Assessing Pollinator Assembly And Efficacy Across Species Ranges In The Genus Triodanis (Campanulaceae)




self fertilization, dimorphic cleistogamy, native pollinators, Syrphidae, plant mating system


Plant-insect interactions are a key topic in evolutionary ecology, especially in the face of anthropogenic changes which threaten to disrupt these mutualisms. An in-depth pollinator survey for species in the genus Triodanis is performed here for the first time, with sampling covering four species and spanning a large portion of their geographic ranges (i.e., four U.S. states). All species in the genus exhibit dimorphic cleistogamy with variability in allocation to open (chasmogamous) flowers among populations and taxa. The genus Triodanis, therefore, provides an opportunity for understanding possible associations between pollinator assemblies and variation in species, breeding system, and geography. To assess these relationships, we sampled four species or subspecies of Triodanis at eight field sites in four states. Sampling encompassed a broad area across the Midwestern U.S. and Texas, and across a gradient of anthropogenically disturbed habitats. We found that for species of Triodanis: 1) small bee and fly generalist pollinators showed some floral constancy during feeding bouts but did not differentiate between species, 2) pollinator community was less diverse and abundant in highly degraded habitats, 3) while allocation to open flowers varied among species and populations, we found no association between breeding system (or species) on pollinator identity or abundance. This study represents the first in-depth survey of pollinator visitors of Triodanis and serves as foundational knowledge about the natural history of this group, provides resolution for members of Campanulaceae exhibiting floral traits of generalist hosts, and important documentation of plant-insect interactions in an era of ongoing anthropogenic changes.


Ansaldi BH, Franks SJ, Weber JJ (2018) The influence of environmental factors on breeding system allocation at large spatial scales. AoB PLANTS 10 DOI:

Ansaldi BH, Weber JJ, Goodwillie C, Franks SJ (2019) Low levels of inbreeding depression and enhanced fitness in cleistogamous progeny in the annual plant Triodanis perfoliata. Botany 97:405-415. DOI:

Basteri G, Benvenuti S (2010) Wildflowers Pollinators- Attractivity in the Urban Ecosystem. Acta Horticulturae:585-590. DOI:

Beattie AJ. 1974. Floral Evolution in Viola. Annals of the Missouri Botanical Garden. 61(3):781. doi:10.2307/2395029. DOI:

Bennett JM, Steets JA, Burns JH, Burkle LA, Vamosi JC, Wolowski M, Arceo-Gómez G, Burd M, Durka W, Ellis AG, Freitas L, Li J, Rodger JG, Ştefan V, Xia J, Knight TM, Ashman T-L (2020) Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene. Nature Communications 11:3999. DOI:

Berg CS, Brown JL, Weber JJ (2019) An examination of climate‐driven flowering‐time shifts at large spatial scales over 153 years in a common weedy annual. American Journal of Botany 106:1435-1443. DOI:

Berg C, Burr N, Weber J (2023) Phenological advancement in the North American wildflower genus Triodanis (Campanulaceae). Accepted: Rhodora

Blionis GJ, Vokou D (2001) Pollination ecology of Campanula species on Mt Olympos, Greece. Ecography 24:287-297. DOI:

Bradley TR (1975) Hybridization Between Triodanis perfoliate and Triodanis biflora (Campanulaceae). Brittonia 27:110. DOI:

Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant-insect mutualisms. New Phytologist 172:412-428. DOI:

Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (Purple Loosestrife) and a native congener. Ecology 83:2328-2336.[2328:CFPBAI]2.0.CO;2 DOI:[2328:CFPBAI]2.0.CO;2

Burkle LA, Alarcon R (2011) The future of plant-pollinator diversity: Understanding interaction networks across time, space, and global change. American Journal of Botany 98:528-538. DOI:

Camilo GR, Muñiz PA, Arduser MS, Spevak EM (2017) A Checklist of the Bees (Hymenoptera: Apoidea) of St. Louis, Missouri, USA. Journal of the Kansas Entomological Society 90:175-188. DOI:

Carril OM, Wilson JS (2021) Common Bees of Eastern North America. Princeton University Press. DOI:

Ceratina -- identification guide -- Discover Life [online] URL: (accessed 27 February 2023).

