Abstract
In the context of ongoing global changes, long-term demographic monitoring data is crucial to assess the viability of natural populations. Such data is particularly important when large fluctuations in population size obfuscate background demographic trajectories. Here, we report results from the first 5 years of a long-term monitoring of a moonwort (Botrychium, Ophioglossaceae) community in Bic National Park, eastern Canada. Our objectives were to provide a first estimate of the composition, size, and demography of the moonwort colonies and to evaluate the putative influence of meteorological and microenvironmental variables on the density of aboveground sporophytes and sporophyte trait variability. Individuals were identified to the species level and tallied in each colony (n = 16 colonies) for the first 3 years (2019–2021) and then marked, monitored, and measured in permanent sample plots (n = 27 plots) for the last 3 years (2021–2023). Although colonies did not vary in composition (n = 8 Botrychium species), the number of emerged individuals differed yearly. Moonwort abundance, re-emergence, and trophophore height were associated with rainfall during the period of sporophyte emergence. Post-drought recovery occurred readily, which might reflect rapid recruitment or dormancy in Botrychium. Moonwort abundance declined as shrub cover and herbaceous vegetation height increased whereas trophophore size was smaller under closed tree canopy. Our results suggest spring rainfall as the limiting factor in opened habitats, whereas competition for sunlight may be limiting under closed canopy. The sizable and species-rich moonwort community of the Bic National Park provides key insights into Botrychium ecology and community dynamics.
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Data availability
Data available are available in the figshare repository at https://doi.org/https://doi.org/10.6084/m9.figshare.25123019 (Harimanana et al. 2024).
References
Ahlenslager K, Potash L (2007) Conservation Assessment for 13 Species of Moonworts (Botrychium Swartz Subgenus Botrychium). USDA Forest Service Region 6 and USDI Bureau of Land Management, Oregon and Washington. pp 57.
Albertson FW, Weaver JE (1944) Nature and degree of recovery of grassland from the great drought of 1933 to 1940. Ecol Monogr 14(4):393–479. https://doi.org/10.2307/194861
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259(4):660–684. https://doi.org/10.1016/j.foreco.2009.09.001
Anderegg WR, Plavcová L, Anderegg LD, Hacke UG, Berry JA, Field CB (2013) Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob Change Biol 19(4):1188–1196. https://doi.org/10.1111/gcb.12100
Anderson DG, Cariveau D (2003) Botrychium campestre WH Wagner & Farrar (Iowa moonwort): a technical conservation assessment. USDA Forest Service, Rocky Mountain Region, Fort Collins, p 47
Anderson DG, Cariveau D (2004) Botrychium echo WH Wagner (reflected grapefern): A technical conservation assessment. USDA Forest Service, Rocky Mountain Region, Fort Collins, p 58
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.48550/arXiv.1406.5823
Berch SM, Kendrick B (1982) Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74(5):769–776. https://doi.org/10.2307/3792863
Bierhorst DW (1971) Morphology of vascular plants. The MacMillan Company, New York, pp 129–153
Braggins JE (1980) Some studies on the New Zealand species of Botrychium SW. (Ophioglossaceae). New Zeal J Bot 18(3):353–366. https://doi.org/10.1080/0028825X.1980.10427253
Brummitt N, Aletrari E, Syfert MM, Mulligan M (2016) Where are threatened ferns found? Global conservation priorities for pteridophytes. J Syst Evol 54(6):604–616. https://doi.org/10.1111/jse.12224
Cayouette J (2001) Les Botrychyaceae du Québec. Ottawa, pp 12.
