Low seed viability of a rare aster
DOI:
https://doi.org/10.26786/1920-7603(2024)771Keywords:
pollination biology, phenology, seed biology, plant reproduction, endemicAbstract
The reproductive ecology of rare plants is often unknown, yet the persistence of most plant populations depends on successful interactions with pollinators and favourable environmental conditions. Sexual reproduction maintains genetic diversity within plant populations using pollinators to transport pollen grains among plants of the same species and producing seeds. We investigated the reproduction of Yermo xanthocephalus Dorn (Desert yellowhead), a perennial member of Asteraceae endemic to central Wyoming, USA, which grows in only two locations within 8 km of each other. Our objectives were to assess the pollination and seed-set of Y. xanthocephalus. We conducted seed-set experiments in both populations to measure self-pollination and estimate if pollinating insects limited seed production. We used vane traps and pan traps to capture pollinators, and we examined pollen carried on bees. Yermo xanthocephalus can self-pollinate, but seed-set was extremely low. The number of viable seeds produced in flowerheads pollinated by insects did not differ from those produced by capitula hand-pollinated with excess pollen, indicating that pollinators did not limit seed production that year. Pollen from Y. xanthocephalus was carried by nine bee genera, suggesting that no one specific insect pollinates this plant. Only 12% of ovules produced viable seeds in the main population and 0% were viable in the other population, suggesting that something beyond pollinators limited seed-set. We recommend continued research to address what is limiting seed production to advance the knowledge and management of this declining plant species.
References
Abrol DP (2012) Pollination Biology: Biodiversity Conservation and Agricultural Production. https://doi.org/10.1007/978-94-007-1942-2 DOI: https://doi.org/10.1007/978-94-007-1942-2
Agrawal AF (2001) Sexual selection and the maintenance of sexual reproduction. Nature 411:692-695. https://doi.org/10.1038/35079590 DOI: https://doi.org/10.1038/35079590
Aigner PA (2004) Ecological and genetic effects on demographic processes: pollination, clonality and seed production in Dithyrea maritima. Biological Conservation 116:27–34. https://doi.org/10.1016/S0006-3207(03)00170-8 DOI: https://doi.org/10.1016/S0006-3207(03)00170-8
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences 100:9383-9387 https://doi.org/10.1073/pnas.1633576100 DOI: https://doi.org/10.1073/pnas.1633576100
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller 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. https://doi.org/10.1126/science.1127863 DOI: https://doi.org/10.1126/science.1127863
Bizecki Robson D (2010) Reproductive ecology of the western silvery aster Symphyotrichum sericeum in Canada. Endangered Species Research 12:49-55. https://doi.org/10.3354/esr00291 DOI: https://doi.org/10.3354/esr00291
Burmeier S, Jensen K (2008) Is the endangered Apium repens (Jacq.) Lag. rare because of a narrow regeneration niche? Plant Species Biology 23:111-118. https://doi.org/10.1111/j.1442-1984.2008.00212.x DOI: https://doi.org/10.1111/j.1442-1984.2008.00212.x
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL, Robinson GE (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences - PNAS 108: 662-667. https://doi.org/10.1073/pnas.1014743108 DOI: https://doi.org/10.1073/pnas.1014743108
Colling G, Reckinger C, Matthies D (2004) Effects of pollen quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Astraceae). American Journal of Botany 91:1774-1782. https://doi.org/10.3732/ajb.91.11.1774 DOI: https://doi.org/10.3732/ajb.91.11.1774
Delignette-Muller ML, Dutang C (2015) “fitdistrplus: An R Package for Fitting Distributions.” Journal of Statistical Software, 64(4), 1–34. https://doi.org/10.18637/jss.v064.i04 DOI: https://doi.org/10.18637/jss.v064.i04
