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Systematics of Cuscuta chinensis species complex (subgenus Grammica, Convolvulaceae): evidence for long-distance dispersal and one new species

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Abstract

Cuscuta chinensis species complex is a small clade from subgenus Grammica (Cuscuta, Convolvulaceae). Many species of this clade exhibit crest- or dome-like multicellular appendages with stomata on the midvein/carena of calyx lobes. Basic morphology, scanning electron microscopy, and DNA sequence data from the plastid trnL-F region and the nuclear internal transcribed spacer (ITS) were used to investigate the phylogenetic relationships within the group and test the species limits. Based on their morphological and molecular similarly, C. chinensis and C. applanata represent one single species, and the latter was retained as a variety of the former. While the clade is centered in the southern USA and Mexico, C. chinensis var. chinensis has a disjunct distribution in Australia and Asia, which is likely the result of relatively recent long-distance dispersal. Cuscuta alata from Mexico, previously considered synonymous to C. applanata, was found to be a distinct species based on both molecular and morphological evidence. Cuscuta potosina var. potosina and var. globifera segregate into two different subclades of the C. chinensis species complex. Because these two taxa are also different morphologically, var. globifera is described as a new species, C. azteca. Cuscuta campestris, an almost cosmopolitan weed species from another clade (“Clade B”; “C. pentagona complex”), is commonly misidentified in Asia as C. chinensis, which raises questions about the identity of the Cuscuta plants used in widely commercialized medicinal herbal mixtures. A taxonomic treatment with an identification key, descriptions, and illustrations is provided.

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Acknowledgments

We thank the curators/directors of AAU, ALTA, ARIZ, ASU, B, BAB, BM, BOL, BRIT, CANB, CAS, CEN, CHR, CHSC, CIIDIR, CIMI, CONC, CORD, CTES, DAO, F, G, GH, H, HUFU, IAC, IEB, IND, J, JEPS, LL, LP, LPB, LPS, K, MEL, MERL, MEXU, MICH, MO, NMC, NY, OAC, OKLA, OSC, OXF, PACA, PRE, QCNE, QFA, P, PACA, RB, RSA, SAM, S, SD, SGO, SI, SPF, TEX, TRT, TRTE, UB, UBC, UCR, UCT, UNB, UNM, UPRRP, UPS, US, USAS, ZEA, WTU and XAL for supplying plant material. Miguel García and Guy Nesom kindly provided comments that improved the quality of the article. Ignacio García Ruiz, Eleazar Carranza and Tom Van Devender sent us additional plant material. This research was supported by NSERC of Canada Discovery grants to M.C. (327013) and S.S. (326439).

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Authors and Affiliations

  1. Department of Biology, Wilfrid Laurier University, Waterloo, Ontario, N2L 3C5, Canada

    Mihai Costea & Ian Spence

  2. Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario, L5L 1C6, Canada

    Saša Stefanović

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  1. Mihai Costea
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  2. Ian Spence
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  3. Saša Stefanović
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Correspondence to Mihai Costea.

Appendices

Appendix 1

Herbarium vouchers used for taxa description and examined for micromorphology. Species accession code: country, region, location, elevation (m a.s.l.), date, collector(s), herbarium acronym

