What is Suksdorf’s hawthorn? Revision of the Western North American 20-stamen black-fruited hawthorns (Crataegus series Douglasianae, Rosaceae subtribe Malinae)
DOI:
https://doi.org/10.17348/jbrit.v17.i1.1292Keywords:
Apomixis, Biogeography, Classification, Microsatellites, Morphology, Pollen, Polyploidy, Species Concepts, TypificationAbstract
An agamic complex of 20- and 10-stamen, black-fruited hawthorns (Crataegus subg. Sanguineae, sect. Douglasianae) occurs in western North America, with a 10-stamen taxon disjunct in the upper Great Lakes basin. Here, we recircumscribe the 20-stamen taxa at the core of this complex (C. ser. Douglasianae). This is needed in order to distinguish between a presumptively ancestral diploid and its allo- and autopolyploid derivatives, all differing in breeding system, distribution, morphology, and pattern of genetic variation. The earliest name for these 20-stamen taxa, Crataegus gaylussacia A. Heller, was given to distinctive plants of Marin and Sonoma counties in California that have recently been shown to be autotriploids. In Flora North America, however, this name was applied to all 20-stamen, black-fruited hawthorns. We recircumscribe C. gaylussacia, and also recircumscribe and typify a slightly younger name, C. suksdorfii (Sarg.) Kruschke, with a specimen from southern Washington with the diminished pollen fertility found in allopolyploid, apomictic black-fruited hawthorns occurring east of the Cascades, from northern California north to southernmost Alaska. Finally, we recognize the diploid, self-incompatible, sexual black-fruited hawthorns found west of the Cascades from northern California to southwestern Washington as Crataegus rhodamae-loveae sp. nov. Together with the 10-stamen, black-fruited hawthorns in predominantly tetraploid, apomictic, and self-fertile C. douglasii Lindl. and its segregates (discussed in detail in a companion paper), these species are linked by whole genome duplications associated in most cases with hybridization, with members of red-fruited C. subg. Americanae, and with each other. We suggest that this complex provides a model for understanding other such groups of Crataegus species that are related by whole genome duplications resulting from the fertilization of unreduced gametes (facilitated by but not necessarily dependent on occurrence of gametophytic apomixis), often together with hybridization. We note that an earlier effort at DNA barcoding these and other hawthorn species that provided limited support for our taxonomic decisions here also demonstrated some limited utility of the original plant DNA barcoding loci in groups like Crataegus. The taxonomic decisions we advocate will warrant consideration when other groups of hawthorns are revised in the light of data like those employed here.
References
ABRÀMOFF, M.D., P.J. MAGALHAES, & S.J. RAM. 2004. Image processing with ImageJ. Biophotonics Int. 11:36–42.
ALBAROUKI, E. & A. PETERSON. 2007. Molecular and morphological characterization of Crataegus L. species (Rosaceae) in southern Syria. Bot. J. Linnean Soc. 153:255–263.
ALEXANDER, M.P. 1969. Differential staining of aborted and non-aborted pollen. Stain Technol. 44:117–122.
ANDERSON, M.J. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. 10.1111/j.1541-0420.2005.00440.x
ANONYMOUS. 2010. Level III and IV ecoregions of Washington. U.S. Geological Survey, Washington, DC, U.S.A.
BERLYN, G.P. & J.P. MIKSCHE. 1976. Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, U.S.A.
BORGES, L.M., V.C. REIS, & R. IZBICKI. 2020. Schrödinger's phenotypes: Herbarium specimens show two-dimensional images are both good and (not so) bad sources of morphological data. Methods Ecol. Evol. 11:1296–1308. https://doi.org/10.1111/2041-210X.13450
BREWER, W.H. & W. WATSON. 1880. Botany Vol. I Polypetalae. In: Whitney JD, ed. Publications. 2nd (Revised) ed. Geological Survey of California, Cambridge, MA, U.S.A.
BROWN, H.B. 1910. The genus Crataegus with some theories of the origin of its species. Bull. Torrey Bot. Club 37:251–260.
BRUNSFELD, S.J. & F.D. JOHNSON. 1990. Cytological, morphological, ecological and phenological support for specific status of Crataegus suksdorfii (Sarg.) Kruschke. Madroño 37:274–282.
