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The Ethnobotany and Ethnopharmacology of Wild , longifolia Nutt., and Related Physalis : A Review1

,2 3 2 2 KELLY KINDSCHER* ,QUINN LONG ,STEVE CORBETT ,KIRSTEN BOSNAK , 2 4 5 HILLARY LORING ,MARK COHEN , AND BARBARA N. TIMMERMANN

2Kansas Biological Survey, University of Kansas, Lawrence, KS, USA 3Missouri Botanical Garden, St. Louis, MO, USA 4Department of Surgery, University of Kansas Medical Center, Kansas City, KS, USA 5Department of Medicinal Chemistry, University of Kansas, Lawrence, KS, USA *Corresponding author; e-mail: [email protected]

The Ethnobotany and Ethnopharmacology of Wild Tomatillos, Nutt., and Related Physalis Species: A Review. The wild , Physalis longifolia Nutt., and related species have been important wild-harvested foods and medicinal . This paper reviews their traditional use as food and medicine; it also discusses taxonomic difficulties and provides information on recent medicinal chemistry discoveries within this and related species. Subtle morphological differences recognized by taxonomists to distinguish this species from closely related taxa can be confusing to botanists and ethnobotanists, and many of these differences are not considered to be important by indigenous people. Therefore, the food and medicinal uses reported here include information for P. longifolia, as well as uses for several related taxa found north of . The importance of wild Physalis species as food is reported by many tribes, and its long history of use is evidenced by frequent discovery in archaeological sites. These plants may have been cultivated, or “tended,” by farmers and other tribes. The importance of this as medicine is made evident through its historical ethnobotanical use, information in recent literature on Physalis species pharmacology, and our Native Medicinal Plant Research Program’s recent discovery of 14 new natural products, some of which have potent anti-cancer activity.

La Etnobotánica y Etnofarmacología de los Tomatillos Silvestres, Physalis longifolia Nutt., y Especies Afines a Physalis: Una Revisión. El tomatillo silvestre, Physalis longifolia Nutt., y especiesafineshansidounimportanterecurso de alimentos silvestres y de plantas medicinales. Revisamos los usos tradicionales para la alimentación y la medicina, las dificultades taxonómicas, y proporcionamos los últimos descubrimientos de la química medicinal de esta y de otras especies afines. Las sutiles diferencias morfológicas reconocidas por los taxónomos para poder distinguir las estrechas relaciones de taxones entre estas especies son confusas para los botánicos y los etnobotánicos, pero estas diferencias no son reconocidas como importantes por las poblaciones nativas. Por lo tanto, los usos alimenticios y medicinales reportados incluyen no sólo información sobre P. longifolia, sino también para varios taxones relacionados que se encuentran al norte de México. La importancia de las especies silvestres de Physalis como alimento es reportada por muchas tribus y su larga historia de uso se pone de manifiesto por el descubrimiento frecuente en yacimientos arqueológicos. Estas plantas pueden haber sido cultivadas o “atendidas” por los agricultores de y otras tribus. La importancia de esta planta como medicina se destaca por su historia de uso etnobotánico, por la literatura reciente sobre la farmacología de las especies de Physalis y por el descubrimiento reciente en nuestro Programa Nativo de Investigación de Plantas Medicinales de 14 nuevos productos naturales, algunos de los cuales tienen potente actividad de anti-cáncer.

1 Received 05 March 2012; accepted 10 August 2012; published online ______.

Economic Botany, XX(X), 2012, pp. 1–13 © 2012, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. ECONOMIC BOTANY [VOL

Key Words: Physalis longifolia, Ethnobotany, medicinal, anti-cancer, Tomatillos, Paleoethnobotany, traditional ecological knowledge, Ethnopharmacology, medicinal chemistry.