1. Cuscuta alata . MEXICO. Sinaloa. La Cofradía, 26 Oct 1904, Brandegee s.n. (MO); Cerro Colorado, 450 m, 10 Dec 1939, Gentry 992 (ARIZ). Mpio. Culiacán, on Rd at Varejonal, 10 Km from the international Hwy, 12 Oct 1984, Ochoa Avalos & Bojórguez 196 (MEXU). Chihuahua. South Western Chihuahua, Aug–Nov 1885, Palmer 142 (GH, K, MEXU). 2. Cuscuta azteca. U.S.A. Arizona. Cochise Co.: Mule Mts., W side, 18 Sep 1961, Goodding 290–61 (ASU). Greenlee Co.: U.S. 666, 7.6 mi S of Hog Trail Saddle, 7 Sep 1968, Pinkava et al. 13685 (ASU). New Mexico. Otero Co.: Caballero Canyon, 2103 m, 13 Jul 1997, Fletcher 2348 (UNM). Mogollon Mts., Sep 1881, Rusby 295 (MO). MEXICO. Chihuahua. Mpio. Temosachi: Nabogame, 28°30′N 108°30′W, 19 Sep 1987, Laferrière 1054 (MEXU). Distrito Federal. Close to San Pablo, 7 Sep 1952, Rzedowski 1742 (MEXU). Durango. Mpio. de Mezquital, Santa María de Ocotán, 27 Aug 1984, Gonzáles 1465 (MEXU). Federal District. Valley of Mexico, Pedrigal, 2225 m, 8 Oct 1896, Pringle 6575 (CAS, F, K, MEXU, MO, S). Hidalgo. Mpio. de Hidalgo: near Tula (de Allende), 2072 m, 14 Oct 1902, Pringle 11305 (F, K). Mpio. Pachuca de Soto: Presa Jaramillo, 4 Km N of Pachuca, 2750 m, 2 Nov 1983, Medina 2493 (F, MICH). Morelos. Cuernavaca, 31 Aug 1910, Orcutt 3874 (CAS, MO). Oaxaca. Vicinity of Oaxaca, Juárez Hill, 25 Jul 1947, Kenoyer 1504 (GH). Mpio. San Lorenzo Albarradas: Hierve el Agua, 1757 m, 23 Oct 2003, Torres & Soriano Silva 2360 (MEXU). Puebla. Mpio. Caltepec: vicinity of San Luis Atolotitlán (formerly San Luis Tultitlanapa), 9 Jul 1908, Purpus 3554 (F, MO). Mpio. Tehuacán: El Riego, Aug 1905, Rose & Painter 9888 (K); San Diego, 5 Km from Tehuacàn on Rd to Teotitlan, 1460 m, 12 Dec 1963, McKee 11042 (K); near Cerro el Pinar, 28 Aug 1945, Alexander & Hernández 2242 (NY). Querétaro. Mpio. Pinal de Amoles, 21º04′59.6N 99º36′20.5″, 1546 m, 27 Aug 2007, Ramírez-Amezcua 1099 (IEB). Mpio. Tequisquiapan: Tequisquiapan, 1 Nov 1950, Matuda 18565 (MEXU). San Luis Potosí. Mpio. de Santa María del Río: Paso de Tortugas, San José Albuquerque, 2000 m, 6 Oct 1952, Takaki 10102 (ENCB, MEXU); Sierra de San Miquelito, 2200 m, 10 Sep 1954, Rzedowski 4443 (MEXU); 5 Km al NE de Laguna Seca, 2000 m, 30 Aug 1955, Rzedowski 6298 (MEXU). Sonora. Mpio. Álamos: El Guayabo crossing of Río Cuchujaqui, 2.6 km NE of Sabinito Sur, 14 km (by air) E-SE Álamos; 27°00′05″N 108°47′08″W, 370 m, 21 Nov 1993, Steinmann 93–349 et al. (ARIZ, ASU, UC, UCR). Mpio. Yécora: Restaurant Puerto de la Cruz, 14 km W of Yécora on MEX 16, 28°22′30″N 109°01′42″W, 1920 m, 6 Sep 1996, Van Devender 96–451 et al. (ARIZ, USON, WLU). 