Many recent studies have suggested that the majority of animal-pollinated plants have a higher diversity of pollinators than that expected according to their pollination syndrome. This broad generalization, often based on pollination web data, has been challenged by the fact that some floral visitors recorded in pollination webs are ineffective pollinators. To contribute to this debate, and to obtain a contrast between visitors and pollinators, we studied insect and bird visitors to virgin flowers of Hypoestes aristata in the Bamenda Highlands, Cameroon. We observed the flowers and their visitors for 2-h periods and measured the seed production as a metric of reproductive success. We determined the effects of individual visitors using 2 statistical models, single-visit data that were gathered for more frequent visitor species, and frequency data. This approach enabled us to determine the positive as well as neutral or negative impact of visitors on H. aristata's reproductive success. We found that (i) this plant is not generalized but rather specialized; although we recorded 15 morphotaxa of visitors, only 3 large bee species seemed to be important pollinators; (ii) the carpenter bee Xylocopa cf. inconstans was both the most frequent and the most effective pollinator; (iii) the honey bee Apis mellifera acted as a nectar thief with apparent negative effects on the plant reproduction; and (iv) the close relationship between H. aristata and carpenter bees was in agreement with the large-bee pollination syndrome of this plant. Our results highlight the need for studies detecting the roles of individual visitors. We showed that such an approach is necessary to evaluate the pollination syndrome hypothesis and create relevant evolutionary and ecological hypotheses.

Faculty of Science University of South Bohemia České Budějovice Czech Republic

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Willmer P (2011) Pollination and floral ecology. Princeton and Oxford: Princeton University Press. 778 p.

Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 1st edn. London: Murray John. PubMed PMC

Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. Annual Review of Ecology and Systematics 1: 307–326.

Faegri K, van der Pijl L (1979) The principles of pollination ecology, third revised edition. Oxford: Pergamon Press xi. 244 p.

Hodges SA, Arnold ML (1994) Columbines - a geographically widespread species flock. Proceedings of the National Academy of Sciences of the United States of America 91: 5129–5132. PubMed PMC

Renner SS, Feil JP (1993) Pollinators of Tropical Dioecious Angiosperms. American Journal of Botany 80: 1100–1107.

Manning JC, Goldblatt P (1997) The Moegistorhynchus longirostris (Diptera: Nemestrinidae) pollination guild: Long-tubed flowers and a specialized long-proboscid fly pollination system in southern Africa. Plant Systematics and Evolution 206: 51–69.

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

Ollerton J, Alarcon R, Waser NM, Price MV, Watts S, et al. (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103: 1471–1480. PubMed PMC

Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytologist 165: 81–89. PubMed

Primack RB (1979) Reproductive-biology of Discaria-Toumatou (Rhamnaceae). New Zealand Journal of Botany 17: 9–13.

Bullock SH, Delrio CM, Ayala R (1989) Bee visitation rates to trees of Prockia-Crucis differing in flower number. Oecologia 78: 389–393. PubMed

Beattie AJ (1971) Pollination mechanisms in Viola. New Phytologist 70: 343–360.

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

Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2395–2399. PubMed PMC

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

Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6: 69–81.

Olesen JN, Dupont YL, Ehlers BK, Hansen DM (2007) The openness of a flower and its number of flower-visitor species. Taxon 56: 729–736.

Niemirski R, Zych M (2011) Fly pollination of dichogamous Angelica sylvestris (Apiaceae): how (functionally) specialized can a (morphologically) generalized plant be? Plant Systematics and Evolution 294: 147–158.

Kishore K, Kalita H, Singh M, Avasthe R, Pandey B, et al. (2011) Pollination studies in large cardamom (Amomum subulatum Roxb.) of Sikkim Himalayan region of India. Scientia Horticulturae 129: 735–741.

Inouye DW (1980) The terminology of floral larceny. Ecology 61: 1251–1253.

Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81: 2651–2661.

Roubik DW (1982) The ecological impact of nectar-robbing bees and pollinating hummingbirds on tropical shrub. Ecology 63: 354–360.

Janeček Š, Patáčová E, Bartoš M, Padyšáková E, Spitzer L, et al. (2011) Hovering sunbirds in the Old World: occasional behaviour or evolutionary trend? Oikos 120: 178–183.

Herrera CM (1987) Components of pollinator quality - comparative analysis of a diverse insect assemblage. Oikos 50: 79–90.

