Generalist pollinators are important in many habitats, but little research has been done on small-scale spatial variation in interactions between them and the plants that they visit. Here, using a spatially explicit approach, we examined whether multiple species of flowering plants occurring within a single meadow showed spatial structure in their generalist pollinator assemblages. We report the results for eight plant species for which at least 200 individual visits were recorded. We found that for all of these species, the proportions of their general pollinator assemblages accounted for by particular functional groups showed spatial heterogeneity at the scale of tens of metres. This heterogeneity was connected either with no or only subtle changes of vegetation and flowering species composition. In five of these species, differences in conspecific plant density influenced the pollinator communities (with greater dominance of main pollinators at low-conspecific plant densities). The density of heterospecific plant individuals influenced the pollinator spectrum in one case. Our results indicate that the picture of plant-pollinator interactions provided by averaging data within large plots may be misleading and that within-site spatial heterogeneity should be accounted for in terms of sampling effort allocation and analysis. Moreover, spatially structured plant-pollinator interactions may have important ecological and evolutionary consequences, especially for plant population biology.

Department of Botany Faculty of Science Charles University Prague Czech Republic

See more in PubMed

Lázaro A, Hegland SJ, Totland Ø (2008) The relationships between floral traits and specificity of pollination systems in three Scandinavian plant communities. Oecologia 157: 249–257. PubMed

Memmott J (1999) The structure of a plant-pollinator food web. Ecol Lett 2: 276–280. PubMed

Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89: 1573–1582. PubMed

Bartomeus I, Vila M, Steffan-Dewenter I (2010) Combined effects of Impatiens glandulifera invasion and landscape structure on native plant pollination. J Ecol 98: 440–450.

Forup ML, Henson KSE, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands. J Appl Ecol 45: 742–752.

Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, et al. (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458: 1018–U1091. PubMed

Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. P Natl Acad Sci USA 104: 19891–19896. PubMed PMC

Waser NM (1986) Flower constancy - Definition, cause, and measurement. Am Nat 127: 593–603.

Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11: 564–575. PubMed

Olesen JM, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83: 2416–2424.

Morales JM, Vázquez DP (2008) The effect of space in plant-animal mutualistic networks: insights from a simulation study. Oikos 117: 1362–1370.

Herrera CM (2005) Plant generalization on pollinators: Species property or local phenomenon? Am J Bot 92: 13–20. PubMed

Greig-Smith P (1983) Quantitative plant ecology. Oxford: Blackwell Scientific.

Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153: 589–596. PubMed

Goulson D (2010) Bumblebees - Behaviour, ecology, and conservation. Oxford: Oxford University Press. 317 p.

Jakobsson A, Lázaro A, Totland Ø (2009) Relationships between the floral neighborhood and individual pollen limitation in two self-incompatible herbs. Oecologia 160: 707–719. PubMed

Schuett EM, Vamosi JC (2010) Phylogenetic community context influences pollen delivery to Allium cernuum . Evol Biol 37: 19–28.

Brunet J, Sweet HR (2006) Impact of insect pollinator group and floral display size on outcrossing rate. Evolution 60: 234–246. PubMed

Larsson M (2005) Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knautia arvensis (Dipsacaceae). Oecologia 146: 394–403. PubMed

Williams NM, Kremen C (2007) Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17: 910–921. PubMed

Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31: 389–394.

Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77: 1043–1060.

Gibson RH, Knott B, Eberlein T, Memmott J (2011) Sampling method influences the structure of plant-pollinator networks. Oikos 120: 822–831.

Tolasz R, editor (2007) Atlas podnebí Česka [Climatic atlas of the Czech Republic]. Praha: Český hydrometeorologický ústav. 255 p.

Chytrý M, editor (2007) Vegetace České republiky. 1. Travinná a keříčková veegtace [Vegetation of the Czech Republic. Vol. 1 - Grassland and heathland vegetation]. 1. vydání ed. Praha, Česká republika: Academia. 528 p.

ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Ithaca: Microcomputer Power.

Legendre P, Legendre L (2003) Numerical Ecology. Amsterdam, Netherlands: Elsevier. 853 p.

Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge: Cambridge University Press.

Lázaro A, Lundgren R, Totland Ø (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118: 691–702.

Hegland SJ, Boeke L (2006) Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol 31: 532–538.

Bosch M, Waser NM (1999) Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae). Am J Bot 86: 871–879. PubMed

Klinkhamer PGL, de Jong TJ (1990) Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare (Boraginaceae). Oikos 57: 399–405.

Kunin WE (1997) Population size and density effects in pollination: Pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber . J Ecol 85: 225–234.

Kirchner F, Luijten SH, Imbert E, Riba M, Mayol M, et al. (2005) Effects of local density on insect visitation and fertilization success in the narrow-endemic Centaurea corymbosa (Asteraceae). Oikos 111: 130–142.

Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126: 76–83. PubMed

Rader R, Howlett BG, Cunningham SA, Westcott DA, Newstrom-Lloyd LE, et al. (2009) Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J Appl Ecol 46: 1080–1087.

Hegland SJ, Grytnes J-A, Totland Ø (2009) The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecol Res 24: 929–936.

Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94: 295–304.

Kunin WE (1993) Sex and the single mustard - Population density and pollinator behavior effects on seed set. Ecology 74: 2145–2160.

Charnov EL (1976) Optimal foraging, marginal value theorem. Theor Popul Biol 9: 129–136. PubMed

Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, et al. (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36: 519–533.

Sowig P (1989) Effects of flowering plants patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera, Apidae). Oecologia 78: 550–558. PubMed

Forup ML, Memmott J (2005) The relationship between the abundances of bumblebees and honeybees in a native habitat. Ecol Entomol 30: 47–57.

Dorado J, Vazquez DP, Stevani EL, Chacoff NP (2011) Rareness and specialization in plant-pollinator networks. Ecology 92: 19–25. PubMed

Chacoff NP, Vazquez DP, Lomascolo SB, Stevani EL, Dorado J, et al. (2012) Evaluating sampling completeness in a desert plant-pollinator network. J Anim Ecol 81: 190–200. PubMed

Blüthgen N (2010) Why network analysis is often disconnected from community ecology: A critique and an ecologist's guide. Basic Appl Ecol 11: 185–195.

Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany 103: 1445–1457. PubMed PMC

Experimental loss of generalist plants reveals alterations in plant-pollinator interactions and a constrained flexibility of foraging

Flower visitation by hoverflies (Diptera: Syrphidae) in a temperate plant-pollinator network