BURGESS, M.B., K.R. CUSHMAN, E.T. DOUCETTE, C.T. FRYE, & C.S. CAMPBELL. 2015. Understanding diploid diversity: A first step in unraveling polyploid, apomictic complexity in Amelanchier. Amer. J. Bot. 102:2041–2057. doi:10.3732/ajb.1500330
BURGESS, M.B., K.R. CUSHMAN, E.T. DOUCETTE, N. TALENT, C.T. FRYE, & C.S. CAMPBELL. 2014. Effects of apomixis and polyploidy on diversification and geographic distribution in Amelanchier (Rosaceae). Amer. J. Bot. 101:1375–1387. 10.3732/ajb.1400113
CAMP, W.H. 1942. The Crataegus problem. Castanea 7:51–55.
CANADENSYS. 2020. Crataegus species. Acadia University, Université de Montréal Biodiversity Centre, University of Toronto Mississauga, University of British Columbia. Available at http://data.canadensys.net/explorer (accessed 21 Mar 2012).
CHRISTENSEN, K.I. 1992. Revision of Crataegus Sect. Crataegus and Nothosect. Crataeguineae (Rosaceae-Maloideae) in the Old World. Syst. Bot. Monogr. 35:1–199.
CHRISTENSEN, K.I, M. ZARREI, M. KUZMINA, N. TALENT, C. LIN, & T.A. DICKINSON. 2014. Crataegus ×ninae-celottiae and C. ×cogswellii (Rosaceae, Maleae), two spontaneously formed intersectional nothospecies. Phytokeys 36:1–26. 10.3897/phytokeys.36.6784
CONSIDINE, M.J., Y. WAN, M.F. D'ANTUONO, Q. ZHOU, M. HAN, H. GAO, & M. WANG. 2012. Molecular genetic features of polyploidization and aneuploidization reveal unique patterns for genome duplication in diploid Malus. PloS ONE 7:e29449. 10.1371/journal.pone.0029449
COUGHLAN, J., S.H. SHERY HAN, S. STEFANOVI?, & T.A. DICKINSON. 2017a. Data from: Widespread generalist clones are associated with range and niche expansion in allopolyploids of Pacific Northwest Hawthorns (Crataegus L.). Dryad Data Repository.
COUGHLAN, J.M. 2012. Mechanisms for range size and distribution variation in the polyploid complex black-fruited hawthorn (Crataegus series Douglasianae): Biogeographic implications for the maintenance of cytotype diversity. M.Sc. University of Toronto, Canada.
COUGHLAN, J.M., S. HAN, S. STEFANOVI?, & T.A. DICKINSON. 2017b. Widespread generalist clones are associated with range and niche expansion in allopolyploids of Pacific Northwest Hawthorns (Crataegus L.). Molec. Ecol. 26:5484–5499. 10.1111/mec.14331
COUGHLAN, J.M., S. STEFANOVI?, & T.A. DICKINSON. 2014. Relative resource allocation to dispersal and competition demonstrates the putative role of hybridity in geographical parthenogenesis. J. Biogeogr. 41:1603–1613. 10.1111/jbi.12316
CRIBARI-NETO, F. & A. ZEILEIS. 2010. Beta regression in R (vignette). J. Statist. Software 34:1–24.
CUSHMAN, K.R., M.B. BURGESS, E.T. DOUCETTE, G.A. NELSON, & C.S. CAMPBELL. 2017. Species Delimitation in Tetraploid, Apomictic Amelanchier (Rosaceae). Syst. Bot. 42:234–256.
DAI, H., X. GUO, Y. ZHANG, Y. LI, L. CHANG, & Z. ZHANG. 2009. Application of random amplified polymorphic DNA and inter-simple sequence repeat markers in the genus Crataegus. Ann. Appl. Biol. 154:175–181.
DICKINSON, T.A. 1983. Crataegus crus-galli L. sensu lato in southern Ontario: Phenotypic variation and variability in relation to reproductive behavior Ph.D. Ph.D. University of Western Ontario, Canada.
DICKINSON, T.A. 1986. Topodeme differentiation in Ontario taxa of Crataegus (Rosaceae: Maloideae): Leaf morphometric evidence. Canad. J. Bot. 64:2738–2747.
DICKINSON, T.A. 1998. Taxonomy of agamic complexes in plants: a role for metapopulation thinking. Folia Geobot. 33:327–332.
DICKINSON, T.A. 1999. Species concepts in agamic complexes. In: Raamsdonk LWDv, and Nijs JCMd, eds. Evolution in man-made habitats. Institute for Systematics & Ecology, Amsterdam, The Netherlands. Pp. 319–339.
DICKINSON, T.A. 2018. Sex and Rosaceae apomicts. Taxon 67:1093–1107.
DICKINSON, T.A. 2021. Geographic distribution of sites occupied by Crataegus sect. Douglasianae and C. sect. Salignae. Available at https://zenodo.org/record/5567919.
