Abstract
Agalinis is a diverse and wide-ranging genus within the Orobanchaceae. Species may be either widespread or restricted in range. Natural populations tend to be small and isolated being distributed across natural grassland or open habitats that are frequently fragmented due to habitat loss. We ask whether patterns of distribution and limited occurrence may be related to visiting bee diversity. We conducted a review of the bee taxa recorded visiting flowers of the genus Agalinis involving 15 published surveys plus our own field observations. We assessed the association of visiting bee diversity on flower size, geographical distribution, regional distribution, and conservation status of 14 species of Agalinis. From a total of 160 floral records, we found 5 families, 18 genera and 58 bee taxa have been documented visiting flowers of Agalinis. Halictidae (43.1%) and Apidae (29.3%) constituted the largest proportion of bees. The number of bee taxa recorded for a species of Agalinis showed a significant positive relationship with geographic range across the United States and Canada. However, no differences in bee diversity at the level of family were noted for flower size, regional distribution or conservation status. Bee diversity patterns recorded to date suggest a generalized pollination system not associated with the limited distribution or small population sizes of many Agalinis species. Nevertheless, previous studies indicate a level of specialization with respect to flower form and bee foraging behavior. The gibbous to ventricose corolla, combined with dimorphic stamens bearing filament trichomes facilitate inverted bee foraging for pollen gathering.
Similar content being viewed by others
References
Addinsoft (2022) XLSTAT statistical and data analysis solution. XLSTAT, New York
Adler LS (2003) Host species affects herbivory, pollination and reproduction in experiments with parasitic Castilleja. Ecology 84:2083–2091
Arduser M (2010) Bees (Hymenoptera: Apoidea) of the Kitty Todd Preserve, Lucas County, Ohio. Gt Lakes Entomol 43:1–24
Bartholomew CS, Prowell D, Griswol T (2006) An annotated checklist of bees (Hymenoptera: Apoidea) in longleaf pine savannas of southern Louisiana and Mississippi. J Kans Entomol Soc 79:184–198
Bernhardt CE, Mitchell RJ, Michaels HJ (2008) Effects of population size and density on pollinator visitation and pollinator behavior, and pollen tube abundance in Lupinus perennis. Int J Plant Sci 169:944–953
Campbell LG, Husband BC (2007) Small populations are mate-poor but pollinator-rich in a rare, self-compatible plant, Hymenoxys herbacea (Asteraceae). New Phytol 174:915–925
Canne-Hilliker JM (1988) Agalinis (Scrophulariaceae) in Peru and Bolivia. Brittonia 40:433–440
Canne-Hilliker JM, Hays JF (2019) Agalinis Rafinesque, New Fl. 2: 16. 1837, name conserved. In: Flora of North America Editorial Committee (ed) Floral of North America, vol 17. Oxford University Press, New York
Colwell, RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. Persistent URL <purl.oclc.org/estimates>
Deyrup M, Edirisinghe J, Norden B (2002) The diversity of floral hosts of bees at the Archbold biological Station, Florida (Hymenoptera: Apoidea). Insecta Mundi 16:87–120
Dieringer G (1988) Intrapopulational variation in the pollination biology of Agalinis strictifolia (Benth.) Penn. (Scrophulariaceae). The University of Texas at Austin, Austin
Dieringer G (1991) Variation in flowering time and reproductive success of Agalinis strictifolia (Scrophulariaceae). Am J Bot 78:497–503
Dieringer G (1992) Pollinator effectiveness and seed set in populations of Agalinis strictifolia (Scrophulariaceae). Am J Bot 79:1018–1023
Dieringer G (1999) Reproductive biology of Agalinis skinneriana (Scrophulariaceae), a threatened species. J Torr Bot Soc 126:289–295
Dieringer G, Cabrera RL (2022) Stamen dimorphism, bee visitation and pollen removal in three species of Agalinis (Orobanchaceae). Botany 100(4):377–386. https://doi.org/10.1139/cjb-2021-0110