Cook BI, Smerdon JE, Seager R, Coats S (2014) Global warming and 21st century drying. Clim Dyn 43:2607–2627. https://doi.org/10.1007/s00382-014-2075-y
Dauphin B, Vieu J, Grant JR (2014) Molecular phylogenetics supports widespread cryptic species in moonworts (Botrychium ss, Ophioglossaceae). Am J Bot 101(1):128–140. https://doi.org/10.3732/ajb.1300154
Dauphin B, Farrar DR, Maccagni A, Grant JR (2017) A worldwide molecular phylogeny provides new insight on cryptic diversity within the moonworts (Botrychium ss, Ophioglossaceae). Syst Bot 42(4):620–639. https://doi.org/10.1600/036364417X696483
de Lafontaine G, Ducharme Martin C (2021) Suivi des botryches (Botrychium spp.) au parc national du Bic (été 2020). Rapport préparé pour la direction du parc national du Bic, Sépaq, Québec, pp 46.
Diggle PK (1997) Extreme preformation in alpine Polygonum viviparum: an architectural and developmental analysis. Am J Bot 84(2):154–169. https://doi.org/10.2307/2446077
Ducharme Martin C, de Lafontaine G (2020) Suivi des botryches (Botrychium spp.) au parc national du Bic (été 2019). Rapport préparé pour la direction du parc national du Bic, Sépaq, Québec, pp 54.
Ducharme Martin C, de Lafontaine G (2022) Suivi des botryches (Botrychium spp.) au parc national du Bic (été 2021) : inventaire général et déploiement d’un protocole de suivi démographique. Rapport préparé pour la direction du parc national du Bic, Sépaq, Québec, pp 25.
Epling C, Lewis H (1952) Increase of the adaptive range of the genus Delphinium. Evolution 6:253–267. https://doi.org/10.2307/2405412
Evers SM, Knight TM, Inouye DW, Miller TE, Salguero-Gómez R, Iler AM, Compagnoni A (2021) Lagged and dormant season climate better predict plant vital rates than climate during the growing season. Glob Change Biol 27(9):1927–1941. https://doi.org/10.1111/gcb.15519
Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68. https://doi.org/10.1007/BF00038687
Farrar DR (2011) Systematics and taxonomy of genus Botrychium. Iowa State University, Ames, p 29
Farrar DR, Johnson CL (2022) Methodologies for soil extraction and conservation analysis of ferns and lycophytes with belowground gametophytes. Appl Plant Sci 10(2):1–8. https://doi.org/10.1002/aps3.11469
Field KJ, Leake JR, Tille S, Allinson KE, Rimington WR, Bidartondo MI et al (2015) From mycoheterotrophy to mutualism: mycorrhizal specificity and functioning in Ophioglossum vulgatum sporophytes. New Phytol 205(4):1492–1502. https://doi.org/10.1111/nph.13263
Forest J, Dionne M (2006) Parc national du Bic : Synthèse des connaissances, Première version. Rapport réalisé pour la Société des établissements de plein air du Québec, Réseau Sépaq, Parc Québec, pp 221.
Fujiwara M, Takada T (2017) Environmental stochasticity. In: John Wiley & Sons, Ltd (ed) eLS. Wiley: New York. https://doi.org/10.1002/9780470015902.a0021220.pub2
Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of scots pine 4 yr after a drought episode. New Phytol 190(3):750–759. https://doi.org/10.1111/j.1469-8137.2010.03628.x
Gilman AV (2004) Botrychium pallidum newly discovered in maine. Am Fern J 94(3):155–156. https://doi.org/10.1640/0002-8444(2004)094[0155:SN]2.0.CO;2
Government of Canada (2023a) Climate data extraction tool: daily climate data. Climate change Canada. https://climate-change.canada.ca/climate-data/#/daily-climate-data
Government of Canada (2023b) Moonworts and quillworts: Waterton Lakes National Park. Parks Canada. https://parks.canada.ca/pn-np/ab/waterton/nature/environment/verdure-green/botryche-lunaire-moonwart
Gremer JR, Venable DL (2014) Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecol Lett 17(3):380–387. https://doi.org/10.1111/ele.12241
Gremer JR, Crone EE, Lesica P (2012) Are dormant plants hedging their bets? demographic consequences of prolonged dormancy in variable environments. Am Nat 179(3):315–327. https://doi.org/10.1086/664459
Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125(2):779–786. https://doi.org/10.1104/pp.125.2.779
Harimanana S, de Lafontaine G (2023) Suivi des botryches (Botrychium et Sceptridium) au parc national du Bic (été 2022): Deuxième année du suivi démographique individuel. Rapport préparé pour la direction du parc national du Bic, Sépaq, Québec, pp 38.