Chisausky J, Soley N, Kassim L, Bryan C, Miranda GF, Gage K, Sipes S (2020) Syrphidae of Southern Illinois: Diversity, floral associations, and preliminary assessment of their efficacy as pollinators. Biodiversity Data Journal 8:e57331. DOI:

Crowl AA, Miles NW, Visger CJ, Hansen K, Ayers T, Haberle R, Cellinese N (2016) A global perspective on Campanulaceae: Biogeographic, genomic, and floral evolution. American Journal of Botany. 103(2):233-245. doi:10.3732/ajb.1500450. DOI:

Devaux C, Lepers C, Porcher E (2014) Constraints imposed by pollinator behaviour on the ecology and evolution of plant mating systems. Journal of Evolutionary Biology 27:1413-1430. DOI:

Dewitz, J (2019) U.S. Geological Survey. National Land Cover Database (NLCD) 2019 Products (ver. 2.0, June 2021). U.S. Geological Survey data release, 2021.

Diggs GM, Lipscomb BL, O'Kennon RJ, O'Kennon B, Austin College (Sherman Tex). C for ES, Project ITF (1999) Shinners & Mahler's Illustrated Flora of North Central Texas. Botanical Research Institute of Texas.

Fernald ML (1946) Identifications and reidentifications of North American plants. Contributions from the Gray Herbarium of Harvard University no. 154-164 1945-46:137-216. DOI:

Gara B, Muenchow G (1990) Chasmogamy/Cleistogamy in Triodanis perfoliata (Campanulaceae): Some CH/CL comparisons in fitness parameters. American Journal of Botany 77:1-6. DOI:

Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. Journal of Animal Ecology 71:757-764. DOI:

Gleason HA, Cronquist A Manual of Vascular Plants of Northeastern United States and Adjacent Canada: Second Edition.

Gómez JM, Abdelaziz M, Lorite J, Jesús Muñoz-Pajares A, Perfectti F (2010) Changes in pollinator fauna cause spatial variation in pollen limitation: Pollinator assemblage and pollen limitation. Journal of Ecology 98:1243-1252. DOI:

Goodwillie C, Patel HR, Dvorak DM (2018) Does stigma curvature promote delayed selfing? An experimental investigation in Triodanis perfoliata (Campanulaceae) Ren Z-X (ed). Plant Biology 20:199-204. DOI:

Goodwillie C, Sargent RD, Eckert CG, Elle E, Geber MA, Johnston MO, Kalisz S, Moeller DA, Ree RH, Vallejo‐Marin M, Winn AA (2010) Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phytologist 185:311-321. DOI:

Goodwillie C, Stewart E (2013) Cleistogamy and Hybridization in Two Subspecies of Triodanis perfoliata (Campanulaceae). Rhodora 115:42-60. DOI:

Kastinger C, Weber A (2001) Bee-flies (Bombylius spp., Bombyliidae, Diptera) and the pollination of flowers. Flora 196:3-25. DOI:

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen Limitation of Plant Reproduction: Pattern and Process. Annual Review of Ecology, Evolution, and Systematics 36:467-497. DOI:

Kobayashi S, Inoue K, Kato M (1999) Mechanism of selection favoring a wide tubular corolla in Campanula punctata. Evolution 53:752-757. DOI:

Koski MH, Ison JL, Padilla A, Pham AQ, Galloway LF (2018) Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant-pollinator mutualism. Proceedings of the Royal Society B: Biological Sciences 285:20180635. DOI:

Koski MH, Layman NC, Prior CJ, Busch JW, Galloway LF (2019) Selfing ability and drift load evolve with range expansion. Evolution Letters 3:500-512. DOI:

Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC (2016) The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytologist 210:1430-1442. DOI:

Lau JA, Galloway LF (2004) Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae). Oecologia 141:577-583. DOI:

Leibman L, Rowe A, Koski MH, Galloway LF (2018) Populations with greater flexibility in floral traits modify mating system in response to the pollinator environment Schleuning M (ed). Functional Ecology 32:1457-1466. DOI:

MacInnis G, Normandin E, Ziter CD (2023) Decline in wild bee species richness associated with honey bee ( Apis mellifera L.) abundance in an urban ecosystem. PeerJ 11:e14699. DOI:

