Generalist versus specialist pollination systems in 26 Oenothera (Onagraceae)

Kyra Neipp Krakos; Scott A. Fabricant

doi:10.26786/1920-7603(2014)23

Authors

Kyra Neipp Krakos Maryville University
Scott A. Fabricant Macquarie University

DOI:

https://doi.org/10.26786/1920-7603(2014)23

Abstract

Although generalized and specialized plants are often discussed as alternative states, the biological reality may better be viewed as a continuum. However, estimations of pollinator specificity have been confounded in some studies by the assumption that all floral visitors are pollinators. Failure to account for pollen load can lead to inaccurate conclusions regarding the number of pollinators with which a species actually interacts. The aim of this study was to clarify the distribution of pollination-system specialization within one clade, using a more rigorous assessment of pollen flow. The genus Oenothera has long been used as a model system for studying reproductive biology, and it provides a diversity of pollination systems and a wealth of historical data. Both floral visitation rate and pollen-load analysis of sampled pollinators, combined into a metric of pollen flow, were used to quantify the pollination systems of 26 Oenothera taxa. Metric of pollinator specialization were calculated as functions of both total pollinator taxa, and as pollinator functional groups. We found that for Oenothera, the number of floral visitors highly overestimates the number of pollinators, and is inadequate for determining or predicting pollination system specialization. We found that that pollination systems were distributed on a gradient from generalized to specialized, with more pollinator-specialized plant taxa, especially when estimated using pollinator functional groups. These results are in conflict with previous studies that depict most plant species as generalists, and this finding may be related to how prior studies have estimated specialization.

Author Biographies

Kyra Neipp Krakos, Maryville University

Asst Professor of Biology

Scott A. Fabricant, Macquarie University

Department of Biological Science

References

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. DOI: https://doi.org/10.1093/aob/mcj012

Alarcon R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117:1796-1807. DOI: https://doi.org/10.1111/j.0030-1299.2008.16987.x

Armbruster WS (1985) Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution 9(4): 733-752. DOI: https://doi.org/10.1111/j.1558-5646.1985.tb00416.x

Armbruster, WS (1992) Phylogeny and the evolution of plant-animal interactions. BioScience 42(1): 12-20. DOI: https://doi.org/10.2307/1311623

Armbruster WS, Keller S, Matsuki M, Clausen TP (1989). Pollination of Dalechampia magnoliifolia (Euphorbiaceae) by male Euglossine bees. American Journal of Botany 76(9): 1279-1285. DOI: https://doi.org/10.1002/j.1537-2197.1989.tb15109.x

Ashworth L, Quesada M, Casas A, Aguilar R, Oyama K (2009) Pollinator-dependent food production in Mexico. Biological Conservation 142:1050-1057. DOI: https://doi.org/10.1016/j.biocon.2009.01.016

Bascompte J (2009) Mutualistic networks. Frontiers in Ecology and the Environment 7:429-436. DOI: https://doi.org/10.1890/080026

Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100:9383-9387. DOI: https://doi.org/10.1073/pnas.1633576100

Bernhardt P, Sage T, Weston P, Azuma H, Lam M, Thien LB, Bruhl J (2003) The pollination of Trimenia moorei (Trimeniaceae): Floral volatiles, insect/wind pollen vectors and stigmatic self-incompatibility in a basal angiosperm. Annals of Botany 92:445-458. DOI: https://doi.org/10.1093/aob/mcg157

Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351-354. DOI: https://doi.org/10.1126/science.1127863

Bosch J, Martín González AM, Rodrigo A, Navarro D (2009) Plant–pollinator networks: adding the pollinator’s perspective. Ecology Letters 12:409-419. DOI: https://doi.org/10.1111/j.1461-0248.2009.01296.x

Buchmann SL, Nabhan FP (1996) The Forgotten Pollinators. Shearwater Books, Washington D.C.

Cayenne Engel E, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. American Journal of Botany 90:1612-1618. DOI: https://doi.org/10.3732/ajb.90.11.1612

Clinebell RR, Crowe A, Gregory DP, Hoch PC (2004) Pollination ecology of Gaura and Calylophus (Onagraceae, Tribe Onagreae) in western Texas, USA. Annals of the Missouri Botanical Garden 91:369-400.

