Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Loza Cornejo, Sofía; Terrazas, Teresa; López Mata, Lauro Fruits, and germination in five of globose (Cactaceae) Interciencia, vol. 37, núm. 3, marzo, 2012, pp. 197-203 Asociación Interciencia Caracas, Venezuela

Available in: http://www.redalyc.org/articulo.oa?id=33922725006

How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative FRUITS, SEEDS AND GERMINATION IN FIVE SPECIES OF GLOBOSE CACTEAE (CACTACEAE)

Sofía Loza-Cornejo, Teresa Terrazas and Lauro López-Mata

SUMMARY

The morphological characteristics of fruits and seeds, and the weight, and fruit width. Larger fruits with more seeds are ob- germination responses of freshly matured seeds of five species of served for F. histrix, whereas smaller fruits with less weight and Cacteae ( bumamma, C. clavata, C. cornifera, Fero- fewer seeds are seen for C. clavata. germination is a rapid histrix and uncinata) were studied at room process and usually starts on the third day. High percentages of temperature under laboratory conditions. The aim of the study germination (>80%) are observed on the sixth day in F. histrix was to record the macro- and micro-morphology of fruits and and M. uncinata. It is concluded that some morphological cha- seeds of these species and to investigate specific requirements racteristics of fruits and seeds can be used to support further for germination. Variance analysis detected significant differen- systematic studies of genera and will contribute new ces (p<0.05) for several variables: number of seeds per fruit, knowledge for their potential use and conservation.

Introduction distributed in this country carpus and some Mammillaria members, is based on scarce (Guzmán et al., 2003). Indeed, species) to giant ( analysis of the morphology, Cacti are a typical compo- 73% of the genera and 78% and ) genera. anatomy and composition of nent of arid and semiarid en- of the species are estimated to Recently, significant progress stems, fruits and seeds. Some vironments in the Western be endemic to Mexico has been made in understand- species of this tribe produce Hemisphere, and the second (Hernández and Godínez, ing various aspects of the bi- edible fruits. For example, largest family restricted 1994), and the tribes Cacteae ology, phylogeny, and mor- produces a to the New World (Anderson, and Echinocereae are almost pho-anatomy of Cactaceae small and acidic fruit called 2001). Mexico is one of the exclusively distributed in (Nobel, 2002; Godínez-Álva- ‘tuna of biznaga’, which is main centers of diversification Mexico (Anderson, 2001). rez et al., 2003; Terrazas and traded in regions of , of the Cactaceae family Members of Cacteae range Arias, 2003; Hernández- Querétaro, and San Luis Po- (Goettsch and Hernández, from globular or depressed to Hernández et al., 2011). The tosí. The small red fruits of 2006); around 560 species short columnar cacti, varying current understanding of cac- Mammillaria species are gen- belonging to 50 genera are in size from dwarf (Turbini- ti, particularly of Cacteae erally edible and consumed

KEYWORDS / Coryphantha / Ferocactus / Fruits / Germination / Mammillaria / Seeds / Received: 10/28/2011. Modified: 02/17/2012. Accepted: 02/23/2012.

Sofía Loza-Cornejo. Ph.D. in Teresa Terrazas. Ph.D. in Biol- ma de México, Apartado Pos­ Lauro López-Mata. Ph.D. in Botany, Colegio de Postgradua- ogy, University of North Caro- tal 70-233, México, D.F. 04510. Biology, University of North dos (COLPOS), México. Profes- lina at Chapel Hill, USA. Pro- México. e-mail: tterrazas@ Carolina at Chapel Hill, USA. sor-Researcher, Centro Univer- fessor, UNAM, Mexico. Ad- ibiologia.unam.mx Professor, COLPOS, Monte- sitario de los Lagos, Mexico. dress: Instituto de Biología, cillo, México. e-mail: [email protected] Universidad Nacional Autóno-

MAR 2012, VOL. 37 Nº 3 0378-1844/12/03/197-07 $ 3.00/0 197 FRUTOS, SEMILLAS Y GERMINACIÓN DE CINCO ESPECIES DE CACTEAE GLOBOSAS (CACTACEAE) Sofía Loza-Cornejo, Teresa Terrazas y Lauro López-Mata RESUMEN Las características morfológicas de los frutos y semillas, y llas por fruto, peso y ancho de fruto. Los frutos más grandes la respuesta germinativa de semillas maduras y recién cose- y con mayor número de semillas son los de F. histrix, mientras chadas de cinco especies de Cacteae (Coryphantha bumamma, que los frutos más pequeños y ligeros con el menor número de C. clavata, C. cornifera, Ferocactus histrix, and Mammillaria semillas son los de C. clavata. La germinación es un proceso uncinata) fueron estudiadas bajo condiciones de laboratorio y rápido que inicia al tercer día. El porcentaje de germinación temperatura ambiente. Se registraron las características ma- más alto (>80%) se observó al sexto día en F. histrix y M. un- cro y micromorfológicas de los frutos y semillas de estas espe- cinata. Se concluye que algunas características morfológicas cies e investigaron los requerimientos específicos de germina- de los frutos y las semillas pueden apoyar futuros estudios de ción. El análisis de varianza mostró diferencias significativas sistemática en los géneros de Cactoideae y que el conocimien- (p<0.05) para algunas variables tales como número de semi- to generado contribuirá a su uso potencial y conservación.