3.1. C. chinensis var. chinensis . AUSTRALIA. Northern Territory, 7 May 1948, Sprecht 390 (CANB); Western Australia: at NE end of airstrip One Arm Point, N Dampier Peninsula, W Kimberley, 16º27′S 123º04′E, 9 Apr 1993, Carter 628 (CANB, PERTH); 9 Mar 1989, Keighery 11100 (PERTH); Queensland, 23 Feb 1934, Garvey 71 (BRI). AFGANISTAN. Chanabad, 7 Oct 1927, Bukinitach 7 (NY). CHINA. Anhui Prov.: Qing-hill Dongzhi, 300 m, 9 Sep 1992, Yao 12002 (PE, OSU). Beijing Municipality: Miyunxian, 8 Sep 1951, Wang Web-Tsai 2378 (RSA); Xianshan, 11 Jun 1956, Zhao Fu et al. 1425 (PE, RSA); Xizhimenwai, 30 Jun 1953, Zhao Fu et al. 338 (PE, RSA); near Beijing, Nov 1874, Bushell s.n (NY). Inner Mongolia Autonomous Region, Yin Shan Mts., 22 Jul 1990, Boyd et al. 4379 (RSA). Jiangsu Prov., Yuntaishan, 20 Aug 1981, Yao 8388 (NY). Shantung Prov.: Tsinanfu, 4 Sep 1930, Chiao 3033 (GH, NY); Lao Shan, 16 Aug 1930, Chiao 2931 (GH, NY). Xinjiang Prov.: 3–5 Km N of Dushanzi, 16 Jun 1989, Liston 823–21 (NY, RSA). NORTH KOREA. Rikiho, Sep 1930, Dorsett & Morse 6336 (NY). THAILAND. Nakornrajsima, 3 Mar 1959, Surapat 137(IND). 3.2. C. chinensis var. applanata . U.S.A. Arizona. Cochise Co.: Pearce, 14 Aug 1996, McGill 6746 (ASU); vicinity of Tombstone, 12 Sep 1969, García 348 (MEXU); Huachuca Mountains, Miller Canyon, 1 Oct 1929, Jones s.n. (RSA). New Mexico. Bernalillo Co.: NW of Albuqueque, 1555 m, 24 Sep 1966, Britt 23 (UNM); Albuquerque, 28 Sep 1932, Casteller 7339 (UNM). Dona Ana Co.: White Sands Missile Range, 1290 m, 23 Sep 1990, Spellenberg & Mahrt s.n. (NMC, NY, RSA, UC). Sierra Co.: 2 Mi W of Hillsboro, 1676 m, 9 Sep 1904, Metcalfe 1288 (NMC); Kingston, 2011 m, 13 Sep 1904, Metcalfe 1300 (CAS). Texas. Deaf Smith Co.: Glenorio, 3 Sep 1967, Waller 1537 (ASU); 1 mi S of Glenorio, 3 Sep 1967, Waller 1540 (ASU). Presidio Co.: 9.3 mi S of Shafter along Hwy 67, 29°43′N 104°21′W, 1020 m, 24 Jul 1973, Henrickson 11268 (RSA). MEXICO. Aguascalientes. Mpio. Calvillo, NW of Escondida, 19 Sep 2002, García 5083 (MEXU). Chihuahua. Mpio de Chihuahua: near Chihuahua, 2 Sep 1886, Pringle 784 (F, G, K, MEXU, MO, S, UPS, US); Sierra Mapula, W base of Pico Chihuahua Viejo, 28°33′N 105°51′30″W, 1500–1675 m, 20 Jul 1977, Lehto 21612 (ASU). Mpio. Jiménez: Biosphere Reserve Mapimí, 26°52′49″N 103°53′9.8″W, 1110 m, 6 Jul 1997, García 2637 (MEXU). Mpio. Madera: vicinity of Nicolás Bravo, 2200 m, 18 Aug 1994, Quintana et al. 3126 (NMC). Coahuila. Ca. 45 Km W of Cuatro Ciénagas, 1100 m, 4–5 Sep 1941, Johnston 8826 (F, GH); 71 Km SSW of Cuatro Cienegas, on Rd 30 to Torreón at Km 159, 26°34′N 102°24′W, 820 m, 13 Sep 1978, Iltis & Lasseigne 70 (F, K, MEXU); 25 mi E of Americanos, 22 Aug 1937, Wynd 754 (GH, IND, K, NY, MO, S). Durango. Mpio. San Juan del Río: San Juan del Rio, 20 Sep 1946, Xolocotzi et al. 2615 (MEXU). Mpio. Gómez Palacio: Dinamita, 2 Aug 1984, Pacheco 67 (MEXU). Mpio. Mapimí: 8 Km SE of Mapimí, 25°47′N 103°46′W, 1999 m, 8 Sep 1983, Torrecillas 237 (MEXU, NY). Mpio. Tlahualilo, Biosphere Reserve Mapimí, 26°34′2.2″N 103°45′0.6″W, 1160 m, 18 Sep 1999, García 3576 (MEXU). Guanajuato. Mpio. San Miguel de Allende: 8 mi N of San Miguel de Allende, 6 Jul 1963, Harris 25806 (GH). Hidalgo. 