Introduction and may contain toxins in some parts of the Physalis longifolia Nutt., wild tomatillo or long- plant. Many in the are edible, groundcherry, is a perennial herb that occurs including the ripe fruits of P. longifolia, although throughout the continental U.S. and into southern its foliage and green are considered poison- Canada and (Fig. 1). Its habitat ous at least to livestock (Fuller and McClintock includes old fields, open woods, and prairies, but it 1986; Peterson 1977). thrives in disturbed sites, including roadsides. Plants form colonies through the spread of underground and, because the plant is so common, it is often considered to be a weed. There are at least 75 known species in the The papery calyx (husk) that encloses the tasty Physalis (Whitson and Manos 2005). At fruit of P. longifolia is a distinctive characteristic times, species in the closely related genera of of the genus Physalis, which includes cultivated , Leucophysalis, Margaranthus, species such as tomatillo (P. philadelphica Lam.) Oryctes, and have been included in the and Chinese lantern (P. alkekengi L.). The name genus Physalis. Physalis species are annual or Physalis is Greek for “a bladder,” a reference to perennial, erect or decumbent, sometimes rhizo- the inflated calyx. The genus Physalis is a member matous, glabrous or pubescent, and with various- of the Nightshade family, Solanaceae, which ly toothed or lobed . Physalis is believed to includes tomatoes, potatoes, and tobacco. All have originated in Mexico, and there is only one nightshades are considered somewhat poisonous species (P. alkekengi) whose origin is not of the

Fig. 1. Range of Physalis longifolia in the U.S. and Canada determined by information we obtained from 14 herbaria and other databases (references available upon request). 2012] KINDSCHER ET AL.: THE ETHNOBOTANY OF PHYSALIS LONGIFOLIA

New World, although many cultivated and weedy The genus Physalis contains several species Physalis species have been introduced, both grown for their ornamental or edible fruits, which intentionally and inadvertently, to warm areas are eaten raw or cooked. The most commonly worldwide. Whitson (2011) has proposed sepa- cultivated species in is the rating P. alkekengi into a new genus, Alkekengi, tomatillo (P. philadelphica), which is often culti- and conserving the name Physalis for the rest of vated for food and used in verde. Many other the species. This is based on recent molecular species, such as the Cape gooseberry (P. peruviana studies that separate Alkekengi, in addition to its L.) and the husk or muyaca in South distinctive red inflated calyx, lobed white , America (P. pubescens), L. have been cultivated and its unique Eurasian geographic distribution. and eaten for their acidulous fruit (von Mueller There are 29 Physalis species in the United 1895). The Chinese lantern plant (P. alkenkengi, States, of which four are non-native. Physalis referred to above), is an ornamental species that is longifolia and P. viscosa L. are listed as noxious cultivated for its brightly colored orange-red husk. weeds in , where P. longifolia was apparently introduced (USDA, NRCS 2011; Native American Food Use Invasive Plant Atlas of the 2011). Physalis species were used by numerous North Historically, Physalis species have been taxonom- American tribes across a large geographic ically classified based on characters such as habit, (Fig. 2). Elias Yanovsky (1936) authored the first hair type, and number of calyx angles (Whitson ethnobotanical compilation of Physalis species and and Manos 2005). Many species are not easily their uses by Native Americans. He listed ten distinguished without careful examination and can species of Physalis, including P. longifolia, that be confused even by botanists. For this reason, were used as food. Due to nomenclatural changes, several species have been misidentified in historical nine species are listed by Moerman (2011). ethnobotanical accounts, as discussed below. Also, However, there has been little study of the food native people likely used several species inter- uses in any depth. Gary Nabhan stated in his changeably, as evidenced by the fact that indige- “Native Crop Diversity in ” that nous names have been used for more than one “the cultural geography of Physalis deserves species. In addition, nomenclatural changes have further investigation” (Nabhan 1985). And it is resulted from recent analyses using molecular data clear that they were used by more tribes than we and the results of artificial hybridization, which have been able to document here. have provided new understanding of relationships Edward Castetter (1935)reportedinhis among taxa. Thus, references to some species in “Uncultivated Native Plants Used as Food— the older literature (e.g., P. pumila Nutt., P. Ethnobotanical Studies in the American South- lanceolata Michx., and P. virginiana Mill.) (USDA, west” that the berries of P. neomexicana Rydb. NRCS 2011)cannotberelieduponwithcertainty. and P. longifolia were both used as food by the The typical Physalis species is an herb with Rio Grande Pueblos in . The fruits axillary yellow flowers that are solitary and bee usually were boiled but sometimes were eaten pollinated (Sullivan 1984). Once fresh. Castetter also reported that at Acoma and has occurred, the corolla drops off and the calyx Laguna Pueblos, the fruits were referred to by the expands until the developing is complete- names charoka and shuma charoka. These species ly enveloped by a papery husk. These husked were used in a similar manner at the San Felipe fruits are characteristic of the genus and make Pueblo and were known as sharoka. them easy to recognize as a group. The many- According to Matilda Stevenson’s(1915) “Eth- seeded berries of Physalis species range from nobotany of the Zuni Indians,” the berries of P. greenish to yellow to orange and are sometimes fendleri A. Gray (now recognized as P. hederifolia flushed with purple or red (Whitson and Manos A. Gray by Allred 2010) had the same Zuni name 2005), thus explaining the use of the common (Ke’tsitokia, which refers to an insect that feeds names “ground tomato” and “husk tomato” upon the plant) as P. longifolia. This suggests that (Castetter 1935). The berry of P. longifolia is these species were not distinguished from one yellow-green when ripe and tastes like an another and may have been used interchangeably. effervescent, under-ripened , or, Stevenson reported that this plant grew wild in when dried, tastes like a cross between a raisin lowlands on the Zuni reservation in western New and dried . Mexico and was also cultivated in the small ECONOMIC BOTANY [VOL