McVaugh R (1948) Generic Status of Triodanis and Specularia. Rhodora Vol. 50, No. 590 (February, 1948), pp. 38-49:38-49. DOI:

Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecology Letters 10:710-717. DOI:

Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant-pollinator interactions. Annals of Botany 103:1355-1363. DOI:

Nyman Y (1993) The pollen-collecting hairs of Campanula (Campanulaceae). II. Function and adaptive significance in relation to pollination. American Journal of Botany 80:1437-1443. DOI:

Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Solymos P, Stevens MHH, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, Caceres MD, Durand S, Evangelista HBA, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill MO, Lahti L, McGlinn D, Ouellette M-H, Cunha ER, Smith T, Stier A, Braak CJFT, Weedon J (2022) vegan: Community Ecology Package. [online] URL: (accessed 20 March 2023).

Olesen JM, Alarcón M, Ehlers BK, Aldasoro JJ, Roquet C (2012) Pollination, biogeography, and phylogeny of oceanic island bellflowers (Campanulaceae). Perspectives in Plant Ecology, Evolution and Systematics 14:169-182. DOI:

Portman ZM, Arduser M, Lane IG, Cariveau DP (2022) A review of the Augochloropsis (Hymenoptera, Halictidae) and keys to the shiny green Halictinae of the midwestern United States. ZooKeys 1130:103-152. DOI:

R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

Robertson C (1928) Flowers and insects; lists of visitors of four hundred and fifty-three flowers. Carlinville, Ill., n.p. [online] URL: (accessed 27 January 2023).

Roquet C, Sáez L, José Aldasoro J, Susanna A, Luisa Alarcón M, Garcia-Jacas N (2008) Natural delineation, molecular phylogeny and floral evolution in Campanula. Systematic Botany 33:203-217. DOI:

Sicard A, Lenhard M (2011) The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Annals of Botany 107:1433-1443. DOI:

Tepedino VJ, Sipes SD, Griswold TL (1999) The reproductive biology and effective pollinators of the endangered beard tongue Penstemon penlandii (Scrophulariaceae). Plant Systematics and Evolution 219:39-54. DOI:

Tooker JF, Hauser M, Hanks LM (2006) Floral Host Plants of Syrphidae and Tachinidae (Diptera) of Central Illinois. Annals of the Entomological Society of America 99:96-112.[0096:FHPOSA]2.0.CO;2 DOI:[0096:FHPOSA]2.0.CO;2

Trent JA (1940) Flowering behavior of Specularia perfoliata in relation to light intensity and light duration. Transactions of the Kansas Academy of Science (1903-) 43:199. DOI:

Trent JA (1942) Studies pertaining to the life history of Specularia perfoliata (l.).a.dc., with special reference to cleistogamy. Transactions of the Kansas Academy of Science (1903-) 45:152. DOI:

Triodanis perfoliata subsp. biflora (Ruiz & Pav.) Lammers URL: (accessed 20 March 2023).

Weakley A (2020) Weakley, A.S. 2020. Flora of the southeastern United States. University of North Carolina Herbarium, North Carolina Botanical Garden, Chapel Hill, NC. Pdf downloadable at

Weinman LR, Ress T, Gardner J, Winfree R (2023) Individual bee foragers are less‐efficient transporters of pollen for plants from which they collect the most pollen in their scopae. American Journal of Botany 110:e16178. DOI:

Wendling BM, Galbreath KE, DeChaine EG (2011) Resolving the Evolutionary History of Campanula (Campanulaceae) in Western North America. Knapp M, editor. PLoS ONE. 6(9):e23559. DOI:

Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton, N.J. DOI:

Willmer PG, Cunnold H, Ballantyne G (2017) Insights from measuring pollen deposition: quantifying the pre-eminence of bees as flower visitors and effective pollinators. Arthropod-Plant Interactions 11:411-425. DOI:

Yeo PF (2012) Secondary pollen presentation: form, function and evolution. Springer Vienna.

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How to Cite

Tillotson-Chavez, K., Lukavsky, S., & Weber, J. (2024). Assessing Pollinator Assembly And Efficacy Across Species Ranges In The Genus Triodanis (Campanulaceae). Journal of Pollination Ecology, 35, 47–60.



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