8 km SSW of Alfajayucan, 2000 m, 6 Sep 1965, Quintero 3026 (MEXU). Oaxaca. Mpio. Villa Tepelmeme de Morelos: La Mesa del Calvario, 18°01′N 97°21′W, 1920 m, 18 Sep 1994, Salinas & Martíz-Correa 7390 (MEXU). Puebla. Mpio. Caltepec: Cerro Coatepec, Sof San Luis Atotitlán, 18°09′N 97°27′W, 2115 m, 9 Sep 1993, Salinas et al. 7541 (MEXU). Mpio Tehuacán: near Tehuacán, 20 Aug–3 Sep 1905, Rose et al. 10275 (US); Tehuacán, El Riego, 30 Aug 1905, Rose et al. 9888 (MEXU, US); 4 Km E of San Pablo Tepetzingo, 24 Jul 1979, Chiang et al. 61 (MEXU); 1 Sep 1979, Chiang et al. 315 (MEXU). Mpio. Zapotitlán: "El Potrero", 2–3 Km S of Zapotitlán de las Salinas, 1500 m, 23 Jul 1992, Salinas & Juárez-Jaimes 6977 (MEXU). Querétaro. Mpio. Pinal de Amoles, 13.8 Km at SE of Mex 120, 21°04′59.6″N 99°36′20.5″W, 1546 m, 24 Aug 2007, Ramírez-Amezcua 1099 (IEB). San Luis Potosí. Mpio. de San Luis Potosí: 18 Km E of San Luis Potosí, 1900 m, 8 Jul 1959, Rzedowski 11200 (MEXU); Mpio. de Matehuala: Matehuala, 29 Jun 1970, Clarke 137 (UCR); Charcas, Jul–Aug. 1934, Lundell 5493 (MICH); 2 mi S of Venado, 1950 m, 6 Sep 1939, Shreve 9323 (GH). Sonora. Mpio. Ónavas: Rancho La Mula, 28.2 km SE of Río Yaqui on MEX 16 (KM 195 E of Hermosillo), 28°28′50″N 109°22′W, 790 m, 30 Aug 2000, Van Devender & Reina-G. 2000–506 (ARIZ, WLU). Mpio. Santa Cruz: 0.8 km S of Santa Cruz on road to San Lázaro, 31°11′23″N 110°36′22″W, 1340 m, 17 Aug 2001, Van Devender et al. 2001–710 (ARIZ, USON, WLU). Zacatecas. 35 mi NNW of Concepción del Oro, 24°38′N 101°56′W, 1706 m, 2 Sep 1971, Henrickson 6353 (MEXU). 4. C potosina . MEXICO. Aguascalientes. Mpio. de Calvillo: extreme N of Temazcal, 1900 m, 11 Oct 1987, García 2834 (IEB). Jalisco. Mpio. Ojuelos de Jalisco: Mesa el Toro, W of Ojuelos, 21°56′33″N 101°70′50″W, 2127 m, 28 Aug 2002, Machuca et al. 8820 (IBUG). San Luis Potosí. Mpio. de Santa María del Río, 1850 m, 27 Aug 1954, Rzedowski 3894 (MEXU); San Luis Potosí, 1879, Schaffner 379 (B, MEXU); [same area], 1878, Parry & Palmer 431 (MO). Estado de Mexico. Rd Ameca-Cautla (exit to Tlamaca), 31 Jul 1989, Arreola Gonzáles 13 (MEXU); Mpio Tequiquiac: Cerro Colima Ladera Norte, 8 Nov 1980, 2350 m, Romero-Rojas 825(MEXU). Guanajuato. Mpio. de San Diego de la Unión, 11 Sep 1997, Pérez et al. 3707 (IEB). Puebla (?). Loma del Ciervo, 20 Aug 1906, Altamirano 1606 (MEXU; "Pue" was added to the label at a later date but we could not find this locality anywhere in Mexico). Querétaro. Hacienda Ciervo, 20 Aug 1905, Rose 9650 (MEXU, NY, US). 5. C. yucatana. MEXICO. Chiapas. Mpio of Tenejapa: Paraje Tenejapa, 2700 m, 7 Nov 1971, Breedlove & Sith 22017 (MEXU). Mpio. San Cristóbal Las Casas, 2200 m, 2 Sep 1974, Breedlove 37107 (MEXU); out of San Cristóbal, along Hwy to Comiton, 20 Aug 1957, Alava 1341 (NY); Mpio. Zinacantán, near the summit of Cerro Huitepec, 2600 m, 15 Aug 1976, Breedlove 39587 (MO). Hidalgo. Presa Jaramillo, 4 Km N of Pachuca, 2800 m, 29 Jul 1978, Rzedowski 25758 (G, MEXU). Puebla. Mpio. Tepeyahualco, Laguna Salado, 6 Km N of Laguna Alchichica, 19°28′N 97°25′W, 2300 m, 20 Feb 1980, Nee & Taylor 29575 (F, MO, XAL). Veracruz. Llanos de Alchichica, 2200 m, 20 Jul 1968, Gómez-Pompa 3809 (MO). Yucatán. Valladolid, 22 m, 2 Jul 1932, Steere 1695 (F, NY). GUATEMALA. Dept. Jalapa: vicinity of Soledad, Miramundo Mt., between Jalapa and Mataquescuintla, 2000–2500 m, 4 Dec 1939, Steyermark 32648 (F).