Harimanana S, Ducharme Martin C, de Lafontaine G (2024) Data from: Responses to spring rainfall and shading in moonworts: trait variability and the dynamics of a genus community. figshare. Dataset. https://doi.org/10.6084/m9.figshare.25123019
Hawryzki AR, Allen GA, Antos JA (2011) Prolonged dormancy in the geophyte Allium amplectens on Vancouver Island. Botany 89(11):737–744. https://doi.org/10.1139/b11-057
Inghe O, Tamm CO (1985) Survival and flowering of perennial herbs IV The behaviour of Hepatica nobilis and Sanicula europaea on permanent plots during 1943–1981. Oikos 45:400–420. https://doi.org/10.2307/3565576
Inghe O, Tamm CO (1988) Survival and flowering of perennial herbs. V Patterns of Flowering. Oikos 51:203–219. https://doi.org/10.2307/3565644
Inkscape Project (2020) Inkscape. Retrieved from https://inkscape.org
Johnson-Groh C, St Peter MN (1997) Field surveys for Botrychium gallicomontanum and phenology of Botrychium mormo in Minnesota. Report submitted to the Minnesota Dept. Nat. Resources, St. Paul, MN, pp 7.
Johnson-Groh CL (1998) Population demographics, underground ecology and phenology of Botrychium mormo. In: Berlin NP, Miller J, Borovansky J, Seal US, Byers O (eds) Population and habitat viability assessment workshop for the Goblin Fern (Botrychium mormo): Final Report. CBSG, Apple Valley, MN, pp 103–108
Johnson-Groh CL, Lee JM (2002) Phenology and demography of two species of Botrychium (Ophioglossaceae). Am J Bot 89(10):1624–1633. https://doi.org/10.3732/ajb.89.10.1624
Johnson-Groh CL, Riedel C, Schoessler L, Skogen K (2002) Belowground distribution and abundance of Botrychium gametophytes and juvenile sporophytes. Am Fern J 92(2):80–92. https://doi.org/10.1640/0002-8444(2002)092[0080:BDAAOB]2.0.CO;2
Kelsall N, Hazard C, Leopold DJ (2004) Influence of climate factors on demographic changes in the New York populations of the federally-listed Phyllitis scolopendrium (L.) Newm. var. americana. J Torrey Bot Soc 131:161–168. https://doi.org/10.2307/4126917
Kéry M, Gregg KB, Schaub M (2005) Demographic estimation methods for plants with unobservable life-states. Oikos 108(2):307–320. https://doi.org/10.1111/j.0030-1299.2005.13589.x
Labrecque J, Cayouette J (2006) Exploration et inventaire des sites de Botrychium pallidum et Botrychium « michiganense » du Parc national du Bic (1 et 2 juillet 2006). Rapport préparé pour la direction du Parc national du Bic, Réseau Sépaq, Parc Québec, pp 25.
Labrecque J, Cayouette J (2008) Inventaires et nouvelles observations de botryches rares (Botrychium spp.) au Parc national du Bic (juin 2007). Rapport préparé pour la direction du Parc National du Bic, Réseau Sépaq, Parc Québec, pp 28.
Labrecque J, Cayouette J, Farrar DR (2011) Inventaire, nouvelles observations et dénombrement de botryches rares (Botrychium spp.) au Parc national du Bic incluant le territoire du camp du Cap-à-l’Orignal compte rendu d’une année exceptionnelle (23 au 27 juin 2008). Rapport préparé pour la direction du Parc national du Bic, Réseau Sépaq, Parcs Québec, pp 28.
Larcher W (2003) Water relations. Physiological plant ecology: ecophysiology and stress physiology of functional groups, 4th edn. Springer Science & Business Media, pp 286–296
Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142(6):911–927. https://doi.org/10.1086/285580
Lenth RV (2023) emmeans: Estimated marginal means, aka Least-squares means. R package version 1.8.6. https://CRAN.R-project.org/package=emmean.