DICKINSON, T.A., S. BELAOUSSOFF, R.M. LOVE, & M. MUNIYAMMA. 1996. North American black-fruited hawthorns: I. Variation in floral construction, breeding system correlates, and their possible evolutionary significance in Crataegus sect. Douglasii Loudon. Folia Geobot. & Phytotax. 31:355–371.
DICKINSON, T.A. & S. HAN. 2023. What is Suksdorf’s hawthorn? Revision of the western North American 20-stamen black-fruited hawthorns (Crataegus section Douglasianae, Rosaceae subtribe Malinae). Available online: http://morphobank.org/permalink/?P832.
DICKINSON, T.A. & S. HAN. in prep. Why so many 10-stamen black-fruited hawthorns in the Pacific Northwest? – further evidence of hybridization in Crataegus section Douglasianae (Rosaceae subtribe Malinae) J. Bot. Res. Inst.
DICKINSON, T.A., E. LO, & N. TALENT. 2007. Polyploidy, reproductive biology, and Rosaceae: understanding evolution and making classifications. Pl. Syst. Evol. 266:59–78.
DICKINSON, T.A., E.Y.Y. LO, N. TALENT, & R.M. LOVE. 2008. Black-fruited hawthorns of western North America – one or more agamic complexes? Botany 86:846–865. 10.1139/B08-072
DICKINSON, T.A. & R.M. LOVE. 1997. [North American black-fruited hawthorns: III.] What IS Douglas hawthorn? In: Kaye T, Liston A, Love RM, Luoma DL, Meinke RJ, and Wilson MV, eds. Conservation and management of Oregon's native flora. Corvallis OR: Native Plant Society of Oregon. Pp. 162–171.
DICKINSON, T.A. & J.B. PHIPPS. 1984. Studies in Crataegus L. (Rosaceae: Maloideae) IX. Short shoot leaf heteroblasty in Crataegus crus-galli L. sensu lato. Canad. J. Bot. 62:1775–1780.
DICKINSON, T.A. & J.B. PHIPPS. 1985. Studies in Crataegus L. (Rosaceae: Maloideae) XIII. Degree and pattern of variation in Crataegus section Crus-galli in Ontario. Syst. Bot. 10:322–337.
DICKINSON, T.A. & J.B. PHIPPS. 1986. Studies in Crataegus (Rosaceae: Maloideae) XIV. The breeding system of Crataegus crus galli sensu lato in Ontario (Canada). Amer. J. Bot. 73:116–130.
DICKINSON T.A., B.X. YAN, S. HAN, & M. ZARREI. 2021. Niche shifts, hybridization, polyploidy and geographic parthenogenesis in Western North American hawthorns (Crataegus subg. Sanguineae, Rosaceae). Agronomy 11:2133.
DICKINSON, T.A. & B.X. YAN. 2021. Variation in leaf venation in Pacific Northwest hawthorns. Available at http://morphobank.org/permalink/?P2523.
DOUGLAS, D. 1914. Journal kept by David Douglas during his travels in North America 1823–1827. Antiquarian Press for the Royal Horticultural Society, New York, U.S.A.
EDDMAPS. 2016. Crataegus monogyna. Available at http://www.eddmaps.org/distribution/uscounty.cfm?sub=5392 (accessed 23 August 2016.
EL-GAZZAR, A. 1980. The taxonomic significance of leaf morphology in Crataegus (Rosaceae). Bot. Jahrb. Syst. 101:457–469.
EVANS, RC. & T.A. DICKINSON. 1996. North American black-fruited hawthorns II. Floral development of 10- and 20-stamen morphotypes in Crataegus section Douglasii (Rosaceae: Maloideae). Amer. J. Bot. 83:961–978.
FRIENDLY, M. & J. FOX. 2017. Package ‘candisc’ (Visualizing Generalized Canonical Discriminant and Canonical Correlation Analysis). Available at https://cran.r-project.org/web/packages/candisc/candisc.pdf.
FRONTIER, S. 1976. Étude de la décroissance des valeurs propres dans une analyses en composantes principales: comparaison avec le modèle du bâton brisé. J. Exp. Mar. Biol. Ecol. 25:67–75.
GBIF: THE GLOBAL BIODIVERSITY INFORMATION FACILITY. 2021. What is GBIF? Available at https://www.gbif.org/what-is-gbif (accessed 30 Aug 2020).
GITTINS, R. 1985. Canonical analysis. Berlin: Springer-Verlag.
GLADKOVA, V.N. 1968. Karyological studies of the genera Crataegus L. and Cotoneaster Medic. (Maloideae) as related to their taxonomy. Bot. Zhurn. 53:1203–1273.