FRUTOS, SEMENTES E GERMINAÇÃO DE CINCO ESPÉCIES DE CACTEAE GLOBOSAS (CACTACEAE) Sofía Loza-Cornejo, Teresa Terrazas e Lauro López-Mata RESUMO As características morfológicas dos frutos e sementes, e a gura de fruta. As frutas maiores e com maior número de se- resposta germinativa de sementes maduras e recém colhidas de mentes são as de F. histrix, enquanto que os frutos menores e cinco espécies de Cacteae (Coryphantha bumamma, C. clavata, leves com o menor número de sementes são as de C. clavata. A C. cornifera, Ferocactus histrix, e ) foram germinação é um processo rápido que inicia ao terceiro dia. A estudadas sob condições de laboratório e temperatura ambien- porcentagem de germinação mais alta (>80%) se observou ao te. Registraram-se as características macro e micro morfoló- sexto dia em F. histrix e M. uncinata. Conclui-se que algumas gicas dos frutos e sementes destas espécies e investigaram-se características morfológicas dos frutos e as sementes podem os requerimentos específicos de germinação. A análise de va- apoiar futuros estudos de sistemática nos gêneros de Cactoide- riação mostrou diferenças significativas (p<0,05) para algumas ae e que o conhecimento gerado contribuirá a seu uso poten- variáveis, tais como número de sementes por fruto, peso e lar- cial e conservação.

locally (Bravo-Hollis and Sán- atic studies (Arias and Terra- gated in members of Cacteae The number of seeds per fruit chez-Mejorada, 1991). How- zas, 2004; Arroyo-Cosultchi that co-exist in the scrub of for each species was regis- ever, most of these species et al., 2006) and may also , Mexico. tered. Two hundred seeds per are threatened because they help explain patterns of popu- species were used to record have been removed from their lation dynamics of Cactaceae Materials and Methods quantitative morphological natural populations or their species under field conditions. traits (weight, length, width) habitat has been modified by Studies on seed germination Mature and healthy fruits and qualitative morphological changes in land usage (Her­ in this plant family have fo- of Coryphantha bumamma traits (shape, color, structure nández-Oria et al., 2007). For cused on the relationship be- (Ehrenb.) Britton et Rose, C. of the testa) using an analyti- several genera of Cactaceae, tween germination and differ- clavata (Scheidw.) Backeb, C. cal balance and a dissecting studies on the morphological ent attributes of the plant, cornifera (DC.) Lem., Fe- microscope Leica Zoom 2000 variability of fruits and seeds such as the effect of seed rocactus histrix (DC.) G.E. (Z45V) adapted to an image are scarce or have focused mass and size on regeneration Linds., and Mammillaria unci- analyzer (Media Cybernetics, exclusively on well-known or strategies, mechanisms of re- nata Zucc. ex Pfeiff. were 2006). The roundness index economically important gen- production, abundance of rare collected from their native (width/length ratio) was calcu- era. For example, the compo- species, and ecophysiological populations in Jalisco, Mexi- lated from the length and sition, phytochemicals, and requirements (Rojas-Aréchiga co. An analytical scale (Pre- width measurements. For nutritious elements have been et al., 1997; Rojas-Aréchiga cisa XT 220 A) and a Mitu- scanning electron microscopy analyzed in Opuntia (Joubert, and Vázquez-Yanes, 2000; toyo digital caliper were used (SEM), three or four seeds 1993; Domínguez-López, Flores and Briones, 2001; to record the size and weight per species were washed us- 1996; Sáenz, 1997; Sáenz et Ayala-Cordero et al., 2004; of 30 fruits per species. The ing ultrasound and 95% etha- al., 1998; Butera et al., 2002; Ramí­ rez-Padilla­ and Valverde, fruits were dissected in the nol. Dry seeds were fixed to Duru and Turker, 2005; 2005; Sánchez-Salas et al., laboratory and the seeds were aluminum specimen holders Stintzing et al., 2005), Hylo- 2006; Jiménez-Aguilar and then washed in tap water to with double-sided adhesive (Wybraniec and Miz- Flores, 2010; Flores et al., eliminate pulp remains and tape and coated with gold in rahi, 2002), and Myrtillocac- 2011). In the present study, mucilage. The seeds were im- a JEOL-JFC-1100 sputter tus (Barrera et al., 1998). The differences in fruit and seed mediately placed on absorbent coater. Morphological obser- study of seed morphology and macro- and micro-morpholo- paper until they dried and vations and micrographs were germination processes is im- gy, and the rates of germina- were stored in paper enve- carried out with a JEOL-JSM- portant for supporting system- tion processes were investi- lopes at room temperature. 5310LV field-emission scan-