General locations of tribes referenced in the text. 1Zuni 2 Rio Grande Pueblo 3 Acoma 4 Laguna 5 San Felipe 6Hopi 7Omaha 8 Ponca 9Dakota 10 Pawnee 11 Cherokee 12 13 Meskwaki 14 Hidatsa 15 Pima 16 White Mountain 17 Mohave 18 Yuma 19 Ramah Navaho 20 Winnebago 21 22 Mescalero Apache 23 Mountain Pima

Fig. 2. Tribes (numbers refer to names on the key) who used Physalis species for food or medicine, and stars designate some of the archeological sites (citations in text) where Physalis seeds have been found. The shaded range, by state and province, for all Physalis species, is from the USDA Plants database (USDA NRCS 2011).

gardens worked by women. The ripe red fruits, favor with the ancient Zunis as food according to which were described as tasting similar to a Cushing. They were boiled or stewed to make a tomato, were boiled with a small amount of sauce, which, although not quite so acidic, water and ground in a mortar with raw , otherwise tasted like cranberry sauce (Cushing and seeds. The dish was regarded 1920). The wild tomatillo is still currently used as as a great delicacy (Castetter 1935). Ethnologist food at the Zuni Reservation. In Rita Edaakie’s Walter Hough (1898) also reported that the Zuni “Idonaphshe—Let’sEat—Traditional Zuni dried and ground the berries to produce a meal Foods,” she gives a recipe for the use of K’e: for making bread and stated that in the “old ts’ido’kya K’yalk’osenne, or tomatillo paste, in times” the berries of P. longifolia were eaten by which the domesticated tomatillos, P. philadelph- the . ica, are used to make a tasty sauce that includes In Frank Cushing’s “Zuni Breadstuffs” (based roasted chiles and green onions (Edaakie 1999; on his work on the Zuni Reservation in the Nabhan 2008). This recipe is certainly an 1880s), he writes: “Among the sandy defiles of adaptation of the previous use of native Physalis the upper plains, mesas, and mountains, grow species. abundant low bushes bearing very juicy little There is documented food use of seven other yellow berries called k’ia’-po-ti mo’-we, or the Physalis species found north of Mexico. Because ‘juice-filled fruitage’.” These berries were in high these species co-occur in the region of use of P. 2012] KINDSCHER ET AL.: THE ETHNOBOTANY OF PHYSALIS LONGIFOLIA longifolia in the United States and are similar to the Winnebago in Wisconsin in the 1930s it, they are being reported here. Melvin Gilmore (Kindscher and Hurlburt 1998). The annual P. reported that the fruits of P. heterophylla Nees angulata L. fruit were eaten fresh by the Eastern were made into a sauce for food by the Omaha, Band of the Cherokee when they turned yellow Ponca, Dakota, and Pawnee. When there was (Cozzo 2004). Also, the annual P. neomexicana sufficient quantity, the fruits were dried for the was reported by Edward Castetter in 1936 to be winter (Gilmore 1913). The Omaha and Ponca considered a delicacy and commonly eaten by name, Pe igatush, translates as “forehead, to pop,” Chiricahua and Mescalero Apache in New Mex- referring to popping the inflated calyx against the ico (Castetter and Opler 1936). Additionally, in head, a playful diversion that kids still shared in northern Mexico, P. caudella Standl. (which also Nebraska when growing up in the 1970s occurs in and New Mexico) is common (Kindscher, personal communication). in Mountain Pima agricultural fields in Chihua- When the Dakota first saw figs, they likened hua. Fruits are eaten green or ripe, primarily by them (likely