GREENE, E.L. 1891. Flora Franciscana. An attempt to classify and describe the vascular plants of middle California. Cubery & Co., Printers, San Francisco, California, U.S.A.
GRIFFITH, G.E., J.M. OMERNIK, D.W. SMITH, T.D. COOK, E. TALLYN, K. MOSELEY, & C.B. JOHNSON. 2016. Ecoregions of California (poster). U.S. Geological Survey. p Open-File Report 2016–1021.
HAN, S. 2013. The role of physiological homeostasis in enabling a wider distribution in tetraploid Crataegus douglasii (Rosaceae). University of Toronto, Canada. P. 16.
HAN, S, Q. SUN, & X. ZHEN. 2013. The role of physiological homeostasis in enabling a wider distribution in tetraploid Crataegus douglasii (Rosaceae) [poster]. University of Toronto & Royal Ontario Museum, Canada.
HAUCK, N.R., H. YAMANE, R. TAO, & A.F. IEZZONI. 2006. Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172:1191–1198.
HELLER, A.A. 1903. Notes on plants from middle western California. Bull. S. Calif. Acad. Sci. 2:65–70.
HOJSGAARD, D. & T. PULLAIAH. 2022. Chapter 6, Apomictic roses. Apomixis in angiosperms: mechanisms, occurrences, and biotechnology. Taylor & Francis Group, Milton, UK. Pp. 77–100.
HOLMGREN, N.H. 1997. Rosaceae. In: Cronquist A, Holmgren NH, and Holmgren PK, eds. Intermountain flora. New York Botanical Garden, Bronx, U.S.A. Pp. 64–158.
HOOKER, W.J. 1832. Flora boreali-americana; or the botany of the northern parts of British America. London: Henry G. Bohn.
HUNT INSTITUTE FOR BOTANICAL DOCUMENTATION. 2005. The Torner Collection of Sessé and Mociño Biological Illustrations. Nootka Crataegus = #1959 (http://huntbot.org/artdb/art-collection-search?title_op=%3D&title=6331.1959) (accessed 15 April 2019).
JARDINE, N. & R. SIBSON. 1970. Quantitative attributes in taxonomic descriptions. Taxon 19:862–870.
JOMBART, T. 2015. An Introduction to adegenet 2.0.0. Available at http://adegenet.r-forge.r-project.org/files/tutorial-basics.pdf (accessed 07 Jan 2023.
JOMBART, T. & AHMED I. 2011. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. doi: 10.1093/bioinformatics/btr521
JOMBART, T. & C. COLLINS. 2015. A tutorial for Discriminant Analysis of Principal Components (DAPC) using adegenet 2.0.0. Available at http://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf (accessed 28 Jun 2020.
JUDD, W.S., D.E. SOLTIS, P.S. SOLTIS, & G. IONTA. 2007. Tolmiea diplomenziesii: A new species from the Pacific Northwest and the diploid sister taxon of the autotetraploid T. menziesii (Saxifragaceae). Brittonia 59:217–225. 10.1663/0007-196X(2007)59[217:TDANSF]2.0.CO;2
KAHLE, D. & H. WICKHAM. 2013. ggmap: Spatial visualization with ggplot2. The R Journal 5:144–161.
KOLAR?IK, V., V. KOCOVÁ, V. MIKOLÁŠ, L. MÁRTONFIOVÁ, N. HAJDU?EKOVÁ, & P. MÁRTONFI. 2022. Variability of reproduction pathways in the Central-European Populations of hawthorns with emphasis on triploids. Plants 11:3497.
KOLAR?IK, V., V. KOCOVA?, & D. VAS?KOVA?. 2018. Flow cytometric seed screen data are consistent with models of chromosome inheritance in asymmetrically compensating allopolyploids. cytometry Part A 93:online. DOI: 10.1002/cyto.a.23511
KRUSCHKE, E.P. 1965. Contributions to the taxonomy of Crataegus. Milwaukee Public Museum, Wisconsin, U.S.A.
LEGENDRE, L. & P. LEGENDRE. 1998. Numerical Ecology. In: Jorgensen SE, ed. Developments in environmental modelling. 2nd ed. Elsevier Scientific Publishing Company, Amsterdam, The Netherlands. P. 419.
LEVENE, H.I. 1960. Robust tests for equality of variances. In: Olkin, I., S.G. Ghurye, W. Hoeffding, W.G. Madow, & H.B. Mann, eds. Contributions to Probability and Statistics. Stanford University Press, Stanford, CA, U.S.A. Pp. 278–292.