Discover Life (2021) Served by Sam Houston State University, Texas. https://Discoverlife.org. Accessed 15 Feb 2021
Duncan TM, Rausher MD (2013) Evolution of the selfing syndrome in Ipomea. Front Plant Sci 4:301. https://doi.org/10.3389/fpls.2013.00301
Environment and Climate Change Canada (2017) Recovery strategy for the Gattinger’s agalinis (Agalinis gattingeri) in Canada [Proposed]. Environment and Climate Change Canada, Ottawa
Foster C (2008) Rare plant surveys and stewardship activities by the Manitoba conservation data centre, 2007. MS report 08-01. Manitoba Conservation Data Centre, Winnipeg
Francisco-Gutiérrez A, Castillo-Campos G, Garcia-Franco JG (2018) A new rare species of Agalinis (Orobanchaceae) from the coast of Veracruz, México. Phytotaxa 349:265–272. https://doi.org/10.11646/phytotaxa.349.3.7
Galen G, Newport MEA (1987) Bumblebee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia 74:20–23
Gerner EE, Sargent RD (2022) Local plant richness predicts bee abundance and diversity in study of urban residential yards. Basic Appl Ecol 58:64–73
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia. https://doi.org/10.1007/s00442-007-0752-9
Hays JF (2010) Agalinis flexicaulis sp. nov. (Orobanchaceae: Lamiales), a new species from northeast Florida. J Bot Res Inst Tex 4:1–6
Marvier MA, Smith DL (1997) Conservation implications of host use for rare parasitic plants. Conserv Biol 11:839–848
Matthies D (2017) Interactions between a root hemiparasite and 27 different hosts: growth, biomass allocation and plant architecture. Zur Open Repos Arch Univ Zur. https://doi.org/10.5167/uzh/-131707
Mitchell TB (1960) Bees of the eastern United States. N C Agric Exp Stn Tech Bull 141:1–583
Molano-Flores B, Feist MA, Whelan CJ (2003) Seed germination, seedling survivorship and host preference of Agalinis auriculata (Michx.) Blake (Orobanchaceae), an Illinois, USA, threatened species. Nat Area J 23:152–157
Mulvaney CR, Molano-Flores B, Whitman DW (2004) The reproductive biology of Agalinis auriculata (Michx.) Raf. (Orobanchaceae), a threatened North American prairie inhabitant. Int J Plant Sci 165:605–614. https://doi.org/10.1086/386564
Musselman LJ, Mann Jr WF (1978) Root parasites of southern forests. Southern Forest Experiment Station, Southeastern Area, State and Private Forestry, Forestry Service, U.S. Department of Agriculture, General Technical Report SO-20
NatureServe (2021) NatureServe explorer [web application]. NatureServe, Arlington
Neel MC (2002) Conservation implications of the reproductive ecology of Agalinis acuta (Scrophulariaceae). Am J Bot 89:972–980
Neel MC, Cummings MP (2004) Section-level relationships of North American Agalinis (Orobanchaceae) based on DNA sequence analysis of three chloroplast gene regions. BMC Evol Biol 4:15. https://doi.org/10.1186/1471-2148-4-15
Neff JL, Simpson BB (1988) Vibratile pollen-harvesting by Megachile mendica Cresson (Hymenoptera: Megachilidae). J Kans Entomol Soc 61:242–244
Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:406–415
Owens BE, Allain L, Van Gorder EC, Bossart JL, Carlton CE (2018) The bees (Hymenoptera: Apoidea) of Louisiana: an updated, annotated checklist. Proc Entomol Soc Wash 120:272–307
Pennell FW (1929) Agalinis and allies in North America – II. Proc Acad Nat Sci Phil 81:111–249
Pettengill JB, Neel MC (2008) Phylogenetic patterns and conservation among North American members of the genus Agalinis (Orobanchaceae). BMC Evol Biol 8:264. https://doi.org/10.1186/1471-2148-8-264
Pettengill JB, Neel MC (2011) A sequential approach using genetic and morphological analyses to test species status: the case of United States federally endangered Agalinis acuta (Orobanchaceae). Am J Bot 98:859–871. https://doi.org/10.3732/ajb.1000267
Robertson C (1892) Flowers and insects, Asclepiadaceae to Scrophulariaceae. Trans St Louis Acad Sci 5:569–598