198 MAR 2012, VOL. 37 Nº 3 Table I when germination cies to red berries in M. unci- seed number, mass and size of fruits of five ceased. A seed was nata and yellow-green in F. globose species of Cacteae considered to be histrix. The fruits exhibited germinated when ovoid to claviform shapes, Species Seeds/fruit Weight Length Width (number) (g) (cm) (cm) the radicle protrud- and only F. histrix showed ed. Interspecific thick walls and was dehiscent Coryphantha bumamma 84 ±35 b 2.0 ±0.56 c 2.7 ±0.5 b 0.6 ±0.40 a differences in mor- at the base. The smallest fruit Coryphantha clavata 56 ±8 a 0.5 ±0.18 a 1.4 ±0.3 a 0.6 ±0.15 a phological charac- (1.4cm length) with the lowest Coryphantha cornifera 99 ±2 b 1.4 ±0.22 b 2.7 ±0.9 b 1.2 ±0.80 ab ters of fruits and number of seeds (56 seeds/ Ferocactus histrix 2100 ±90 c 8.0 ±2.80 d 3.2 ±0.6 b 2.2 ±0.40 b seeds were evalu- fruit) occurred in C. clavata Mammillaria uncinata 70 ±13 b 0.5 ±0.20 a 1.5 ±0.3 a 0.5 ±0.01 a ated through vari- and the largest fruit (3.2cm Means ±SD. n= 30 fruits. Different letters in columns mean significant differences (p<0.05). ance analyses fol- length) with the most seeds

Figure 1 Fruits of globose Cacteae. a:. Coryphantha cornifera, b: Fe- rocactus histrix, c: Mammillaria uncinata. ning electron microscope. The saturated with 10ml of dis- morphological descriptions of tilled water in 9cm diameter the seeds followed the termi- sterile Petri dishes. The mean nology proposed by Barthlott temperature in the laboratory Figure 2 SEM of Coryphantha species seeds, whole seeds and seed and Hunt (2000). was measured using a Data- surface view. a,b: Coryphantha bumamma; c,d: C. clavata; e,f: C. cor- nifera. Bar= 1mm in a; 500μm in c,e; 50μm in b, d and f. The germination experi- logger Dickson SP125/175 ments were carried out under Pro series thermometer. The laboratory conditions using mean temperature was three replicates of 50 seeds 25°C ±2°C during the day, lowed by Tukey’s pair-wise (>2000) was observed in F. per species. Seeds were disin- which has been mentioned to means comparison analyses histrix, the species that also fected by immersion in a so- be optimal for seed germina- (p<0.05). Differences in the had the heaviest fruits (8 ±3g, lution of 10% commercial tion of cacti (Nobel, 1988; number of seeds per fruit Table I). The seeds were oval bleach during 5min (Vega- Rojas-Aréchiga and Vázquez- were evaluated through cova- to reniform, small to medium- Villasante et al., 1996), Yanes, 2000), and 12°C ±3°C riance analyses. All analyses sized (Table II, Figures 2-4), washed several times with during the night. Germina- were performed with SAS glossy or matte, and light- distilled water, and sown on tion was recorded at three software V 9.1.3 (SAS, 2000). brown to brown. The anticli- Whatman Nº 2 filter paper day intervals for 30 days, nal boundaries were incon- Results spicuous or raised. The Table II boundaries were straight ex- mass, size and roundness index of feeds Morphology of cept in M. uncinata, and the of five globose species of Cacteae fruits and seeds microrelief verrucose. Species Weight Length Width Roundness (mg) (mm) (mm) index Fruits varied in Interspecific comparison of shape, size and col- fruit and seed morphology Coryphantha bumamma 1.9 ±0.10 d 2.3 ±0.12 d 0.7 ±0.50 ab 0.3 or (Table I, Figure Coryphantha clavata 1.8 ±0.28 d 1.4 ±0.12 c 0.9 ±0.13 b 0.6 1). Most were juicy The analysis of variance Coryphantha cornifera 0.2 ±0.07 a 0.9 ±0.04 a 0.6 ±0.10 a 0.7 Ferocactus histrix 0.6 ±0.20 b 1.4 ±0.10 c 0.9 ±0.10 b 0.6 berries, varying in detected significant differ- Mammillaria uncinata 1.1 ±0.15 c 1.0 ±0.02 b 0.7 ±0.14 a 0.7 color from pale ences for the number of green with light seeds per fruit (F= 17419, Means ±SD. n= 200 seeds. Different letters in columns mean significant differences red at the apex in df= 4, p<0.0001), weight (F= (p<0.05). Coryphantha spe- 3295.67, df= 4, p<0.0001),