LEWIS, D. 1947. Competition and dominance of incompatibility alleles in diploid pollen. Heredity 1:85–108.
LINDLEY, J. 1835. Crataegus douglasii - The Douglas thorn. Edwards's Bot. Reg. 21:t. 1810.
LISTON, A., K.A. WEITEMIER, L. LETELIER, J. PODANI, Y. ZONG, L. LIEU, & T.A. DICKINSON. 2021. Phylogeny of Crataegus (Rosaceae) based on 257 nuclear loci and chloroplast genomes: evaluating the impact of hybridization. PeerJ 9:e12418. http://doi.org/10.7717/peerj.12418
LIU, B.-B., C.S. CAMPBELL, D.-Y. HONG, & J. WEN. 2020. Phylogenetic relationships and chloroplast capture in the Amelanchier-Malacomeles-Peraphyllum clade (Maleae, Rosaceae): Evidence from chloroplast genome and nuclear ribosomal DNA data using genome skimming. Molec. Phylogen. Evol. 147:106784. https://doi.org/10.1016/j.ympev.2020.106784
LIU, B.-B., D.-Y. HONG, S.-L. ZHOU, C. XU, W.-P. DONG, G. JOHNSON, & J. WEN. 2019. Phylogenomic analyses of the Photinia complex support the recognition of a new genus Phippsiomeles and the resurrection of a redefined Stranvaesia in Maleae (Rosaceae). J. Syst. Evol. 57:678–694. 10.1111/jse.12542
LO, E.Y.Y. 2008. Global and fine scale molecular studies of polyploid evolution in Crataegus L. (Rosaceae) Ph.D. Ph.D. University of Toronto, Canada.
LO, E.Y.Y., S. STEFANOVI?, K.I. CHRISTENSEN, & T.A. DICKINSON. 2009a. Evidence for genetic association between East Asian and Western North American Crataegus L. (Rosaceae) and rapid divergence of the Eastern North American lineages based on multiple DNA sequences. Molec. Phylogen. Evol. 51:157–168. doi:10.1016/j.ympev.2009.01.018
LO, E.Y.Y., S. STEFANOVI?, & T.A. DICKINSON. 2007. Molecular reappraisal of relationships between Crataegus and Mespilus (Rosaceae, Pyreae) - two genera or one? Syst. Bot. 32:596–616.
LO, E.Y.Y., S. STEFANOVI?, & T.A. DICKINSON. 2009b. Population genetic structure of diploid sexual and polyploid apomictic hawthorns (Crataegus; Rosaceae) in the Pacific Northwest. Molec. Ecol. 18:1145–1160. 10.1111/j.1365-294X.2009.04091.x
LO, E.Y.Y., S. STEFANOVI?, & T.A. DICKINSON. 2010. Reconstructing reticulation history in a phylogenetic framework and the potential of allopatric speciation driven by polyploidy in an agamic complex in Crataegus (Rosaceae). Evolution 64:3593–3608. 10.1111/j.1558-5646.2010.01063.x
LO, E.Y.Y., S. STEFANOVI?, & T.A. DICKINSON. 2013. Geographical parthenogenesis in Pacific Northwest hawthorns (Crataegus; Rosaceae). Botany 91:107–116. 10.1139/cjb-2012-0073
LONGLEY, A.E. 1924. Cytological studies in the genus Crataegus. Amer. J. Bot. 11:295–317.
LOUDON, J.C. 1838. Arboretum et fruticetum brittanicum, vol. 2. Longman, Orme, Brown, Green, and Longmans, London, UK.
LOVE, R. & M. FEIGEN. 1978. Interspecific hybridization between native and naturalized Crataegus (Rosaceae) in western Oregon. Madroño 25:211–217.
LOVE, RM. 1998. Wilhelm Nikolaus Suksdorf (1850–1932), pioneer botanist of the Pacific northwest. Pacific N.W Quart. 89:171–187.
LOVE, R.M. 2007. Pioneer botanist William Cusick: His dark and silent world. Kalmiopsis 14:8–16.
MACKLIN, JA, PHIPPS JB. & BOUFFORD DE. 2000. Charles Sargent's type concept: a guide to interpreting his names in Crataegus (Rosaceae). Harvard Pap. Bot. 5:123–128.
MAJESKÝ, L, F. KRAHULEC, & R.J. VAŠUT. 2017. How apomictic taxa are treated in current taxonomy: A review. Taxon 66:1017–1040. DOI: 10.12705/665.3
MARSHALL, H.H. 1978. Identification of Crataegus species native to Manitoba. Canadian Field Naturalist 92:321–326.
