Abstract
Competition for pollination is thought to be an important factor structuring flowering in many plant communities, particularly among plant taxa with morphologically similar and easily accessible flowers. We examined the potential for heterospecific pollen transfer (HPT) in a community of four Acacia species in a highly seasonal tropical habitat in Mexico. Partitioning of pollen flow among sympatric species appears to be achieved, in part, through segregation of flowering in seasonal time, and interspecific differences in pollinator guilds. However, two coflowering species (Acacia macracantha and Acacia angustissima) shared multiple flower visitors, raising the possibility of HPT. Each of these coflowering species showed high intraspecific daily synchrony in pollen release, but dehisce at different times of day. Pollinators rapidly harvested available pollen from one species before abandoning it to visit the flowers of the second later in the day. The activity of shared pollinators, predominantly bees, is thus structured throughout the day, and potential for HPT reduced. Suggestive evidence in favour of a resource partitioning explanation for this pattern is provided by the fact that A. macracantha showed significantly greater intraspecific synchrony when coflowering with a potential competitor (A. angustissima) than when flowering alone. We discuss our results in light of previous work on coflowering acacia assemblages in Tanzania and Australia.
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Notes
Flower heads have often been termed ‘inflorescences’, although as defined by the Flora of Australia (vol. 11A, Mimosaceae, Acacia), the term ‘inflorescence’ more properly applies to groups of flower heads on a floral shoot. For clarity we use the term flower head throughout.
References
Armbruster WS (1985) Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution 39:733–752
Armbruster WS (1986) Reproductive interactions between sympatric Dalechampia species: are natural assemblages “random” or organised? Ecology 67:522–533
Armbruster WS, Herzig AL (1984) Partitioning and sharing of pollinators by four sympatric species of Dalechampia (Euphorbiaceae) in Panama. Ann Mo Bot Gard 71:1–16
Armbruster WS, Edwards ME, Debevec EM (1994) Floral character displacement generates assemblage structure of western Australian triggerplants (Stylidium). Ecology 75:315–329
Ashman TL (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81:2577–2591
Ashman TL, Schoen DJ (1994) How long should flowers live? Nature 371:788–791
Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering of the Dipterocarpaceae: new insights into floral induction and the evolution of mast flowering in the aseasonal tropics. Am Nat 132:44–66
Bailey MA, Mian MAR, Carter TE, Ashley DA, Boerma HR (1997) Pod dehiscence of soybean: identification of quantitative trait loci. J Hered 88:152–154
Bennett B, Bread MD (1985) The nesting biology, mating behaviour and foraging ecology of Perdita opuntiae (Andrenidae). J Kansas Entomol Soc 58:185–194
Bernhardt P (1987) A comparison of the diversity, density and foraging behaviour of bees and wasps on Australian Acacia. Ann Mo Bot Gard 74:42–50
Bernhardt P, Kenrick J, Knox RB (1984) Pollination biology and the breeding system of Acacia retinodes (Leguminosae: Mimosoideae). Ann Mo Bot Gard 71:17–29
Bierzychudek P (1981) Asclepias, Lantana and Epidendrum: a floral mimicry complex? Biotropica 13:54–58
Bonner LJ, Dickinson HG (1990) Anther dehiscence in Lycopersicon esculentum II. water relations. New Phytol 115:367–375
Brown JH, Wilson EO (1956) Character displacement. Syst Zool 5:49–64
Buchmann SL (1983) Buzz-pollination in Angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Scientific and Academic Editions, New York, pp 73–113
Buchmann SL, Cane JH (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia 81:289–294
Bullock SH, Solis-Magallanes JA (1990) Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:22–35
Butler CG, Finney DJ (1942) The influence of various physical and biological aspects of the environment on honeybee activity: an examination of the relationship between activity and solar radiation. J Exp Biol 18:206–212
Chappill JA, Maslin BR (eds) (1995) A phylogenetic assessment of the tribe Acacieae. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435