MAR 2012, VOL. 37 Nº 3 199 Figure 5 Percentage of germination of seeds of five species of globose Cactoideae. Bars represent mean ±standard deviation of Figure 3. SEM of Ferocactus histrix and Mammillaria uncinata seeds. Complete three replicates of 50 seeds each. Cb: Coryphantha bumamma, Cc: seed and details of testa Ferocactus histrix (a, b). Mammillaria uncinata (c, d). C. clavata, Cco: C. cornifera, Fh: Ferocactus histrix, Mun: Mam- Bar= 500μm in a, c; 100μm in b; 200μm in d. millaria uncinata.

nation 12 and 8 das re- Sánchez-Mejorada, 1991). spectively. By contrast, Other Mammillaria species C. bumamma concluded (M. gigantea Hildm. ex K. its germination 21 das Schum. and M. melanocentra with 10% of its seeds Poselg) can be distinguished germinated in that time by their claviform fruits, (Figure 5). which are pink or purple in color. Noticeable differences Discussion were observed in the fruit size (length) of M. uncinata Morphology of fruits and other species such as M. and seeds gigantea. In the latter, the fruits were 2.5-3.0cm long The studied species (Bravo-Hollis and Sánchez- showed considerable Mejorada, 1991), whereas the variation in fruit and fruits of M. uncinata were seed morphology. The smaller (1.5 ±0.3cm). Figure 4. SEM of the hilum-micropylar region, HMR. a: Coryphantha bu- mamma, b: C. clavata, c: Ferocactus histrix, d: Mammillaria uncinata. Bar= Coryphantha species had Cactoideae seeds show con- 400μm in a; 500μm in b-d. similarities in fruit mor- siderable variation in their phology with other spe- shape, size, structure and tes- cies of the (C. ta color (Barthlott and Hunt, length (F= 2191.58, df= 4, Seed germination response echinoidea Britton & Rose, C. 2000). Indeed, the studied p<0.0001) and fruit width (F= greenwoodii Bravo, C. scheeri species exhibited morphologi- 1917.22, df= 4, p<0.0001). F. All species reached 100% (Muehlenpf.) L.D. Benson, C. cal variability. The seeds of histrix was characterized by germination in the three rep- sulcata (Engelm.) Britton & C. bumamma and C. cor- larger and heavier fruits, and etitions per species. Seed ger- Rose, and C. werdermannii nifera were curved or reni- more seeds. By contrast, C. mination was a rapid process Boed.) (Bravo-Hollis, 1978; form, and similar to those of clavata and M. uncinata had that started 3-6 days after Bravo-Hollis and Sánchez- C. durangensis (Runge ex K. fruits with fewer seeds and sowing (das). In C. cor- Mejorada, 1991). Characteris- Schum) Britton & Rose. C. were smaller and lighter in nifera and C. clavata, germi- tics, such as red and clavi- clavata and M. uncinata had weight than the other species nation started on the third form fruits of 1.5×0.5cm size, oval seeds, similar to other (Table I). Significant differ- day, reaching the highest per- in M. uncinata were similar species of Mammillaria like ences in seeds among species centages (24-28%) at 6 and 15 to other Mammillaria species M. gigantea, M. petterssonii were observed for weight (F= das (Figure 5). Seed germina- like M. standleyi (Britton & Hildm. and Coryphantha like 3797.76, df= 4, p<0.0001), tion of C. bumamma began Rose) Orcutt, M. johnstonii C. gracilis L. Bremer & A. length (F= 9416.14, df= 4, on the sixth das, also reach- (Britton & Rose) Orcutt, M. B. Lau, C. pseudoechinus p<0.0001) and seed width ing the highest percentage heyderi Muehlenpf., M. mie- Boed., C. recurvata (Engelm.) (F= 429.19, df= 4, p<0.0001). (24%) 9 das (Figure 5). F. giana W.H. Earle, M. ortegae Britton & Rose, C. robusti- C. bumamma seeds present- histrix and M. uncinata were (Britton & Rose) Orcutt, M. spina (Ant. Schott ex En- ed higher weights and characterized by higher rates pachycylindrica Backeb., M. gelm.) Brittion & Rose (Bra- lengths than the lighter and of seed germination (>80%) scrippsiana (Britton & Rose) vo-Hollis, 1978; Bravo-Hollis smaller seeds of C. cornifera on the sixth das. These two Orcutt and M. magnimamma and Sánchez-Mejorada, 1991; (Table II). species concluded their germi- Haw. (see Bravo-Hollis and Barthlott and Hunt, 2000;