Crane PR, Friis EM, Pedersen KR (1995) The origin and early diversification of angiosperms. Nature 374:27-33. DOI: https://doi.org/10.1038/374027a0

De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends in Ecology & Evolution 20:591-597. DOI: https://doi.org/10.1016/j.tree.2005.07.008

Endress PK (1994) Floral structure and evolution of primitive angiosperms - recent advances. Plant Systematics and Evolution 192:79-97. DOI: https://doi.org/10.1007/BF00985910

Faegri K, Pijl Lvd (1966) The principles of pollination ecology. Pergamon, Oxford, UK

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. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Forup ML, Henson KSE, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. Journal of Applied Ecology 45:742-752. DOI: https://doi.org/10.1111/j.1365-2664.2007.01390.x

Freckleton R (2000) Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence. Functional Ecology 14:129-134. DOI: https://doi.org/10.1046/j.1365-2435.2000.00400.x

Fumero-Cabán JJ, Meléndez-Ackerman EJ (2007) Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). American Journal of Botany 94:419-424. DOI: https://doi.org/10.3732/ajb.94.3.419

Goldblatt P, Manning JC, Bernhardt P (1998) Adaptive radiation of bee-pollinated Gladiolus species (Iridaceae) in southern Africa. Annals of the Missouri Botanical Garden 85:492-517. DOI: https://doi.org/10.2307/2992045

Grant V, Grant KA (1965) Flower pollination in the Phlox family. Columbia University Press, New York, NY

Grimaldi D (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Annals of the Missouri Botanical Garden 86:373-406. DOI: https://doi.org/10.2307/2666181

Hoch PC, Crisci JV, Tobe H, Berry PE (1993) A cladistic analysis of the plant family Onagraceae. Systematic Botany 18:31-47. DOI: https://doi.org/10.2307/2419786

Hoggard GD, Kores PJ, Molvray M, Hoggard RK (2004) The phylogeny of Gaura (Onagraceae) based on ITS, ETS, and trnl-F sequence data. American Journal of Botany 91:139-148. DOI: https://doi.org/10.3732/ajb.91.1.139

Jacobs J, Clark S, Denholm I, Goulson D, Stoate C, Osborne J (2010) Pollinator effectiveness and fruit set in common ivy, Hedera helix (Araliaceae). Arthropod-Plant Interactions 4:19-28. DOI: https://doi.org/10.1007/s11829-009-9080-9

Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends in Ecology & Evolution 15:140-143. DOI: https://doi.org/10.1016/S0169-5347(99)01811-X

King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution 4:811-818. DOI: https://doi.org/10.1111/2041-210X.12074

Levin RA, Wagner WL, Hoch PC, Hahn WJ, Rodriguez A, Baum DA, Katinas L, Zimmer EA, Sytsma KJ (2004) Paraphyly in tribe Onagreae: Insights into phylogenetic relationships of Onagraceae based on nuclear and chloroplast sequence data. Systematic Botany 29:147-164. DOI: https://doi.org/10.1600/036364404772974293

Levin RA, Wagner WL, Hoch PC, Nepokroeff M, Pires JC, Zimmer EA, Sytsma KJ (2003) Family-level relationships of Onagraceae based on chloroplast rbcL and ndhF data. American Journal of Botany 90:107-115. DOI: https://doi.org/10.3732/ajb.90.1.107

Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Annals of Botany 94:365-376. DOI: https://doi.org/10.1093/aob/mch152

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. DOI: https://doi.org/10.1006/anbo.2001.1500

Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society of London Series B-Biological Sciences 271:2605-2611. DOI: https://doi.org/10.1098/rspb.2004.2909

Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant-pollinator interactions. Annals of Botany 103:1355-1363. DOI: https://doi.org/10.1093/aob/mcp122

Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). American Journal of Botany 88:1615-1622. DOI: https://doi.org/10.2307/3558406

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. DOI: https://doi.org/10.1111/j.1469-185X.2009.00108.x

Nonnenmacher HF (1999) The comparative floral ecology of vernal and autumnal Onagraceae in and near Konza Prairie Research Natural Area, Kansas. PhD, St. Louis University, St. Louis

Nosil P, Mooers AO (2005) Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59:2256-2263. DOI: https://doi.org/10.1111/j.0014-3820.2005.tb00933.x

Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: The apparent paradox of plant-pollinator systems. Journal of Ecology 84:767-769. DOI: https://doi.org/10.2307/2261338

Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103:1471-1480. DOI: https://doi.org/10.1093/aob/mcp031

Padyšáková E, Bartoš M, Tropek R, Janeček Š (2013) Generalization versus specialization in pollination systems: visitors, thieves, and pollinators of Hypoestes aristata (Acanthaceae). PLoS One 8:e59299. DOI: https://doi.org/10.1371/journal.pone.0059299

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. Ecology Letters 11:564-575. DOI: https://doi.org/10.1111/j.1461-0248.2008.01170.x

Popic TJ, Wardle GM, Davila YC (2013) Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecology 38:76-86. DOI: https://doi.org/10.1111/j.1442-9993.2012.02377.x

Raven PH (1979) A survey of reproductive biology in Onagraceae. New Zealand Journal of Botany 17:575-593. DOI: https://doi.org/10.1080/0028825X.1979.10432572

Raven PH (ed) (1988) Onagraceae as a model of plant evolution. Chapman and Hall, New York DOI: https://doi.org/10.1007/978-94-009-1207-6_4

Raven PH, Gregory DP (1972) A revision of the genus Gaura (Onagraceae). Memoirs of the Torrey Botany Club 23:1-96.

Reynolds RJ, Fenster CB (2008) Point and interval estimation of pollinator importance: a study using pollination data of Silene caroliniana. Oecologia 156(2): 325-332. DOI: https://doi.org/10.1007/s00442-008-0982-5

Reynolds RJ, Westbrook MJ, Rohde AS, Cridland JM, Fenster CB, Dudash, MR (2009). Pollinator specialization and pollination syndromes of three related North American Silene. Ecology 90(8): 2077-2087. DOI: https://doi.org/10.1890/08-1141.1

Robertson C (1928) Flowers and insects: lists of visitors of four hundred and fifty-three flowers. Charles Robertson, Carlinville, IL DOI: https://doi.org/10.5962/bhl.title.11538

Sahli HF, Conner JK (2006) Characterizing ecological generalization in plant-pollination systems. Oecologia 148:365-372. DOI: https://doi.org/10.1007/s00442-006-0396-1

Sakai AK, Weller SG, Chen M-L, Chou S-Y, Tasanont C (1997) Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution:724-736. DOI: https://doi.org/10.1111/j.1558-5646.1997.tb03656.x

Sanderson MJ, Donoghue MJ (1996) Reconstructing shifts in diversification rates on phylogenetic trees. Trends in Ecology & Evolution 11:15-20. DOI: https://doi.org/10.1016/0169-5347(96)81059-7

Solds DE, Bell CD, Kim S, Soltis PS (2008) Origin and early evolution of angiosperms. Year in Evolutionary Biology 1133: 3-25

Soltis DE, Bell CD, Kim S, Soltis PS (2008) Origin and early evolution of angiosperms. Annals of the New York Academy of Sciences 1133:3-25. DOI: https://doi.org/10.1196/annals.1438.005

Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annual Review of Ecology and Systematics 1:307-326. DOI: https://doi.org/10.1146/annurev.es.01.110170.001515

Straley GB (1977) Systematics of Oenothera sect. Kneffia (Onagraceae). Annals of the Missouri Botanical Garden 64:381-424. DOI: https://doi.org/10.2307/2395256

Tripp EA, Manos PS (2008) Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution 62:1712-1736. DOI: https://doi.org/10.1111/j.1558-5646.2008.00398.x

Vamosi J, Otto S, Barrett S (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology 16:1006-1018. DOI: https://doi.org/10.1046/j.1420-9101.2003.00559.x

Wagner WL, Hoch PC, Raven PH (2007) Revised classification of the Onagraceae. Systematic Botany Monographs 83:1-240.

Wagner W, Krakos K, Hoch PC. (2013) Taxonomic changes in Oenothera sections Gaura and Calylophus (Onagraceae) Phytokeys 28: 61-72. DOI: https://doi.org/10.3897/phytokeys.28.6143

Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043-1060. DOI: https://doi.org/10.2307/2265575

Winfree R (2008) Pollinator-dependent crops: an increasingly risky business. Current Biology 18:R968-R969. DOI: https://doi.org/10.1016/j.cub.2008.09.010