Diamond AR, Folkerts DR, Boyd RS (2006) Pollination Biology, Seed Dispersal, and Recruitment in Rudbeckia auriculata (Perdue) Kral, a Rare Southeastern Endemic. Castanea 71:226-238. https://doi.org/10.2179/05-20.1 DOI: https://doi.org/10.2179/05-20.1
Dorn RD (1991) Yermo xanthocephalus (Asteraceae: Senecioneae): A new genus and species from Wyoming. Madroño 38(3): 198-201
El-Sharnouby ME, Azab E, Alotaibi SS, Saleh D (2019) Influence of air temperature and soil moisture on growth and chemical composition of geranium plants. Pakistan Journal of Botany. https://doi.org/10.30848/PJB2019-1(20) DOI: https://doi.org/10.30848/PJB2019-1(20)
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24: 217-242. https://doi.org/10.1146/annurev.es.24.110193.001245 DOI: https://doi.org/10.1146/annurev.es.24.110193.001245
ESRI (2011) ArcGIS Desktop: Release 10. Redlands, CA: Environmental Systems Research Institute
Fertig W (1995) Status report on Yermo xanthocephalus in central Wyoming. Unpublished report prepared for the BLM Wyoming State Office and Rawlins District by the Wyoming Natural Diversity Database. Laramie, WY. [online] URL: https://wyndd-reports.s3.us-west-2.amazonaws.com/U95FER09WYUS.pdf
Franz, X. 2021. prais:Prais-Winsten estimator for AR(1) serial correlation. [online] URL: https://github.com/franzmohr/prais
Freeland E Natural Resources Specialist - Invasive Species & Botany, Lander Field Office, Bureau of Land Management Wyoming
Goulson D, Nicholls E (2016) The canary in the coalmine; bee declines as an indicator of environmental health. Science Progress 99:312-326. https://doi.org/10.3184/003685016X14685000479908 DOI: https://doi.org/10.3184/003685016X14685000479908
Handley J, Tronstad LM (2023) Pollinators limit seed production in an early blooming rare plant: Evidence of a mismatch between plant phenology and pollinator emergence. Nordic Journal of Botany. https://doi.org/10.1111/njb.03877 DOI: https://doi.org/10.1111/njb.03877
Heidel B, Handley J, Andersen M (2011) Distribution and habitat requirements of Yermo xanthocephalus (Desert yellowhead), Fremont County, Wyoming. Report prepared for the USDI Bureau of Land Management - Wyoming State Office by the Wyoming Natural Diversity Database - University of Wyoming, Laramie, WY. [online] URL: https://wyndd-reports.s3.us-west-2.amazonaws.com/U11HEI05WYUS.pdf
Jabis MD, Ayers TJ, Allan GJ (2011) Pollinator-mediated gene flow fosters genetic variability in a narrow alpine endemic, Abronia alpina (Nyctaginaceae). American Journal of Botany 98:1583-1594. https://doi.org/10.3732/ajb.1000515 DOI: https://doi.org/10.3732/ajb.1000515
Jones GD (2014) Pollen analyses for pollination research, acetolysis. Journal of Pollination Ecology 13:203-217. https://doi.org/10.26786/1920-7603(2014)19 DOI: https://doi.org/10.26786/1920-7603(2014)19
Kempel A, Bornand CN, Gygax A, Juillerat P, Jutzi M, Sager L, Bäumler B, Eggenberg S, Fischer M (2020) Nationwide revisitation reveals thousands of local extinctions across the ranges of 713 threatened and rare plant species. Conservation Letters 13: e12749. https://doi.org/10.1111/conl.12749 DOI: https://doi.org/10.1111/conl.12749
Larson DL, Larson JL, Buhl DA (2018) Conserving all the pollinators: variation in probability of pollen transport among insect taxa. Natural Areas Journal 38:393-401. https://doi.org/10.3375/043.038.0508 DOI: https://doi.org/10.3375/043.038.0508
Leitão RP, Zuanon J, Villéger S, Williams SE, Baraloto C, Fortunel C, Mendoça, FP, Mouillot D (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proceedings of the Royal Society B-Biological Sciences 283: 20160084. https://doi.org/10.1098/rspb.2016.0084 DOI: https://doi.org/10.1098/rspb.2016.0084
Lenth RV (2022) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.3. https://CRAN.R-project.org/package=emmeans