MATZK, F., A. MEISTER, & I. SCHUBERT. 2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Pl. J. 21:96–108.
MCGOEY, B.V., K. CHAU, & T.A. DICKINSON. 2014. Stomata size in relation to ploidy level in North American hawthorns (Crataegus, Rosaceae). Madroño 61:177–193. 10.3120/0024-9637-61.2.177
MEEHAN, T. 1898. The plants of Lewis and Clark's expedition across the continent, 1804–1806. Proc Acad Nat Sci Phila 1898:12–49.
MEIRMANS, P.G. 2020. GENODIVE version 3.0: Easy-to-use software for the analysis of genetic data of diploids and polyploids. Molec. Ecol. Res. DOI: 10.1111/1755-0998.13145
MEYERS, S.C., T. JASTER, K.E. MITCHELL, L.K. HARDISON. & T. HARVEY. 2015. Flora of Oregon, Vol. 1. Botanical Research Institute of Texas Press, Fort Worth, U.S.A.
MOFFETT, A.A. 1931. The chromosome constitution of the Pomoideae. Proc. Roy. Soc. London, Ser. B, Biol. Sci. 108:423–446.
MUNIYAMMA, M. & J.B. PHIPPS. 1979a. [Studies in Crataegus (Rosaceae: Maloideae). I.] Cytological proof of apomixis in Crataegus (Rosaceae). Amer. J. Bot. 66:149–155.
MUNIYAMMA, M. & J.B. PHIPPS. 1979b. [Studies in Crataegus (Rosaceae: Maloideae). II.] Meiosis and polyploidy in Ontario species of Crataegus in relation to their systematics. Canad. J. Genet. Cytol. 21:231–241.
MUNIYAMMA, M. & J.B. PHIPPS. 1984. Studies in Crataegus: XI. Further cytological evidence for the occurrence of apomixis in North American hawthorns. Canad. J. Bot. 62:2316–2324.
MUNIYAMMA, M. & J.B. PHIPPS. 1985. Studies in Crataegus. XII. Cytological evidence for sexuality in some diploid and tetraploid species of North American hawthorns. Canad. J. Bot. 63:1319–1324.
NUTTALL, T. 1846. The North American Sylva. Townsend Ward, Philadelphia, Pennslyvania, U.S.A.
OKSANEN, J. 2008. Multivariate analysis of ecological communities in R: vegan tutorial. P. 39.
OKSANEN, J., G. SIMPSON, F. BLANCHET, R. KINDT, P. LEGENDRE, P. MINCHIN, R. O'HARA, P. SOLYMOS, S. DURAND, H. EVANGELISTA, R. FITZJOHN, M. FRIENDLY, B. FURNEAUX, G. HANNIGAN, M. HILL, L. LAHTI, D. MCGLINN, M. OUELLETTE, E. RIBEIRO CUNHA, T. SMITH, A. STIER, C. TER BRAAK & J. WEEDON. 2022. vegan: Community Ecology Package, R package version 2.6-2. https://CRAN.R-project.org/package=vegan
PALMER, E.J. 1925. Synopsis of North American Crataegi. J. Arnold Arbor. 6:5–128.
PARADIS, E, J. CLAUDE, & K. STRIMMER. 2004. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. 10.1093/bioinformatics/btg412
PHIPPS, J.B. 1997. Monograph of northern Mexican Crataegus (Rosaceae, subfam. Maloideae). Sida, Bot. Misc. 15:1–94.
PHIPPS, J.B. 1999. The relationships of the American black-fruited hawthorns Crataegus erythropoda, C. rivularis, C. saligna, and C. brachyacantha to C. Ser. Douglasianae (Rosaceae). Sida 18:647–660.
PHIPPS, J.B. 2008. Kruschke names in North American Crataegus (Rosaceae): A correction and clarifications. J. Bot. Res. Inst. Texas 2:473.
PHIPPS, J.B. 2013. Crataegus. Available at http://ucjeps.berkeley.edu/cgi-bin/get_IJM.pl?tid=91319 (accessed 31 Jul 2014.
PHIPPS, J.B. 2015. Crataegus. In: 1993+ FNAEC, ed. Flora of North America North of Mexico. Oxford University Press, New York, U.S.A. and Oxford, UK. Pp. 491–643.
PHIPPS, J.B. & MUNIYAMMA M. 1980. [Studies in Crataegus (Rosaceae: Maloideae) III.] A taxonomic revision of Crataegus (Rosaceae) in Ontario. Canad. J. Bot. 58:1621–1699.