200 MAR 2012, VOL. 37 Nº 3 Dicht and Lüthy, 2005). Great Bisnaga) are related to F. fla- Ecological aspects of seed the species of Coryphantha variability occurs in the color vovirens (Scheidw.) Britton & germination response showed a wider period of of the seed testa in Cactaceae. Rose and include species dis- germination with their higher A black or brown color is tributed mainly in Central Differences in the number values at 9 das or even 15 characteristic in most species, Mexico and areas in the puta- of seeds per fruit were found das (22 or 28% respective- whereas a red or brown color tive center of the origin of the between the species studied. ly). Although there was a dif- is common in other species, genus (Tehuacan Valley). The A high variability was ob- ferential time of germination such as C. bumamma and M. morphological characteristics served in this trait even with- all species reached 100% ger- uncinata. C. clavata and C. of the fruit, seed characteris- in the same genus. For ex- mination after 22 DAS. The cornifera exhibited dark tics and distribution of F. his- ample, C. bumamma and C. germination in the species brown or brown seed testas, trix support its inclusion in cornifera had 84-99 seeds, studied is greater than those which is characteristic of C. the Bisnaga section along whereas C. clavata contained reported by Sánchez-Soto et duranguensis (Runge ex K. with other species like F. 56 seeds per fruit on average. al. (2010), Jiménez and Flores Schum) Britton & Rose, C. glaucescens (DC.) Britton & F. histrix was distinguished (2010), and Flores et al. pseudonickelsiae Backeb., C. Rose, F. lindsayi Bravo, F. by larger fruits and more (2011) for other species of pallida Britton & Rose, C. macrodiscus (Mart.) Britton seeds than the other Cacteae Ferocactus (62-91%), Mam- macromeris (Engelm.) Lem., & Rose, F. recurvus (Mill.) species studied. Mcintosh millaria (42-99%) and Cory- and C. sulcata (Engelm.) Brit- Y. Ito ex G. E. Linds., F. (2005) found 1727-3064 seeds phantha (72-98%) However, ton & Rose, according to latispinus (Haw.) Britton & per fruit in F. cylindraceus the high germination percent- Bravo-Hollis and Sánchez- Rose and F. flavovirens, as (Engelm.) Orcutt and F. wisli- ages did not include any pre- Mejorada (1991). Glossy seeds suggested by Cota and Wal- zeni (Engelm.) Britton & germination treatment, in were only observed in C. bu- lace (1997). Rose, so F. histrix is near the contrast with other studies in mamma, in agreement with average for the genus. Ac- which specific requirements seeds of some columnar spe- Potential importance of cording to Rojas-Aréchiga and were needed as for light, wa- cies (Arias and Terrazas, Cacteae fruits Vázquez-Yanes (2000), the ter availability, and mechani- 2004; Arroyo-Cosultchi et al., number of seeds per fruit in cal scarification (Nolasco et 2007). In Cactaceae, studies Most cactus fruits are edi- Cactaceae species is highly al., 1996, 1997; Godínez-Ál- on the macro- and micro-mor- ble; however, information on variable; these differences varez and Valiente-Banuet, phology of the seeds have their morphology and nutri- may serve as strategies for 1998; De la Barrera and No- been successfully applied to tional value is scarce (Kies- reproductive efforts as men- bel, 2003; Martínez-Mendoza different taxonomic levels ling, 2001; Pardo, 2002). Ac- tioned by Harper et al. (1970). et al., 2004; Larrea-Alcázar (Friedrich and Glaetzle, 1983; cording to Esquivel (2004), The number of seeds per fruit and López, 2008). The pre- Glaetzle and Prestlé, 1986; most studies have focused on may also depend on the age germination treatments in- Arias and Terrazas, 2004; the fruit of prickly