Chittka L, Ings TC, Raine NE (2004) Chance and adaptation in the evolution of island bumblebee behaviour. Popul Ecol 46:243–251
Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377
Cole CB (1981) Overlap, regularity and flowering phenologies. Am Nat 117:993–997
Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35:131–138
Cook JM, Rasplus JY (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18:241–248
Corbet SA, Chapman H, Saville N (1988) Vibratory pollen collection and flower form: bumble bees on Actinidia, Symphytum, Borago and Polygonatum. Funct Ecol 2:147–155
Dornhaus A, Chittka L (1999) Evolutionary origins of bee dances. Nature 401:38
Dornhaus A, Chittka L (2004) Why do honey bees dance? Behav Ecol Sociobiol 55:395–401
Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210
Feinsinger P (1987) Effects of plants species on each others’ pollination—is community structure influenced? Trends Ecol Evol 2:123–126
Fenchel T (1975) Character displacement and coexistence in mud snails (Hydrobiidae). Oecologia 20:19–32
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol S 35:375–403
Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77:1061–1073
Frankie GW, Opler PA, Bawa KS (1976) Foraging behaviour of solitary bees: implications for outcrossing of a neotropical forest tree species. J Ecol 64:1049–1057
Frankie GW, Haber WA, Opler PA, Bawa KS (1983) Characteristics and organization of the large bee pollination system in the Costa Rican dry forest. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Scientific and Academic Editions, pp 411–447
Gilbert FS (1981) Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecol Entomol 6:245–262
Ginsberg HS (1984) Foraging behavior of the bees Halictus ligatus (Hymenoptera: Halictidae) and Ceratina calcarata (Hymenoptera: Anthophoridae). J NY Entomol Soc 92:162–168
Gleeson SK (1981) Character displacement in flowering phenologies. Oecologia 51:294–295
Goulson D, Wright N (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav Ecol 9:213–219
Grant PR (1972) Convergent and divergent character displacement. Biol J Linn Soc 4:39–68
Grant WF (1996) Seed pod shattering in the genus Lotus (Fabaceae)—a synthesis of diverse evidence. Can J Plant Sci 76:447–456
Heinrich B (1976) Resource partitioning among some eusocial insects: bumblebees. Ecology 57:874–889
Heithaus ER (1974) The role of plant–pollinator interactions in determining community structure. Ann Mo Bot Gard 61:676–691
Herrera CM (1997) Thermal biology and foraging responses of insect pollinators to the forest floor irradiance mosaic. Oikos 78:601–611
Hocking B (1968) Insect-flower associations of the high arctic with special reference to nectar. Oikos 19:359–387
Horvitz CC, Schemske DW (1990) Spatiotemporal variation in insect mutualists of a neotropical herb. Ecology 71:1085–1097
Huey RB, Pianka ER (1974) Ecological character displacement in a lizard. Am Zool 14:1127–1136
Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59:672–678
Janzen DH (1967) Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21:620–637
Johnson SD (1992) Climatic and phylogenetic determinants of flowering seasonality in the cape flora. J Ecol 81:567–572
Jolivet P (1995) Observations on the host-plants of Chrysomelidae (Coleoptera). Entomologiste 51:77–93
Kay QON (1976) Preferential pollination of yellow-flowered morphs of Raphanus raphinistrum by Pieris and Eristalis spp. Nature 261:230–232
Keijzer CJ (1987) The process of anther dehiscence and pollen dispersal: 1. the opening mechanism of longitudinally dehiscing anthers. New Phytol 105:487–498
Kenrick J (2003) Review of pollen–pistil interactions and their relevance to the reproductive biology of Acacia. Aust Syst Bot 16:119–130
Kephart SR (1983) The partitioning of pollinators among three species of Asclepias. Ecology 64:120–133
Knox RB, Kenrick J (1982) Polyad function in relation to the breeding system of Acacia. In: Mulcahy D, Ottavianopp E (eds) Pollen biology. North Holland Press, Amsterdam, Holland, pp 411–418
Kochmer JP, Handel SN (1986) Constraints and competition in the evolution of flowering phenology. Ecol Monogr 56:303–325
Laverty TM (1980) The flower-visiting behaviour of bumble bees: floral complexity and learning. Can J Zool 58:1324–1335
Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47:531–545
Levin DA (1978) The origins of isolating mechanisms in flowering plants. Evol Biol 11:185–317