Herrera CM (1989) Pollinator abundance, morphology, and flower visitation rate - analysis of the quantity component in a plant-pollinator system. Oecologia 80: 241–248. PubMed

Stone JL (1996) Components of pollination effectiveness in Psychotria suerrensis, a tropical distylous shrub. Oecologia 107: 504–512. PubMed

Inouye DW, Gill DE, Dudash MR, Fenster CB (1994) A model and lexicon for pollen fate. American Journal of Botany 81: 1517–1530.

Mayfield MM, Waser NM, Price MV (2001) Exploring the ‘most effective pollinator principle’ with complex flowers: Bumblebees and Ipomopsis aggregata. Annals of Botany 88: 591–596.

Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: Experiments with pollen and fluorescent dye. Annals of Botany 97: 141–150. PubMed PMC

Young HJ, Dunning DW, von Hasseln KW (2007) Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). American Journal of Botany 94: 1267–1271. PubMed

Ne’eman G, Jurgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biological Reviews 85: 435–451. PubMed

Olsen KM (1997) Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109: 114–121. PubMed

Sahli HF, Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanismum (Brassicaceae). American Journal of Botany 94: 203–209. PubMed

Robertson IC, Leavitt H (2011) Relative contributions to seed production by floral visitors of slickspot peppergrass, Lepidium papilliferum (Brassicaceae). Arthropod-Plant Interactions 5: 379–389.

Lara C, Ornelas JF (2001) Preferential nectar robbing of flowers with long corollas: experimental studies of two hummingbird species visiting three plant species. Oecologia 128: 263–273. PubMed

Dedej S, Delaplane KS (2004) Nectar-robbing carpenter bees reduce seed-setting capability of honey bees (Hymenoptera : Apidae) in rabbiteye blueberry, Vaccinium ashei, ‘Climax’. Environmental Entomology 33: 100–106.

Castro S, Silveira P, Navarro L (2008) Consequences of nectar robbing for the fitness of a threatened plant species. Plant Ecology 199: 201–208.

van der Pijl L (1960) Ecological aspects of flower evolution. I. Phyletic evolution. Evolution 14: 403–416.

Potgieter CJ, Edwards TJ (2005) The Stenobasipteron wiedemanni (Diptera, Nemestrinidae) pollination guild in Eastern Southern Africa. Annals of the Missouri Botanical Garden 92: 254–267.

Larsen MW, Peter C, Johnson SD, Olesen JM (2008) Comparative biology of pollination systems in the African-Malagasy genus Brownleea (Brownleeinae : Orchidaceae). Botanical Journal of the Linnean Society 156: 65–78.

Riegert J, Fainova D, Antczak M, Sedlacek O, Horak D, et al. (2011) Food niche differentiation in two syntopic sunbird species: a case study from the Cameroon Mountains. Journal of Ornithology 152: 819–825.

Bartoš M, Janeček Š, Padyšáková E, Patáčová E, Altman J, et al. (2012) Nectar properties of the sunbird-pollinated plant Impatiens sakeriana: A comparison with six other co-flowering species. South African Journal of Botany 78: 63–74.

Janeček Š, Riegert J, Bartoš M, Hořák D, Reif J, et al. (2012) Food selection by avian floral visitors: an important aspect of plant-flower interactions in West Africa. Biological Journal of the Linnean Society 107: 355–367.

Cheek M, Onana JM, Pollard JB (2000) The plants of Mount Oku and the Ijim Ridge, Cameroon. A conservation Checklist.: Royal Botanic Gardens, Kew.

Reif J, Sedlacek O, Horak D, Riegert J, Pesata M, et al. (2007) Habitat preferences of birds in a montane forest mosaic in the Bamenda Highlands, Cameroon. Ostrich 78: 31–36.

Tropek R, Konvicka M (2010) Forest eternal? Endemic butterflies of the Bamenda highlands, Cameroon, avoid close-canopy forest. African Journal of Ecology 48: 428–437.

Hepper JMe (1963) Flora of West Tropical Africa, volume 2. Kew, UK: Royal Botanic Gardens.

Balkwill K, Norris FG (1985) Taxonomic studies in the Acanthaceae - the genus Hypoestes in southern Africa. South African Journal of Botany 51: 133–144.