because of their sticky texture and children (Laferriere et al. 1991). sweetness when dried) to Physalis, and called them Tomaniohpe washichu, “White man’s Phys- alis” (Gilmore 1977). The Cherokee (Hamel and Ancient Uses of Physalis Species Chiltoskey 1975), Cheyenne (Hart 1981), and as Food Meskwaki (Smith 1928) also used the berries of Physalis species occur commonly in archaeo- P. heterophylla as food. Buffalobird Woman (a logical materials in the Southwest, , Hidatsa), informed ethnobotanist Gilbert Wilson and Midwest (see Fig. 2). Identifying charred in 1916 that wild tomatillos were scarce on the seeds to species is not possible, so they all are Hidatsa reservation in North Dakota, but when simply identified as Physalis species. The charred they were found, the fruits were collected and seeds have been found at archaeological sites in eaten fresh in the field or brought back to the New Mexico dating from as early as AD 298 at lodges. When occasionally found in quantity, the LA 109100 on Ceja Mesa west of Albuquerque fruits were pounded and shaped into patties that (Dello-Russo 1999) and at the Basketmaker III/ were dried, similar to those made with choke- (AD 650–900) at River’s Edge cherries (Nickel 1974) west of the Rio Grande River and north of The bud clusters of a species identified as P. Corrales (Brandt 1991). The period of use lanceolata were used in the spring by the Dakota extends into the Coalition and Classic periods of as food (Gilmore 1913). Later, this tribe also ate the Rio Grande Classification (AD 1200–1600), the firm young, green “seed pods” boiled with occurring at LA 1051 (Toll and McBride 2011), meat. According to current taxonomic authori- LA 2 (McBride and Smith 2011), and at Arroyo ties, P. lanceolata is a species that occurs only in Hondo Pueblo (Wetterstrom 1986) in the Santa the Carolinas and Georgia, so Gilmore’s account Fe district, as well as on the Pajarito Plateau near must actually refer to one of the perennial species Los Alamos (McBride 2008). Seeds also have —P. virginiana, P. longifolia,orP. pumila. All of been found at Salmon Ruin, an ancestral Pueblo these species occur in northeast Nebraska on the site in northwest New Mexico (Doebley 1981). Dakota reservation where Gilmore interviewed At the Yellowjacket site in southwest , elders and collected roots (see Fig. 3)but 800--old charred seeds of Physalis species were apparently did not collect a voucher specimen. common in hearths and middens (Kuckelman Other species used as food include P. acutifolia 2003). (Miers) Sandw., which the Pima in the Southwest The plants often are associated with aban- desert ate raw (Rea 1997). P. hederifolia fruits doned fields, as they flourish in disturbed, were eaten by the White Mountain Apache, weedy habitats, but some archeologists (Yarnell Mohave, and Yuma (Moerman 2011). P. pubes- 1965) suspect that wild tomatillos actually were cens fruit were eaten fresh, cooked, or dried by the cultivated or at least encouraged among other Mohave, Yuma, and Ramah (Moerman crops before Pueblo times. Prehistoric inhab- 2011). P. virginiana fruit were eaten raw by the itants probably cooked fresh fruits, dried the Meskwaki in Wisconsin after they were “touched fruits, or ground dried seeds to cook with other by frost in the fall” (Smith 1928). This species foods (Wetterstrom 1986). All of these uses also was reported by Huron Smith to be eaten by would provide opportunity for some seeds to be ECONOMIC BOTANY [VOL

