERIOR ALASKA , 1991 .

[137]  P. Klinkhamer,et al.  Pollen dynamics of bumble-bee visitation on Echium vulgare , 1997 .

[138]  K. Holsinger,et al.  Pollen Discounting in Erythronium grandiflorum: Mass-Action Estimates from Pollen Transfer Dynamics , 1994, The American Naturalist.

[139]  M. V. Price,et al.  RESPONSES OF SUBALPINE MEADOW VEGETATION TO FOUR YEARS OF EXPERIMENTAL WARMING , 2000 .

[140]  A. S. Kinyo EFFECTS OF DISTANCE FROM INVASIVE LYTHRUM SALICARIA ON POLLINATOR VISITATION RATE AND REPRODUCTIVE SUCCESS IN NATIVE LYTHRUM ALATUM , 2005 .

[141]  D. Larson,et al.  Insect visitation and pollen deposition in an invaded prairie plant community , 2006 .

[142]  Ignasi Bartomeus,et al.  Contrasting effects of invasive plants in plant–pollinator networks , 2008, Oecologia.

[143]  B. Rathcke Interactions for Pollination among Coflowering Shrubs , 1988 .

[144]  J. Thomson,et al.  THE EFFECT OF A FOREIGN POLLEN ON OVULE DEVELOPMENT IN DIERVILLA LONICERA (CAPRIFOLIACEAE) , 1982 .

[145]  C. Herrera Components of pollinator "quality": comparative analysis of a diverse insect assemblage , 1987 .

[146]  R. M. Straw A Markov Model for Pollinator Constancy and Competition , 1972, American Naturalist.

[147]  Anna Traveset,et al.  Biological invasions as disruptors of plant reproductive mutualisms. , 2006, Trends in ecology & evolution.

[148]  R. Mitchell,et al.  INTERSPECIFIC COMPETITION FOR POLLINATION LOWERS SEED PRODUCTION AND OUTCROSSING IN MIMULUS RINGENS , 2005 .

[149]  J. Thomson Pollen Transport and Deposition by Bumble Bees in Erythronium: Influences of Floral Nectar and Bee Grooming , 1986 .

[150]  R. Wyatt,et al.  POLLINATOR‐MEDIATED COMPETITION, REPRODUCTIVE CHARACTER DISPLACEMENT, AND THE EVOLUTION OF SELFING IN ARENARIA UNIFLORA (CARYOPHYLLACEAE) , 1999, Evolution; international journal of organic evolution.

[151]  C. Caruso COMPETITION FOR POLLINATION INFLUENCES SELECTION ON FLORAL TRAITS OF IPOMOPSIS AGGREGATA , 2000, Evolution; international journal of organic evolution.