pears and size of the plant, the clude light-dark treatment, Arroyo-Cosultchi et al., 2006, (Opuntia spp.). Little has been number of flowers produced, different temperatures, addi- 2007). Buxbaum (1958) recog- investigated on the composi- and the origin (wild or culti- tion of growth regulators nized four subtribes, particu- tion and aspects of fruit culti- vated species), as demonstrat- (Cancino et al., 1993; Flores larly in the Cacteae tribe, vation of other species of cac- ed for Cactoideae (Parker, et al., 2006; Ortega-Baes and based on seed morphology: ti, despite the high potential of 1987; León de la Luz and Rojas-Aréchiga, 2007; Orte- Echinocactinae exhibits a these fruits for industrial use Domínguez-Cadena, 1991; ga-Baes et al., 2010; Sánchez- perisperm and hard, black (Ortega-Nieblas et al., 2001). Rojas-Aréchiga et al., 2001; Soto et al., 2010), chemical seed testas; Thelocactinae has For example, the presence of Guillen et al., 2011), or may scarification (Rosas-López black seed testas and a mostly red-purple pigments in the reflect environmental hetero- and Collazo-Ortega, 2004), warty surface; Ferocactinae fruit epidermis of M. uncinata geneity (Harper et al., 1970). and various stress conditions exhibits dotted or reticulated is an important source of nat- However, more detailed stud- and water potentials (Guillén seed testas; and Coryphan- ural dyes in foods and in ies are needed on intra-and et al., 2009). In the present thinae has soft, smooth, and various applications (Stintzing interspecific variability for study, seeds recently collected brown testas, similar to the et al., 2001; Wybraniec and this characteristic. were included. Moreover, lab- Coryphantha and Mammil- Mizrhi, 2002; Stintzing and With the exception of oratory conditions during the laria species studied herein. Carle, 2005; Emaldi et al., Opuntioideae seeds, cacti experiment (20-25°C) were More recently, Taylor and 2006). Antihyperglycemic and seeds germinate quickly sufficient to promote seed Clark (1983) recognized that antihyperlipidemic effects (Bregman and Bouman, 1983; germination. Temperature is the Ferocactus section in- found in the fruits of F. latis- Potter et al., 1984; Del Cas- an important factor that can cludes species with a larger pinus and F. histrix have been tillo, 1986; Rojas-Aréchiga significantly affect the germi- hilum-micropylar region demonstrated, suggesting their and Vázquez-Yanes, 2000; nation percentage. Trujillo (HMR), dried fruit dehiscing application in the prevention Mandujano et al., 2005). The (1982) mentioned that cactus by a basal pole and glossy of diabetes (Pérez-Gutiérrez species analyzed in this study seeds germinate at tempera- seed testas. By contrast, the and Mota-Flores, 2010). Fur- began the germination pro- tures between 24 and 27°C. Bisnaga section includes spe- ther studies involving analyses cess between 3 and 6 das. There are species of cacti cies with seeds whose HMR of the nutritional composition Two studied species, F. his- that require temperatures is narrow with bright seed of fruits of Cacteae species trix and M. uncinata, showed ranging from 15 to 35°C for testas (Taylor and Clark, as well as their morphologi- the highest percentages of germination, such as T. ters- 1983). Cota and Wallace cal characterization may con- germination at 6 das checkii (J. Parm. ex Pfeiff.) (1997) used chloroplast DNA tribute significantly in the (>80%), suggesting that this Britton & Rose (Ortega-Baes evidence to determine that the search for alternative medici- process is synchronized with and Rojas-Aréchiga, 2007), members of one lineage (Sect. nal products. available water. In contrast, Echinocactus platyacanthus