Lesica P, Ahlenslager K (1996) Demography and life history of three sympatric species of Botrychium subg. Botrychium in Waterton Lakes National Park, Alberta. Can J Bot 74(4):538–543. https://doi.org/10.1139/b96-068
Lesica P, Crone EE (2007) Causes and consequences of prolonged dormancy for an iteroparous geophyte, Silene spaldingii. J Ecol 95:1360–1369. https://doi.org/10.1111/j.1365-2745.2007.01291.x
Light MH, MacConaill M (2006) Appearance and disappearance of a weedy orchid, Epipactis helleborine. Folia Geobot 41:77–93. https://doi.org/10.1007/BF02805263
Lüdecke D et al (2021) Performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6(60):3139. https://doi.org/10.21105/joss.03139
Maccagni A, Parisod C, Grant JR (2017) Phylogeography of the moonwort fern Botrychium lunaria (Ophioglossaceae) based on chloroplast DNA in the Central-European Mountain System. Alpine Bot 127:185–196. https://doi.org/10.1007/s00035-017-0188-8
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178(4):719–739. https://doi.org/10.1111/j.1469-8137.2008.02436.x
Mesipuu M, Shefferson RP, Kull T (2009) Weather and herbivores influence fertility in the endangered fern Botrychium multifidum (SG Gmel.) Rupr. Plant Ecol 203:23–31. https://doi.org/10.1007/s11258-008-9501-3
Ministère des Ressources naturelles et des Forêts (2023) Guide d’utilisation de la carte interactive Forêt ouverte, Québec, Secteur des forêts, Direction des inventaires forestiers, pp 67.
Montgomery JD (1990) Survivorship and predation changes in five populations of Botrychium dissectum in eastern Pennsylvania. Am Fern F 80(4):173–182. https://doi.org/10.2307/1547206
Muller S (1992) The impact of a drought in spring on the sporulation of Botrychium matricariifolium (Retz) A. Br. in the Bitcherland (Northern Vosges, France). Acta Oecol 13:335–343
Muller S (1993) Population dynamics in Botrychium matricariifolium in Bitcherland (Northern Vosges Mountains, France). Belg J Bot 126:13–19. https://doi.org/10.1023/A:1008988709046
Müller LM, Bahn M (2022) Drought legacies and ecosystem responses to subsequent drought. Glob Change Biol 28(17):5086–5103. https://doi.org/10.1111/gcb.16270
NatureServe (2023) NatureServe Network Biodiversity Location Data accessed through NatureServe Explorer. NatureServe, Arlington, Virginia. Available https://explorer.natureserve.org/. (Accessed: 16th Aug 2023).
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, De Caceres M, Durand S, Beatriz H, Evangelista A, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill MO, Lahti L, McGlinn D, Ouelette MH, Ribero Cunha E, Smith T, Stier A, Ter Braak CJF, Weedon J (2022) vegan : Community Ecology Package. R package version 2.6–4. https://CRAN.R-project.org/package=vegan
Pomerleau R (1987) Parc du Bic, le plan directeur, Québec, Ministère du Loisir, de la Chasse et de la Pêche, Direction de l’Aménagement, Service des plans directeurs, p 199.
Popovich SJ, Johnson CL, Farrar DR (2024) Population persistence of Botrychium (Ophioglossaceae) without production of aboveground plants. Am Fern J 114(1):84–93. https://doi.org/10.1640/0002-8444-114.1.84
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Shefferson RP (2006) Survival costs of adult dormancy and the confounding influence of size in lady’s slipper orchids, genus Cypripedium. Oikos 115(2):253–262. https://doi.org/10.1111/j.2006.0030-1299.15231.x
Shefferson RP, Kull T, Hutchings MJ, Selosse MA, Jacquemyn H, Kellett KM et al (2018) Drivers of vegetative dormancy across herbaceous perennial plant species. Ecol Lett 21(5):724–733. https://doi.org/10.1111/ele.12940
Shorina NI (2001) Population biology of gametophytes in homosporous Polypodiophyta. Russ J Ecol+ 32:164–169. https://doi.org/10.1023/A:1011306010154
Tardif B, Tremblay B, Jolicoeur G, Labrecque J (2016) Les plantes vasculaires en situation précaire au Québec. Centre de données sur le patrimoine naturel du Québec (CDPNQ). Gouvernement du Québec, ministère du Développement durable, de l’Environnement et de la Lutte contre les changements climatiques (MDDELCC), Direction de l’expertise en biodiversité, Québec, pp 420.