Roof SM, DeBano S, Rowland MM, Burrows S (2020) Associations between blooming plants and their bee visitors in a riparian ecosystem in eastern Oregon. Northwest Sci 92(2):119–135
Rubiales D, Heide-Jørgensen HS (2011) Parasitic plants. Encyclopedia of life sciences. Wiley, Chichester
Sánchez-Castro D, Armbruster G, Willi Y (2022) Reduced pollinator service in small populations of Arabidopsis lyrate at is southern range limit. Oecologia 200:107–117
Sandner TM, Matthies D (2017) Interactions of inbreeding and stress by poor host quality in a root hemiparasite. Ann Bot 119:143–150
Sellers E, McCarthy D (2015) Distribution and floral hosts of Anthophorula micheneri (Timberlake, 1947) and Hylaeus sparsus (Cresson, 1869), (Insecta: Hymenoptera: Apoidea: Anthophila), with new state records in Giles and Loudoun counties, Virginia, eastern USA. Check List 11(3):1665. https://doi.org/10.15560/11.3.1665
Simpson DT, Weinman LR, Genung MA, Roswell M, MacLeod M, Winfree R (2022) Many bee species, including rare species, are important for function of entire plant-pollinator networks. Pro R Soc B 289:20212689. https://doi.org/10.1098/rspd.2021.2689
Slagle MW, Hendrix SD (2009) Reproduction of Amorpha canescens (Fabaceae) and diversity of its bee community in a fragmented landscape. Oecologia 161:813–823
Sokal RR, Rohlf FJ (2011) Biometry, 4th edn. W. H Freeman and Company, New York
Souza VC, Elias SI, Giulletti AM (2001) Notes on Agalinis (Scrophulariaceae) from Brazil. Novon 11:484–488
Souza VC, Gontijo FD, Dornas TT, Colletta GD, Scatigna AV, Moura MM (2022) Agalinis marianae (Orobanchaceae), a new endangered species endemic to the Quadrilátero Ferrífero, Minas Gerais, Brazil. Acta Bot Brasilica 36:e20210318. https://doi.org/10.1590/0102-3306-ABB-2021-0318
Steffens JC, Lynn DG, Riopel JL (1986) An haustoria inducer for the root parasite Agalinis purpurea. Phytochemistry 25:2291–2298
Theodorou P, Herbst SC, Kahnt B, Landaverde-González BLM, Osterman J, Paxton RJ (2020) Urban fragmentation leads to lower floral diversity, with knock-on impacts on bee biodiversity. Sci Rep 10:21756. https://doi.org/10.1038/s41598-020-78736-x
Voss EG (1996) Michigan Flora, part III, Dicots (Pyrolaceae-Compositae). Rhodora 98:460
Wilhelm G, Rericha L (2017) Flora of the Chicago region: a floristic and ecological synthesis. Indiana Academy of Science, Indianapolis
Wilmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton
Acknowledgements
The study was funded, in part, by the following institutions: The University of Texas at Austin, The University of Texas at Brownsville, Western Illinois University, and Northwest Missouri State University. Permission to conduct field studies was granted by: Lower Rio Grande National Wildlife Refuge, TX; Illinois Department of Natural Resources, IL; Mr. Larry Maher of Stanberry, MO; Mr. Doug Keever of Maryville, MO; Missouri Department of Conservation, MO; and Loess Bluffs National Wildlife Refuge, MO. We would like to thank Ms. Michelle Allen for laboratory assistance. We are especially grateful to Dr. John Neff of the Central Texas Melittological Institute, Austin, TX for identification of bee specimens. We also thank anonymous reviewers for critical comments on earlier drafts of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose. The authors have no competing interests to declare that are relevant to the content of this article. The authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article.
Additional information
Handling Editor: Isabel Alves dos Santos.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dieringer, G., Cabrera Rodriguez, L. Bee diversity and flower visitation to the genus Agalinis (Orobanchaceae) in North America. Arthropod-Plant Interactions 18, 141–148 (2024). https://doi.org/10.1007/s11829-023-09999-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-023-09999-0