Appendix 2

Taxa, DNA accession numbers, sources of plant material from which DNA was extracted, and GenBank accession numbers for sequences used in this study. DNA extraction numbers are indicated on the phylogenetic trees in the main text following species names. GenBank accession numbers are given for trnL-F followed by ITS. Sequences newly generated for this study are indicated in bold. A dash (−−) indicates missing data. Abbreviations of herbaria in which the vouchers are deposited follow Index Herbariorum

Cuscuta alata: 992, Gentry 5188 (ARIZ), JN234819, JN234825. C. azteca, 592, Medina 2493 (MICH), EF194365, EF194599; 862, Axelrod & Hernandez 2242 (NY), EF194366, EF194600; 1006, Chiang et al. 2187 (TEX/LL), JN234820, JN234826. C. chinensis var. chinensis : 459, Surapat 137 (IND), EF194369, ---; 837, Carter 628 (CANB), EF194368, JN234827/JN234828. C. chinensis var. applanata : 507, Spellenberg & Mahrt 10680 (NMC), EF194373, JN234829; 508, Torrecillas 237 (NY), EF194371, JN234830; 535, Johnston 8826 (F), EF194372, EF194605; 674, Rodrigues 653 (XAL), EF194370, EF194603; 844, Shreve 9323 (GH), JN234821, EF194602; 850, Corral-Diaz 3912 (NMC), JN234822, EF194604; 1159, Valdés 611 (IEB), JN234823, JN234831; 1211, Valdés 621 (ENCB), JN234824, JN234832. C. potosina: 845, Rose et al. 9650 (NY), EF194367, EF194601. C. sandwichiana Choisy: 155, Degener & Degener 36596 (WTU), n/a, EU288356; 686, Degener & Degener 35248A (CANB), n/a, EU288357; 748, Sylva & Rumel s.n. (NY), n/a, EU288358. C. yucatana Yunck.: 657, Alava 1341 (NY), EF194364, EF194598. Outgroups: C. americana L.: 698, Garneau et al. 1470 (TRT), EF194363, ---; 699, Buswell 6231 (NY), ---, EF194597. C. victoriana Yunck.: 678, Cowie 9624 (CANB), EF194383, EF194616.

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Costea, M., Spence, I. & Stefanović, S. Systematics of Cuscuta chinensis species complex (subgenus Grammica, Convolvulaceae): evidence for long-distance dispersal and one new species. Org Divers Evol 11, 373–386 (2011). https://doi.org/10.1007/s13127-011-0061-3

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