Levin DA, Anderson WW (1970) Competition for pollinators between simultaneously flowering species. Am Nat 104:455–467
Lunau K, Maier EJ (1995) Innate color preferences of flower visitors. J Comp Physiol A 177:1–19
Maslin BR (2006) Generic and infrageneric names in Acacia following retypification of the genus. http://www.worldwidewattle.com/infogallery/taxonomy/names-for-acacia-following-ibc.pdf. Cited July 2006
Maslin BR, Miller JT, Seigler DS (2003) Overview of the generic status of Acacia (Leguminosae: Mimosoideae). Aust Syst Bot 16:1–18
Michener CD (1974) The social behavior of the bees: a comparative study. Belknap Press of Harvard University Press, Cambridge
Minckley RL, Wcislo WT, Yanega D, Buchmann SL (1994) Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75:1406–1419
Mosquin T (1971) Competition for pollinators as a stimulus for the evolution of flowering time. Oikos 22:398–402
Motten AF (1986) Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol Monogr 56:21–42
Motten AF, Campbell DR, Alexander DR, Miller HL (1981) Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62:1278–1287
Murray KG, Feinsinger P, Busby WH, Linhart YB, Beach JH, Kinsman S (1987) Evaluation of character displacement in two tropical pollination guilds. Ecology 68:1283–1293
Ollerton J, Lack AJ (1992) Flowering phenology: an example of relaxation of natural selection? Trends Ecol Evol 7:274–276
Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland asclepiads in South Africa. Ann Bot Lond 92:807–834
Parmenter L (1958) Flies (Diptera) and their relations with plants. Lond Nat 37:115–125
Pianka ER (1973) The structure of lizard communities. Ann Rev Ecol Syst 4:53–74
Pleasants JM (1980) Competition for bumblebee pollinators in rocky mountain plant communities. Ecology 61:1446–1459
Pleasants JM (1983) Structure of plant and pollinator communities. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 375–393
Poole RW, Rathcke B (1979) Regularity, randomness and aggregation in flowering phenologies. Science 203:470–471
Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Harper Collins, London
Raine NE (2001) The pollination ecology of a Mexican Acacia community. D. Phil. thesis, University of Oxford, Oxford
Raine NE, Chittka L (2005) Comparison of flower constancy and foraging performance in three bumblebee species (Hymenoptera: Apidae: Bombus). Entomol Gen 28:81–89
Raine NE, Chittka L (2007a) Flower constancy and memory dynamics in bumblebees (Hymenoptera: Apidae: Bombus). Entomol Gen 29:179–199
Raine NE, Chittka L (2007b) Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Naturwissenschaften 94:459–464
Raine NE, Willmer P, Stone GN (2002) Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in a Mexican ant-acacia. Ecology 83:3086–3096
Raine NE, Gammans N, MacFadyen IJ, Scrivner GK, Stone GN (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant-plant. Ecol Entomol 29:345–352
Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L (2006) Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Adv Stud Behav 36:305–354
Rathcke B (1983) Competition and facilitation among plants for pollination. In: Real L (ed) Pollination biology. Academic Press, Orlando, FL, pp 305–329
Rathcke B (1988) Flowering phenologies in a shrub community: competition and constraints. J Ecol 76:975–994
Reich PB, Borchert R (1984) Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J Ecol 72:61–74
Ross JH (1981) An analysis of the African Acacia species: their distribution, possible origins and relationships. Bothalia 13:389–413
Rothstein SI (1973) The niche variation model—is it valid? Am Nat 107:598–620
Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge, Massachusetts
Roubik DW (1992) Loose niches in tropical communities: why are there so few bees and so many trees? In: Hunter MD, Ohgushi T, Price PW (eds) Effects of resource distribution on animal–plant interactions. Academic Press, New York, pp 327–354
Schoener TW (1970) Non-synchronous spatial overlap of lizards in patchy habitats. Ecology 51:408–418
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285
Slatkin M (1980) Ecological character displacement. Ecology 61:163–177
Sokal RR, Rohlf FJ (1981) Biometry. W.H. Freeman, New York, USA
Stone GN (1994) Activity patterns of females of the solitary bee Anthophora plumipes in relation to temperature, nectar supplies and body size. Ecol Entomol 19:177–189