Littell R, Stroup WW, Freund RJ (2002) SAS for Linear Models. Care, North Carolina, USA: SAS Institute Inc.

Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists: Cambridge University Press. 537 p.

Eberly LE (2007) Multiple linear regression: Huumana Press Inc. PubMed

Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E: Plymouth, UK.

Searle SR, Casella G, McCulloch CE (1992) Variance components: John Wiley & Sous Inc.

Renner SS (1989) A survey of reproductive biology in Neotropical Melastomataceae and Memecylaceae. Annals of the Missouri Botanical Garden 76: 496–518.

Raju AJS, Rao SP (2006) Nesting habits, floral resources and foraging ecology of large carpenter bees (Xylocopa latipes and Xylocopa pubescens) in India. Current Science 90: 1210–1217.

Janeček Š, Hrázský Z, Bartoš M, Brom J, Reif J, et al. (2007) Importance of big pollinators for the reproduction of two Hypericum species in Cameroon, West Africa. African Journal of Ecology 45: 607–613.

Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends in Ecology & Evolution 21: 208–216. PubMed

Escaravage N, Wagner J (2004) Pollination effectiveness and pollen dispersal in a Rhododendron ferrugineum (Ericaceae) population. Plant Biology 6: 606–615. PubMed

Silva-Montellano A, Eguiarte LE (2003) Geographic patterns in the reproductive ecology of Agave lechuguilla (Agavaceae) in the Chihuahuan desert. I. Floral characteristics, visitors, and fecundity. American Journal of Botany 90: 377–387. PubMed

Fumero-Caban JJ, Melendez-Ackerman EJ (2007) Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). American Journal of Botany 94: 419–424. PubMed

Hansen DM, Olesen JM, Jones CG (2002) Trees, birds and bees in Mauritius: exploitative competition between introduced honey bees and endemic nectarivorous birds? Journal of Biogeography 29: 721–734.

Celebrezze T, Paton DC (2004) Do introduced honeybees (Apis mellifera, Hymenoptera) provide full pollination service to bird-adapted Australian plants with small flowers? An experimental study of Brachyloma ericoides (Epacridaceae). Austral Ecology 29: 129–136.

Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57: 2742–2752. PubMed

Nassar JM, Ramirez N (2004) Reproductive biology of the melon cactus, Melocactus curvispinus (Cactaceae). Plant Systematics and Evolution 248: 31–44.

Stang M, Klinkhamer PGL, van der Meijden E (2006) Size constraints and flower abundance determine the number of interactions in a plant-flower visitor web. Oikos 112: 111–121.

Stang M, Klinkhamer PGL, van der Meijden E (2007) Asymmetric specialization and extinction risk in plant-flower visitor webs: a matter of morphology or abundance? Oecologia 151: 442–453. PubMed

Stang M, Klinkhamer PGL, Waser NM, Stang I, van der Meijden E (2009) Size-specific interaction patterns and size matching in a plant-pollinator interaction web. Annals of Botany 103: 1459–1469. PubMed PMC

Herrera CM (1995) Microclimate and individual variation in pollinators - flowering plants are more than their flowers. Ecology 76: 1516–1524.

Herrera CM (1988) Variation in mutualism - the spatio-temporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35: 95–125.

Eckhart VM (1992) Spatiotemporal variation in abundance and variation in foraging behavior of the pollinators of gynodioecious Phacelia-Linearis (Hydrophyllaceae). Oikos 64: 573–586.

Cane JH, Payne JA (1993) Regional, annual, and seasonal-variation in pollinator guilds - intrinsic traits of bees (Hymenoptera, Apoidea) underlie their patterns of abundance at Vaccinium-Ashei (Ericaceae). Annals of the Entomological Society of America 86: 577–588.

Heithaus ER (1974) Role of plant-pollinator interactions in determining community structure. Annals of the Missouri Botanical Garden 61: 675–691.

Grant V, Grant KA (1979) Pollination of north-american cacti. 5. Pollination spectrum in the southwestern american cactus flora. Plant Systematics and Evolution 133: 29–37.

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology Evolution and Systematics 35: 375–403.

Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: The apparent paradox of plant-pollinator systems. Journal of Ecology 84: 767–769.

Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability - a precondition for mutualism specialization. Science 225: 519–521. PubMed

Asymmetric competition for nectar between a large nectar thief and a small pollinator: an energetic point of view