MAR 2012, VOL. 37 Nº 3 201 Link & Otto (Quintana, 1994) REFERENCES Cota JH, Wallace SR (1997) Chloro- graphic trends in the Cactaceae. and phyllanthus plast DNA evidence for diver- Bot. Rev. 69: 173-203. (L.) Haw. (Simão et al., Anderson EF (2001) The Cactus gence in Ferocactus and its rela- Goettsch B, Hernández HM (2006) Family. Timber Press. Portland, tionships to North American co- Beta diversity and similarity 2010). Other authors suggest OR, USA. 768 pp. lumnar cacti (Cactaceae: Cactoi- among cactus assemblages in the that alternating temperatures Arias S, Terrazas T (2004) Seed deae). Syst. Bot. 22: 529-542. Chihuahuan Desert. J. Arid Env. increase germination rates of morphology and variation in the De la Barrera E, Nobel PS (2003) 65: 513-528. globose species such as Echi- genus (Cactaceae). Physiological ecology of seed Guillén S, Benítez J, Martínez-Ra- nocactus platyacanthus, F. J. Plant Res. 117: 277-289. germination for the columnar mos M, Casas A (2009) Seed Arroyo-Cosultchi G, Terrazas T, cactus queretaroen- germination of wild, in situ- flavovirens, F. robustus (Pfei- sis. J. Arid Env. 53: 297-306. ff.) Britton & Rose, and M. Arias S, Arreola-Nava H (2006) managed, and cultivated popula- The systematic significance of Del Castillo RF (1986) Semillas, ger- tions of columnar cacti in the mazatlanensis (Rojas-Aréchi- seed morphology in Stenocereus minación y establecimiento de Tehuacan-Cuicatlan Valley, Mex- ga et al., 1998; Sánchez-Soto (Cactaceae). Taxon 55: 983-992. Ferocactus histrix. Cact. Suc. ico. J. Arid Env. 73: 407-413. et al., 2010). In addition to Arroyo-Cosultchi G, Terrazas T, Mex. 31: 5-11. Guillén S, Terrazas T, De la Barrera temperature, germination also Arias S, López-Mata L (2007) Dicht RE, Lüthy AD (2005) Cory- E, Casas A (2011) Germination depends on the species and Morfología de la semilla de phantha Cacti of Mexico and differentiation patterns of wild (Cactaceae). Bol. Southern USA. Springer. New and domesticated columnar cacti seed characteristics (thickness Soc. Bot. Mex. 81: 17-25. York, USA. 210 pp. in a gradient of artificial selec- of the seed coat, dormancy, Ayala-Cordero G, Terrazas T, López- Domínguez-López A (1996) Empleo tion intensity. Gen. Res. Crop etc.). In some species, charac- Mata L, Trejo-López C (2004) de frutos y de los cladodios de la Evol. 58: 409-413. teristics of the testa, in par- Variación en el tamaño y peso chumbera (Opuntia ficus) en la Guzmán U, Arias S, Dávila P (2003) ticular cuticular secretions, de la semilla y su relación con alimentación humana. Food Sci. Catálogo de Cactáceas Mexica- contribute to improve the col- la germinación de una población Technol. Int. 1: 65-74. nas. UNAM-CONABIO. Mexi- co. 315 pp. lection and distribution of de Stenocereus beneckei. Inter- Duru B, Turker N (2005) Changes in ciencia 29: 692-697. physical properties and chemical Harker M, García-Rubio LA, Riojas- water during imbibition and Barrera F, Reynoso C, Mejía E composition of cactus pear López ME (2008) Composición increase germination (Breg- (1998) Estabilidad de betalaínas (Opuntia ficus-indica) during florística de cuatrohábitats en el man and Graven, 1997). Spe- extraídas del garambullo (Myrti- maturation. JPACD 7: 22-33. Rancho Las Papas de Arriba, cific features of the seed (thin llocactus geometrizans). Food Emaldi UJ, Nassar M, Semprum C municipio de Ojuelos, Jalisco, seed testa, absence of dor- Sci. Technol. Int. 4: 115-120. (2006) Pulpa del fruto del cardón Mexico. Acta Bot. Mex. 85: 1-29. mancy and others) in the spe- Barthlott W, Hunt D (2000) Seed dato (, Cacta- Harper JL, Lovel PH, Moore KG Diversity in the Subfamily Cac- ceae) como materia prima para la (1970) The shapes and sizes of cies studied herein probably toideae. Remous. Richmond, elaboración de mermelada. Arch. seeds. Ann. Rev. Ecol. System. 1: influenced significantly the UK. 173 pp. Latinoam. Nutr. 56: 1-16. 327-356. higher germination rate, as Bravo-Hollis H (1978) Las Cactáceas Esquivel P (2004) Los frutos de las Hernández MH, Godínez H (1994) has been observed in germi- de México Vol I. UNAM. Mexi- cactáceas y su potencial como Contribución al conocimiento nating seeds of columnar cac- co. 755 pp. materia prima. Agr. Mesoam. 