PHIPPS, J.B. & O'KENNON RJ. 2002. New taxa of Crataegus (Rosaceae) from the northern Okanagan-southwestern Shuswap diversity center. Sida 20:115–144.
PHIPPS J.B., K.R. ROBERTSON, P.G. SMITH, & J.R. ROHRER. 1990. A checklist of the subfamily Maloideae (Rosaceae). Canad. J. Bot. 68:2209–2269.
PTAK, K. 1986. Cyto-embryological investigations on the Polish representatives of the genus Crataegus L. I. Chromosome numbers; embryology of diploid and tetraploid species. Acta Biol. Cracov., Ser. Bot. 28:107–122.
PTAK, K. 1989. Cyto-embryological investigations on the Polish representatives of the genus Crataegus L. II. Embryology of triploid species. Acta Biol. Cracov., Ser. Bot. 31:97–112, Pl. 115.
PURSH, F.T. 1814. Flora Americae septentrionalis. London, UK.
R CORE TEAM. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
REVEAL, J.L., G.E. MOULTON, & A.E. SCHUYLER. 1999. The Lewis and Clark collections of vascular plants: Names, types, and comments. Proc. Acad. Nat. Sci. Philadelphia 149:1–64.
RICH, T.C.G. 2009. Pollen stainability in British Sorbus L. (Rosaceae). Pl. Ecol. & Diversity 2:85–88.
RICKETT, H.W. 1936. Forms of Crataegus pruinosa. Bot. Gaz. (Crawfordsville) 97:780–793.
ROBUCHON, M., D.P. FAITH, R. JULLIARD, B. LEROY, R. PELLENS, A. ROBERT, C. THE?VENIN, S. VE?RON, & S. PAVOINE. 2019. Species splitting increases estimates of evolutionary history at risk. Biol. Conservation 235:27–35. https://doi.org/10.1016/j.biocon.2019.03.041
RONFORT, J, E. JENCZEWSKI, T. BATAILLON, & F. ROUSSET. 1998. Analysis of population structure in autotetraploid species. Genetics 150:921.
RYAN, T.A., JR. & B.L. JOINER. 1974 (updated 1990). Normal probability plots and test for normality. MINITAB. P. 13.
SARGENT, C.S. 1907a. The black-fruited Crataegus of western North America. Bot. Gaz. (Crawfordsville) 44:64–66.
SARGENT, C.S. 1907b. The genus Crataegus in North America. J. Bot. 45:289–292.
SCHNEIDER, C.K. 1906. Illustriertes Handbuch der Laubholzkunde. Gustav Fischer, Jena, Germany.
SIMPSON, G.G. 1961. Principles of animal taxonomy. Columbia University Press, New York, U.S.A.
SMITH, M.R. 2019. TreeTools: Create, modify and analyse phylogenetic trees. Comprehensive R Archive Network.
SMITH, P.G. & J.B. PHIPPS. 1988. Studies in Crataegus (Rosaceae, Maloideae). XIX. Breeding behavior in Ontario Crataegus series Rotundifoliae. Canad. J. Bot. 66:1914–1923. 10.1139/b88-262
SOLTIS, D.E., P.S. SOLTIS, D.W. SCHEMSKE, J.F. HANCOCK, J.N. THOMPSON, B.C. HUSBAND, & W.S. JUDD. 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56:13–30.
STANDISH, L.M. 1916. What is happening to the hawthorns? J. Heredity 7:266–279.
STEUDEL, E.G. 1840. Nomenclator botanicus. J.G. Cottae, Stuttgart, Germany.
TALENT, N. & T.A. DICKINSON. 2005. Polyploidy in Crataegus and Mespilus (Rosaceae, Maloideae): Evolutionary inferences from flow cytometry of nuclear DNA amounts. Canad. J. Bot. 83:1268–1304.
TALENT, N. & T.A. DICKINSON. 2007a. Apomixis and hybridization in Rosaceae subtribe Pyrineae Dumort.: a new tool promises new insights. In: Grossniklaus U, Hörandl E, Sharbel T, and van Dijk P, eds. Apomixis: Evolution, mechanisms and perspectives. Gantner Verlag, Ruggell, Liechtenstein, Germany. Pp. 301–316.
TALENT, N. & T.A. DICKINSON. 2007b. Endosperm formation in aposporous Crataegus (Rosaceae, Spiraeoideae, tribe Pyreae): Parallels to Ranunculaceae and Poaceae. New Phytol. 173:231–249. https://doi.org/10.1111/j.1469-8137.2006.01918.x
TALENT, N. & T.A. DICKINSON. 2007c. The potential for ploidy level increases and decreases in Crataegus (Rosaceae, Spiraeoideae, tribe Pyreae). Canad. J. Bot. 85:570–584.