Lindenbein W (1965) Tetrazolium testing. Proceedings of the International Seed Testing Association 30:89-97
Masini ACA, Rovere AE, Pirk GI (2016) Germination of Gutierrezia solbrigii and Senecio subulatus, endemic Asteraceae from Argentina. Phyton 85:314-323. https://doi.org/10.32604/phyton.2016.85.314 DOI: https://doi.org/10.32604/phyton.2016.85.314
Miller BP, Symons DR, Barrett MD (2019) Persistence of rare species depends on rare events: demography, fire response and phenology of two plant species endemic to a semiarid Banded Iron Formation range. Australian Journal of Botany 67:268-280. https://doi.org/10.1071/BT18214 DOI: https://doi.org/10.1071/BT18214
Mouillot D, Bellwood DR, Baraloto C, Chave J, Galzin R, Harmelin-Vivien M, Kulbicki M, Lavergne S, Lavorel S, Mouquet N, Paine CET, Renaud J, Thuiller W (2013) Rare Species Support Vulnerable Functions in High-Diversity Ecosystems. PLoS Biology 11:e1001569. https://doi.org/10.1371/journal.pbio.1001569 DOI: https://doi.org/10.1371/journal.pbio.1001569
Nyawade SO, Karanja NN, Gachene CKK, Schulte-Geldermann E, Parker M (2018) Effect of potato hilling on soil temperature, soil moisture distribution and sediment yield on a sloping terrain. Soil and Tillage Research 184: 24-36. https://doi.org/10.1016/j.still.2018.06.008 DOI: https://doi.org/10.1016/j.still.2018.06.008
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x
Overpeck JT, Udall B (2020) Climate change and the aridification of North America. Proceedings of the national academy of sciences 117: 11856-11858 https://doi.org/10.1073/pnas.2006323117 DOI: https://doi.org/10.1073/pnas.2006323117
Pol RG, Pirk GI, Marone L (2010) Grass seed production in the central Monte desert during successive wet and dry years. Plant ecology 208:65-75. https://doi.org/10.1007/s11258-009-9688-y DOI: https://doi.org/10.1007/s11258-009-9688-y
Popic TJ, Wardle GM, Davila YC (2013) Flower-visitor networks only partially predict the function of pollen transport by bees. Australian Ecology 38: 76-86. https://doi.org/10.1111/j.1442-9993.2012.02377.x DOI: https://doi.org/10.1111/j.1442-9993.2012.02377.x
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353. https://doi.org/10.1016/j.tree.2010.01.007 DOI: https://doi.org/10.1016/j.tree.2010.01.007
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. [online] URL: https://www.R-project.org/
Rabinowitz D (1981) Seven forms of rarity, in The Biological Aspects of Rare Plant Conservation, H. Synge, Ed. (Wiley) pp. 205–217
Ramos-Jiliberto R, Moisset de Espanés P, Vázquez DP (2020) Pollinator declines and the stability of plant–pollinator networks. Ecosphere 11:e03069. https://doi.org/10.1002/ecs2.3069 DOI: https://doi.org/10.1002/ecs2.3069
Rasmussen C, Engel MS, Vereecken J (2020) A primer of host-plant specialization in bees. Emerging Topics in Life Sciences 4:7–17. https://doi.org/10.1042/ETLS20190118 DOI: https://doi.org/10.1042/ETLS20190118
Rhodes CJ (2018) Pollinator decline – an ecological calamity in the making? Science Progress. 101:121-160. https://doi.org/10.3184/003685018X15202512854527 DOI: https://doi.org/10.3184/003685018X15202512854527
Rodger JG, Bennett JM, Razanajatovo M, Knight TM, van Kleunen M, Ashman T-L, Steets JA, Hui C, Arceo-Gómez G, Burd M, Burkle LA, Burns JH, Durka W, Freitas L, Kemp JE, Li J, Pauw A, Vamosi JC, Wolowski M, Xia J, Ellis AG (2021) Widespread vulnerability of flowering plant seed production to pollinator declines. Science Advances 7:eabd3524 https://doi.org/10.1126/sciadv.abd3524 DOI: https://doi.org/10.1126/sciadv.abd3524
Scott RW, Scott BJ (2009) Yermo xanthocephalus Dorn - A Research Report. Prepared for Bureau of Land Management. Central Wyoming College Herbarium and Scott Environmental Resources, Inc. in cooperation with Wyoming Natural Diversity Database. Riverton, WY. [online] URL: https://wyndd-reports.s3.us-west-2.amazonaws.com/U09SCO01WYUS.pdf