Thomas RD, Briley T, Carroll N (1981) Additional collections of Botrychium lunarioides from Texas and Oklahoma and comments on its dormancy. Phytologia 48(3):276–278
Tilman D, El Haddi A (1992) Drought and biodiversity in grasslands. Oecologia 89:257–264. https://doi.org/10.1007/BF00317226
Trugman AT, Detto M, Bartlett MK, Medvigy D, Anderegg WRL, Schwalm C, Schaffer B, Pacala SW (2018) Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol Lett 21(10):1552–1560. https://doi.org/10.1111/ele.13136
Vilonen L, Ross M, Smith MD (2022) What happens after drought ends: synthesizing terms and definitions. New Phytol 235(2):420–431. https://doi.org/10.1111/nph.18137
Vucetich JA, Waite TA, Qvarnemark L, Ibargüen S (2000) Population variability and extinction risk. Conserv Biol 14(6):1704–1714. https://doi.org/10.1111/j.1523-1739.2000.99359.x
Wagner WH Jr, Wagner FS (1983) Genus communities as a systematic tool in the study of New World Botrychium (Ophioglossaceae). Taxon 32(1):51–63. https://doi.org/10.2307/1219850
Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New-York
Williams EW, Waller DM (2015) Tracking morphological change and demographic dynamics in ephemeral Botrychium ss (Ophioglossaceae) populations. J Torrey Bot Soc 142(2):152–165. https://doi.org/10.3159/TORREY-D-14-00036.1
Williams EW, Farrar DR, Henson D (2016) Cryptic speciation in allotetraploids: Lessons from the Botrychium matricariifolium complex. Am J Bot 103(4):740–753. https://doi.org/10.3732/ajb.1500281
Acknowledgements
We thank A. Atikessé, M. Couture, V. Laflamme, S. Larose, L. Pothier-Guerra, R. Turquin, M. Deslauriers. E. Pelletier, R. Claudepierre, S. Ahmad, J. Cigana, E. Cliché, L. Dumont, F. Bordeleau, A. Langlois, J. Fisette, L. Nondier, G. Rincon Pinilla, D. Ruffio, and G. Demeule for their help with data collection in the field over the last 5 years. We are grateful to Mélanie Sabourin (Société des établissements de plein air du Québec) for initiating and maintaining the monitoring of the moonwort community in Bic National Park.
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This work was supported by Natural Sciences and Engineering Research Council of Canada (Undergraduate Student Research Awards to SH and CDM; Discovery Grant program RGPIN-2018-06586 to GdL), the Canada Research Chairs Program (Canada Research Chair in Integrative Biology of the Northern Flora CRC-2017-00112; CRC-2022-00518 to GdL). GdL has received research support from the Société des établissements de plein air du Québec. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
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All authors contributed to the study conception and design. Material preparation, data collection, and analyses were performed by SH and CDM with the help of GdL. The first draft of the manuscript was written by SH and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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GdL has received research funding from the Société des établissements de plein air du Québec, a state-owned enterprise that manages Québec’s parks and wildlife reserves.
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Harimanana, S., Ducharme Martin, C. & de Lafontaine, G. Responses to spring rainfall and shading in moonworts: trait variability and the dynamics of a genus community. Plant Ecol (2024). https://doi.org/10.1007/s11258-024-01428-3
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DOI: https://doi.org/10.1007/s11258-024-01428-3