TAYLOR, RL. & G.A. MULLIGAN. 1968. Flora of the Queen Charlotte Islands, Part 2. Cytological aspects of the vascular plants. Research Branch Monograph. Ottawa: Canada Department of Agriculture. p ix + 148.
THORSON, T.D., S.A. BRYCE, D.A. LAMMERS, A.J. WOODS, J.M. OMERNIK, J. KAGAN, D.E. PATER, & J.A. COMSTOCK. 2003. Ecoregions of Oregon (color poster with map, descriptive text, summary tables, and photographs). U.S. Geological Survey, Reston, Virginia, U.S.A.
TORREY, J. & GRAY A. 1840. A flora of North America. Wiley & Putnam, New York, U.S.A.
TURNER, N.J. 2014a. Ancient pathways, ancestral knowledge: Ethnobotany and ecological wisdom of indigenous peoples of northwestern north america volume one - the history and practice of indigenous plant knowledge. McGill-Queen's University Press, Montreal, Canada & Kingston.
TURNER, N.J. 2014b. Ancient pathways, ancestral knowledge: Ethnobotany and ecological wisdom of indigenous peoples of northwestern North America Volume Two - The place and meaning of plants in indigenous cultures and worldviews. McGill-Queen's University Press, Montreal, Canada & Kingston.
TURNER, N.J. 2014c. Appendix 2B. Names of native plant species in indigenous languages of northwestern North America. University of Victoria. Available at https://dspace.library.uvic.ca/bitstream/handle/1828/5091/Appendix%202B%20%20UVicSpace%20Indigenous%20names%20of%20native%20species_BIG.pdf (accessed 14 July 2014).
UFIMOV, R.A. & T.A. DICKINSON. 2020. Infrageneric nomenclature adjustments in Crataegus L. (Maleae, Rosaceae). Phytologia 102:177–199.
VAN VALEN, L. 1976. Ecological species, multispecies, and oaks. Taxon 25:233–239.
VAN VALEN, L. 1978. The statistics of variation. Evol. Theory 4:33–43.
VANDER KLOET, S.P. & T.A. DICKINSON. 1999. The taxonomy of Vaccinium section Myrtillus (Ericaceae). Brittonia 51:231–254.
VAŠKOVÁ, D. & V. KOLAR?IK. 2019. Breeding systems in diploid and polyploid hawthorns (Crataegus): Evidence from experimental pollinations of C. monogyna, C. subsphaerica, and natural hybrids. Forests 10:1059.
VÁSQUEZ-CRUZ, M., A.P. VOVIDES, & V. SOSA. 2017. Disentangling species limits in the Vauquelinia corymbosa complex (Pyreae, Rosaceae). Syst. Bot. 42:1–13. 10.1600/036364417X696519
VERBYLAIT?, R., B. FORD-LLOYD, & J. NEWBURY. 2006. The phylogeny of woody Maloideae (Rosaceae) using chloroplast trnL-trnF sequence data. Biologija 2006:60–63.
VOSS, E.G. 1965. A review on Crataegus. Michigan Bot. 4:93–96.
VOSS, E.G. 1966. Contributions to taxonomy of Crataegus. Amer. Midl. Naturalist 75:252–253.
WEBER, W.A. 1942. The botanical collections of Wilhelm N. Suksdorf 1850–1932. M.Sc. State College of Washington, Pullman, U.S.A.
WEBER, W.A. 1944. The botanical collections of Wilhelm N. Suksdorf. Research Studies, State College of Washington XII. Pullman, U.S.A.
ZAPATA, F. & I. JIMÉNEZ. 2012. Species delimitation: Inferring gaps in morphology across geography. Syst. Biol. 61:179–194. 10.1093/sysbio/syr084
ZARREI, M., S. STEFANOVI?, & T.A. DICKINSON. 2014. Reticulate evolution in North American black-fruited hawthorns (Crataegus section Douglasia; Rosaceae): Evidence from nuclear ITS2 and plastid sequences. Ann. Bot. 114:253–269. 10.1093/aob/mcu116
ZARREI, M., N. TALENT, M. KUZMINA, J. LEE, J. LUND, P.R. SHIPLEY, S. STEFANOVI?, & T.A. DICKINSON. 2015. Universal plant DNA barcode loci are poor indicators of species diversity in hawthorns (Crataegus; Rosaceae). AoB Pl. 7: plv045 10.1093/aobpla/plv045
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