Fig. 3. Top left: Physalis longifolia (wild tomatillo) in a field near Cimarron, Kansas. Top right: Fruits, sliced in half and dried, become chewy and sweet, although a little acidulous. Middle left: Roots of P. longifolia. The Omaha and Ponca names for P. lanceolata, and possibly also P. longifolia, has been translated as “crooked medicine,” an apparent reference to the roots, which were used to treat headache and stomach trouble, and as a dressing for wounds. Middle right: Dried root samples of “crooked medicine,” P. lanceolata, collected in 1927 by ethnobotanist Melvin Gilmore, archived at the Smithsonian’s National Museum of the American Indian Cultural Resources Center in Suitland, MD (catalog number: 15/2097), used with permission. Bottom left: P. longifolia seeds as they appear under a microscope. Bottom right: Ripe fruits of P. longifolia. The fruits were eaten raw, cooked or dried by the Zuni, Hopi and other Native American tribes. preserved, since a cook might inadvertently the Southwest. Given that about 10 percent of scatter some seeds during preparation of a sauce fecal samples contained Physalis,itisbelieved or other dish. The lower moisture content of that the fruits were associated with agricultural dried seeds or fruits versus fresh increases the crops and were a food of moderate importance chance of being carbonized in a fire. (Minnis 1989). Further evidence of food usage is the Richard Yarnell (1965) studied archaeological discovery of Physalis seedsincoprolites(dried sites of the Pajarito Plateau (near Los Alamos, feces) of the agricultural Basketmaker III and New Mexico, at elevations from 6,100 to 6,700 Pueblo III people in the region of feet). He commented: “Five species of Solanaceae 2012] KINDSCHER ET AL.: THE ETHNOBOTANY OF PHYSALIS LONGIFOLIA appear to have considerable significance in Ethnopharmacology of Physalis that they are highly correlated with growing longifolia and Other Related Species at archaeological sites. These are In northeast Nebraska, the ethnobotanist jamesii, , Physalis neomexi- Melvin Gilmore (1977) reported in 1919 that cana, pallidum,andDatura meteloides. P. lanceolata was known by the Omaha and Three other species, Chamaesaracha conioides, Ponca as makan bashahon-shon, “crooked medi- var. cordifolia,andSolanum cine,” apparently referring to the crooked roots of elaeagnifolium, are apparently of lesser signifi- the plant. The root of this species (actually P. cance.” These species appear to be more than longifolia, P. virginiana,orP. pumila; see dis- cussion above on Gilmore’s identification) was just weeds associated with the disturbance of used as medicine by the Omaha, Ponca, and archaeological sites, since ethnobotanical evi- Winnebago to treat headache and stomach dence suggests that all of them are associated trouble, and as a dressing for wounds. Alice with agricultural, food, and cultural practices Fletcher and Francis La Flesche (1911) reported (Yarnell 1965). that the Omaha Buffalo doctors used P. viscosa Physalis seeds are frequently found in archeo- (Gilmore reported that this was actually P. logical sites