Tong Z-Y, Wu L-Y, Feng H-H, Zhang M, Armbruster WS, Renner SS, Huang S-Q (2023) New calculations indicate that 90% of flowering plant species are animal-pollinated. National Science Review https://doi.org/10.1093/nsr/nwad219 DOI: https://doi.org/10.1093/nsr/nwad219
Tourbez C, Gómez-Martínez C, González-Estévez MÁ, Lázaro A (2023) Pollen analysis reveals the effects of uncovered interactions, pollen-carrying structures, and pollinator sex on the structure of wild bee–plant networks. Insect Science https://doi.org/ 10.1111/1744-7917.13267 DOI: https://doi.org/10.1111/1744-7917.13267
USDI Bureau of Land Management (2001) Wyoming Bureau of Land Management sensitive species policy and list. Instruction Memorandum no. WY-2001-040. BLM State Office, Cheyenne, WY
USDI Bureau of Land Management (2010) Wyoming Bureau of Land Management sensitive species policy and list. Instruction Memorandum No. WY-2010-027. BLM Wyoming State Office, Cheyenne, WY. [online] URL: https://www.blm.gov/sites/blm.gov/files/docs/2021-01/wy2010-027atch2.pdf
USDI Fish and Wildlife Service (2002) Endangered or Threatened species; Listing the Desert Yellowhead as Threatened. Federal Register 67(50): 11442-11449
Van Houten FB (1964) Tertiary geology of the Beaver Rim area, Fremont and Natrona Counties, Wyoming. Geological Survey Bull. 1164. U.S. Govt. Printing Office. Washington, D.C.
Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant–pollinator interactions. Ecology 85:1251-1257 https://doi.org/10.1890/03-3112 DOI: https://doi.org/10.1890/03-3112
Wagner DL (2020) Insect declines in the Anthropocene. Annual Review of Entomology 65:457-480. https://doi.org/10.1146/annurev-ento-011019-025151 DOI: https://doi.org/10.1146/annurev-ento-011019-025151
Western Regional Climate Center (2022) Jeffrey City, Wyoming (484925). [online] URL: http://wrcc.dri.edu/cgi-bin/cliMAIN.pl?wy4925 and http://wrcc.dri.edu/cgi-bin/cliMAIN.pl?wy7760
Wickham H (2011) The Split-Apply-Combine Strategy for Data Analysis. Journal of Statistical Software 40:1–29. https://doi.org/10.18637/jss.v040.i01 DOI: https://doi.org/10.18637/jss.v040.i01
Willemse MTM (2009) Evolution of plant reproduction: From fusion and dispersal to interaction and communication. Chinese Science Bulletin 54: 390-2403. https://doi.org/10.1007/s11434-009-0323-z DOI: https://doi.org/10.1007/s11434-009-0323-z
Wolf AT, Harrison SP, Hamrick JL (2000) Influence of habitat patchiness on genetic diversity and spatial structure of a serpentine endemic plant. Conservation Biology 14:454-463. https://doi.org/10.1046/j.1523-1739.2000.98499.x DOI: https://doi.org/10.1046/j.1523-1739.2000.98499.x
Xiao Y, Li X, Cao Y, Dong M (2016) The diverse effects of habitat fragmentation on plant–pollinator interactions. Plant Ecology 217: 857-868. https://doi.org/10.1007/s11258-016-0608-7 DOI: https://doi.org/10.1007/s11258-016-0608-7
Xu G, Zhang Y, Zhang S, Ma K (2020) Biodiversity associations of soil fauna and plants depend on plant life form and are accounted for by rare taxa along an elevational gradient. Soil Biology and Biochemistry 140:17640. https://doi.org/10.1016/j.soilbio.2019.107640 DOI: https://doi.org/10.1016/j.soilbio.2019.107640
Young LW, Wilen RW, Bonham‐Smith PC (2004) High temperature stress of Brassica napus during flowering reduces micro‐ and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of experimental botany 55:485-495. https://doi.org/10.1093/jxb/erh038 DOI: https://doi.org/10.1093/jxb/erh038
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Joy Handley, Lusha Tronstad
This work is licensed under a Creative Commons Attribution 4.0 International License.
JPE is an open access journal which means that all content is freely available without charge to the user or his/her institution.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
To assure a broader targeted audience, content will be included into databases (such as EBSCO) and directories (such as DOAJ).