Stone GN (1995) Female foraging responses to sexual harassment in the solitary bee Anthophora plumipes. Anim Behav 50:405–412
Stone GN, Loder PMJ, Blackburn TM (1995) Foraging and courtship behaviour in males of the solitary bee Anthophora plumipes (Hymenoptera: Anthophoridae): thermal physiology and the roles of body size. Ecol Entomol 20:169–183
Stone G, Willmer P, Nee S (1996) Daily partitioning of pollinators in an African Acacia community. Proc Roy Soc B 263:1389–1393
Stone GN, Amos JN, Stone TF, Knight RJ, Gay H, Parrott F (1988) Thermal effects on activity patterns and behavioural switching in a concourse of foragers on Stachytarpheta mutabilis (Verbenaceae) in Papua New Guinea. Oecologia 77:56–63
Stone GN, Willmer PG, Rowe JA (1998) Partitioning of pollinators during flowering in an African Acacia community. Ecology 79:2808–2827
Stone GN, Gilbert F, Willmer P, Potts S, Fayez S, Samy Z (1999a) Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecol Entomol 24:208–221
Stone GN, Willmer PG, Rowe JA, Nyundo B, Abdallah A (1999b) The pollination ecology of Mkomazi Acacia species. In: Coe MJ, McWilliam NC, Stone GN, Packer MJ (eds) Mkomazi: the ecology, biodiversity and conservation of a Tanzanian Savanna. Royal Geographical Society (with the Institute of British Geographers), London, pp 337–360
Stone GN, Raine NE, Prescott M, Willmer PG (2003) The pollination ecology of Acacias (Fabaceae, Mimosoideae). Aust Syst Bot 16:103–118
Strickler K (1979) Specialization and foraging efficiency of solitary bees. Ecology 60:998–1009
Thorp RW (1979) Structural, behavioral and physiological adaptations of bees for collecting pollen. Ann Mo Bot Gard 66:788–812
Thorp RW (2000) The collection of pollen by bees. Plant Syst Evol 222:211–223
Tybirk K (1993) Pollination, breeding systems and seed abortion in some African acacias. Bot J Linn Soc 112:107–137
Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–390
Waser NM (1978a) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59:934–944
Waser NM (1978b) Interspecific pollen transfer and competition between co-occurring plant species. Oecologia 36:223–236
Waser NM (1983) Competition for pollination and floral character differences among sympatric plant species: a review of evidence. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 277–293
Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127:593–603
Waser NM, Fugate ML (1986) Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata. Oecologia 70:573–577
Williams MR (1995) Critical values of a statistic to detect competitive displacement. Ecology 76:646–647
Willmer PG, Stone GN (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. Adv Stud Behav 34:347–466
Wright SJ, Calderon O (1995) Phylogenetic patterns among tropical flowering phenologies. J Ecol 83:937–948
Acknowledgements
We would like to thank Miguel Franco, Graham Floater, Tim Jones, Rubén Pérez, and Juan Ramón Zárate for their considerable help in México, Paul Johnson, George McGavin, David Raubenheimer, David Roberts and Steve Simpson for their assistance in Oxford, and the Estación de Biologia de Chamela IBUNAM for permission to conduct research. Thanks to Ricardo Ayala-Barajas, Felipe Noguera-Martínez, Alicia Rodriguez-Palafox and Arturo Solís-Magallanes for their invaluable taxonomic expertise, and to Mike Raine and two anonymous referees for comments on earlier versions of this manuscript. We are particularly grateful to Rosario ‘Chayo’ Velasco-Aceuedo and everyone at El Tejaban for sustaining the project. NER was supported by a postgraduate studentship from the William Edward’s Educational Charity, Kenilworth, a Varley-Gradwell fellowship from the Department of Zoology, University of Oxford, and Magdalen College, Oxford. GNS was supported by grants from the NERC (GR9/03553) and the Royal Society. This work was supported by the E.P.A. Cephalosporin Fund, the Percy Sladen Memorial Fund c/o Linnean Society of London and Acacia Bank California.
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Alice Sharp Pierson is no longer working as research biologist.
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Raine, N.E., Pierson, A.S. & Stone, G.N. Plant–pollinator interactions in a Mexican Acacia community. Arthropod-Plant Interactions 1, 101–117 (2007). https://doi.org/10.1007/s11829-007-9010-7
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DOI: https://doi.org/10.1007/s11829-007-9010-7