from the Great Plains to the eastern lanceolata) roots to dress wounds. United States as well. They were widely available The Lakota were reported to eat P. heterophylla in the summer and fall in the eastern woodlands, fruits to increase the appetite (Rogers 1980). The where they have been found at several archeo- Iroquois used the dried leaves and roots of P. logical sites (Scarry 2003). Wild tomatillo seeds heterophylla as a wash to treat venereal disease are abundant at two winter camps of the Fort sores and also internally as a tea to treat Ancient culture (1000–1750 AD) in east-central stomachache after one was sick (Herrick 1995). Kentucky. They were among the wild plants The dried leaves and root of P. pubescens were discovered at the Dymock sites in Ontario, used by the Navaho as a “life medicine” (Vestal which are Western Basin Younge phase sites 1952). The Meskwaki made an infusion of the (ca. AD 1000–1200) (Crawford and Smith whole plant of P. virginiana to treat dizziness 2003). Physalis seeds also were found at the (Smith 1928). Meehan-Schell site, a Late Woodland site (AD Many other Physalis species throughout the 850–1100) in Iowa along with many other world have been used traditionally for medicine. native seeds, grains, and nuts (Mead 1981). In One anti-cancer finding relates directly to the South Dakota, they were identified at the work discussed below. It is the use of a paste, Mitchell site, an Initial Middle Missouri Com- extracted from the leaves and stems of P. mimima L. (a weedy species, most likely native to the New plex (AD 900–1400) (Benn 1974). World tropics), which traditionally has been used Seeds were present at the Two Deer site in in Thailand and Malaysia as a medicine to treat Kansas of the Bemis Creek Complex, Late cancer (Lee and Houghton 2005). Woodland (AD 550–1005) (Adair and Brown 1978). In south-central Oklahoma, they were Medicinal Chemistry, Anti-Cancer identified at the Densmore site, Early Plains Studies, and Recent Discoveries Village Period (AD 900–1250) (Drass 1993). They also were being used into the Protohis- Physalis species are known to contain carbohy- toric era at the Longhorn site in Texas in the drates, lipids, minerals, , and early 1600s (Dering 1993a, b). Finally, Physalis (Puente et al. 2011). They also are a major seeds were found at the Recon John Shelter in contributor of -type structures. With- southeastern Colorado, a Woodland/Early Ce- anolides are classically defined as a group of C28 ramicsite(15BC–AD 1000) (Zier and Kalasz ergostane-type with a C-22,26 δ-lactone 1991). In addition to these ancient sites, group, first isolated from the genus archeological remains of Physalis have been (Lavie et al. 1965). They are restricted to the found at historic period Cherokee sites at the Solanaceae family (subfamily ), which Ravensford and Coweeta Creek sites in North includes the genera , Physalis, and With- Carolina and at Brasstown Valley in Georgia ania (Zhang et al. 2012; Misico et al. 2011; Chen (Cable et al. 1997; VanDerwarker 2012). et al. 2011; Eich 2008; and Veleiro et al 2005). ECONOMIC BOTANY [VOL

Withanolides have attracted substantial recent 5) fibroblast control cells tested with IC50 values interest due to their exhibition of significant in the range 0.067–9.3 μM, while the other biological activities, specifically antimicrobial, were inactive (Zhang et al. 2011). In antitumor, anti-inflammatory, immunomodulato- addition, none of the withanolides demonstrated ry, and insect-antifeedant activities (Misico et al. cytotoxicity in normal fibroblast cells at or below 2011; Chen et al. 2011). The typical withanolide, the concentrations where cancer cells demonstrat- , has been shown in vitro and in vivo ed toxicity. For these reasons, there is consider- to suppress the growth of an array of tumor cells, able interest in these new compounds. including breast, pancreatic, prostate, lung, leu- Other recent anti-cancer discoveries include kemia, and head and neck squamous cell carci- those found in P. angulata, which demonstrated noma, by inducing programmed cell death anti-metastatic and anti-angiogenic activity (Hsua (Samadi et al 2010)—therefore possessing poten- et al. 2011). This species also was found to tial to inhibit tumorous cell growth. contain anti-proliferative withanolides, cyto-toxic Most research on these compounds has been against prostate cancer cells (Jin et al. 2012), and studies of ashwagandha, ,an as well as Physalin B, which has anti-melanoma important plant in Ayurvedic medicine for more activity (Hsu et al. 2012). In addition, P. minima than 3,000 (Mishra et al. 2000). It has been has been shown to have significant cytotoxic used traditionally as a liver tonic, anti-inflamma- activity on human lung cancer cells (Leong et al. tory agent, aphrodisiac, treatment for arthritis and 2011). rheumatism, and as an adaptogen to promote overall health and longevity (Monograph 2004; Erroneous Hallucinogenic Information Mishra et al. 2000). The State Act 159 (2006) treats P. As part of an ongoing study of withanolides by subglabrata (now recognized as a variety of P. our group, the and biological longifolia) as a hallucinogenic plant. This poten- activity of P. longifolia was evaluated for the first tial hallucinogen is listed at two popular culture time (Zhang et al. 2011). Fourteen new with- web sites: Wikipedia (2011), and Erowid (2011), anolides (named withalongolides A-N), four apparently because it is listed in this state act. We acetylated derivatives and eight known com- conducted extensive searches of the internet and pounds were isolated and identified from the academic search engines but could not find any aerial parts of this species (Zhang et al. 2011). information to support this claim. We contacted The classically defined withanolide-type steroids the state representative (now the Louisiana isolated from P. longifolia have a diversity of Commissioner of Agriculture) who sponsored oxygenation patterns. the bill, and he informed us that “The Plant Eight known compounds were also identified Kingdom and Hallucinogens” by Dr. Richard from P. longifolia, including seven withanolides Evans Schultes (1970) was the source of infor- (sitoindoside IX, withaferin A, 2,3-dihydro-3β- mation for Act 159. This law restricts cultivation methoxywithaferin A, viscosalactone B, 2,3-dihy- and possession of 39 listed “hallucinogenic dro-3β-O-sulfate withaferin A, 2,3-dihydrowitha- plants,” including the fungi Amanita muscaria ferin A, and 3α,6α-epoxy-4β,5β,27-trihydroxy-1- and Psilocybe spp., entire genera such as Erythrina oxowitha-24-enolideJ) and a flavonoid glucoside, spp. and also Salvia divinorum, Ipomoea violacea, rutin (Zhang et al. 2011). A voucher specimen for and . However, Schultes made this material was collected in Ellsworth County, no mention of the genus Physalis. We have no Kansas, by Hillary Loring (collection number alternative but to believe that the inclusion of P. 3583) and deposited in the R.L. McGregor subglabrata (P. longifolia var. subglabrata)asa Herbarium at the University of Kansas. hallucinogenic plants in Louisiana State Act 159 When tested against human head and neck is erroneous. squamous cell carcinoma and against melanoma cell lines for their cytotoxicity, eight withanolides Toxicity (including withalongolides A,B, C, D, E,G,H, There is little evidence of substantial toxicity in sitoindoside IX, withaferin A, and 2,3-dihydro- Physalis species. The fruits of species north of 3β-O-sulfate withaferin A) and four acetylated Mexico have been documented to be eaten as derivatives showed potent cytotoxic effects against food. Two cases of livestock poisoning involving the cancer cells compared to normal fetal (MRC- P. angulata foliage in hay or forage have been 2012] KINDSCHER ET AL.: THE ETHNOBOTANY OF PHYSALIS LONGIFOLIA reported for California (Fuller and McClintock being used as food and medicine by Native 1986). However, the toxicity has not been Americans. Species identifications are often diffi- confirmed. Overall there is little reason to cult and confusing for both botanists and ethno- consider the plants toxic, other than that they botanists, and many species were traditionally may contain -type glycoalkaloids used interchangeably. Physalis seeds have been (Burrows and Tyrl 2001) present throughout found at numerous archaeological sites, dating most of the Solanaceae. Solanine, a chemical from the Archaic to the Classic period in the Rio destroyed by heat, is reported to be in the green Grande Valley; and fruit. This may explain why the young bud southwestern Colorado; through the Great Plains clusters of the plants and some sauces were and the Midwest; and into Ontario, Canada. prepared by cooking. Like other members of the Physalis species have tasty fruits and likely were Solanaceae, including tomatoes and peppers, only encouraged in agricultural fields and possibly even the fruits of Physalis are generally consumed as cultivated. Although less important than food food, while the foliage is considered somewhat uses, Native American medicinal uses of Physalis poisonous. also were common. Recent work by our Native Medicinal Plant Research Program (http:// Cultivation nativeplants.ku.edu/) has led to the discovery of We have found P. longifolia relatively easy to many interesting new compounds, including grow from seed in the greenhouse. Seedlings were withanolides, within the plant and fruit, some of transplanted to our research garden where all which have potent anti-cancer activity. In addi- individuals of this perennial easily fruited the first tion, several recent studies highlight potential year. The fruits are not only tasty in sauce, but anti-cancer activity and other therapeutic uses of also are sweet and flavorful when cut and dried. Physalis species. Based on the numerous, exten- Because of their widespread use and occurrence in sive, and long-term use of the fruits as food, it traditional Native American gardens, it is possible appears they are safe for consumption. Although that P. longifolia and other wild tomatillos may this common plant is widely ignored and de- have been cultivated. Gary Nabhan (2008) states scribed as a weed, it was once an important plant that Physalis “grows as a weed among Tarahumara for both food and medicine, and may be so again. and Tepehuan fields in the Sierras (of Mexico) but also appears to have been semi-cultivated by Acknowledgements some Pueblo, Navajo, and Hispanic gardeners of This study was supported by grant IND0061464 northern New Mexico.” Paul Minnis surmised (awarded to B. Timmermann and K. Kindscher) that it is one of the numerous species in the from the Kansas Bioscience Authority and Heart- Southwest and adjacent Mexico that was actively land Plant Innovations. We have received help from managed for harvest (Minnis 2001). many people with our work on Physalis.Craig Physalis longifolia was described as cultivated by Freeman of the R.L. McGregor Herbarium at the Pueblo people by both Matilda Stevenson (1915), University of Kansas has been especially helpful who had lived at Zuni Pueblo and observed it in with making species identification. Janet Sullivan their gardens, and also by Edward Castetter of the Albion Hodgdon Herbarium at the Univer- (1935). There is speculation—due to the discov- sity of New Hampshire reviewed the taxonomy in ery of an unusually large Physalis species seed at a the paper. Maria Pontes Ferreira, Nutrition and Classic Period site near Phoenix, Food Science Department, Wayne State Universi- Arizona—that Physalis may have been cultivated ty, and Jennifer Delisle, Kansas Biological Survey, (Adams 2002; Bohrer 1991). It is possible that helped us with field collections. Dana Peterson and this large seed could have been from a cultivated Gorgina Ross (both of the Kansas Biological variety from Mexico. Whether or not wild Survey), respectively, created the distribution map Physalis species were cultivated, it is clear that and wrote the Spanish abstract. Important reviews the Physalis fruits were widely appreciated and of the manuscript and valuable feedback were encouraged. provided by Richard Felger, University of Arizona; Richard Ford, Anthropology Department, Univer- Conclusion sity of Michigan; and Pam McBride, New Mexico The wild tomatillo, P. longifolia, as well as Office of Archeological Studies. 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