15: de las cactáceas mexicanas 215-219. ti (Loza-Cornejo et al., 2008). Bravo-Hollis H, Sánchez-Mejorada H amenazadas. Acta Bot. Mex. 26: (1991) Las Cactáceas de México. Flores J, Briones O (2001) Plant life- 33-52. Further work on the mecha- Vol. III 2ª ed. UNAM. Mexico. form and germination in a Mexi- Hernández-Hernández T, Hernández nisms of germination is need- 599 pp. can intertropical desert: effects of MH, De-Nova JA, Puente R, ed, particularly on the re- Bregman R, Bouman F (1983) Seed soil water potential and tempera- Eguiarte LE, Magallón S (2011) quirements for the germina- germination in Cactaceae. Bot. ture. J. Arid Env. 47: 485-497. Phylogenetic relationships and tion of seeds of other Cactoi- J. Linn. Soc. 86: 357-374. Flores J, Jurado E, Arredondo A evolution of growth form in deae, with the aim of contrib- Bregman R, Graven P (1997) Subcu- (2006) Effect of light on ger- Cactaceae (, Eudi- mination of seeds of Cactaceae cotyledonae). Am. J. Bot. 98: uting to their use, manage- ticular secretion by cactus seeds improves germination by means from the Chihuahuan Desert, 44-61. ment and conservation. Some of rapid uptake and distribution Mexico. Seed Sci. Res. 16: Hernández-Oria JG, Chávez-Martínez species, such as F. histrix, are of water. Ann. Bot. 80: 525-535. 149-155. R, Sánchez-Martínez E (2007) subject to special protection Butera D, Tesoriere L, Di Gaudio F, Flores J, Jurado E, Chapa-Vargas L, Factores de riesgo en las Cacta- in regions of Jalisco and other Bongiorno AM, Pintaudi AM, Ceroni-Stuva A, Dávila-Aranda ceae amenazadas de una región Kohen R, Livrea MA (2002) P, Galíndez G, Gurvich D, semiárida en el sur del Desierto Mexican states, and other spe- León-Lobos P, Ordóñez C, Chihuahuense, Mexico. Inter- cies, such as C. clavata, are Antioxidants activities of Sicil- ian prickly pear (Opuntia ficus- Ortega-Baes P, Ramírez-Bullón ciencia 32: 727-733. considered to be rare species indica) fruits extracts and re- N, Sandoval A, Seal CE, Ulian Jiménez-Aguilar A, Flores J (2010) in Jalisco (Chávez-Martínez et ducing properties of its beta- T, Pritchard HW (2011) Seeds Effect of light on seed germina- al., 2007; Harker et al., 2008). lains: betanin and indicaxan- photoblastism and its relation- tion of succulent species from Significant differences were thin. J. Agric. Food Chem. 50: ship with some plant traits in the southern Chihuahuan Desert: 6895-6901. 136 cacti species. Env. Exp. Bot. comparing germinability and observed for the number of 71: 79-88 Buxbaum F (1958) The phylogenetic relative light germination. seeds per fruit, weight, and division of the subfamily Cereoi- Friedrich H, Glaetzle W (1983) Seed JPACD 12: 12-19. fruit width in the cacti stud- deae, Cactaceae. Madroño 14: morphology as an aid to classi- Joubert E (1993) Processing of the ied. Seed germination was a 177-216. fying the genus fruit of five prickly pear culti- Zucc. Bradleya 1: 91-104. rapid process, usually starting Cancino J, León de la Luz JL, Coria vars grown in South Africa. on the 3 DAS, and high per- R, Romero H (1993) Effect of Glaetzle W, Prestlé H (1986) Seed Food Sci. Technol. Int. 28: morphology of the genus Noto- 377-387. centages of germination were heat treatment on germination of seeds of cardón Pachycereus cactus. Bradleya 4: 79-96. Kiesling R (2001) Cactáceas de la seen. Some morphological pringlei (S. Wats.) Britt. & Rose, Godínez-Álvarez H, Valiente-Banuet Argentina promisorias agronómi- characteristics of fruits and Cactaceae. J. Ariz.-Nev. Acad. A (1998) Germination and early camente. JPACD 4: 11-14. seeds can be used to support Sci. 27: 49-54. growth of Tehuacan Valley cacti Larrea-Alcázar DM, López RP further systematic studies of Chávez-Martínez RJ, Hernández-Oria species: the role of soils and (2008) Seed germination of Cor- Cactoideae genera and will JG, Sánchez-Martínez E (2007) seed ingestion by disperser on ryocactus melanotrichus (K. Documentación de factores de seedling growth. J. Arid Env. 39: Schum.) Britton & Rose (Cacta- contribute to knowledge for amenaza para la flora cactológica 21-31. ceae): and endemic columnar the potential use and conser- del semidesierto Queretano. Bol. Godínez-Álvarez H, Valverde T, cactus of the Bolivian Andes. vation of these . Nakari 18: 89-95. Ortega-Baes P (2003) Demo- Ecol. Bol. 43: 135-140.

202 MAR 2012, VOL. 37 Nº 3 León de la Luz JL, Domínguez-Cade- ceae): light, temperature and tion: a review. J. Arid Env. 44: Simão E, Nakamura AT, Takaki M na R (1991) Evaluación de la re- gibberellic acid effects. J. Arid 85-104. (2010) The germination of producción por semillas de la Env. 69: 169-176. Rojas-Aréchiga M, Orozco-Segovia seeds of Epiphyllum phyllan- pitaya agria (Stenocereus gum- Ortega-Baes P, Aparicio-González M, A, Vázquez-Yanes C (1997) Ef- thus (L.) Haw. (Cactaceae) is mosus) en Baja California Sur, Galíndez G, Del Fueyo P, Süh- fect of light on germination of controlled by phytochrome and México. Acta Bot. Mex. 14: 75-87. ring S, Rojas-Aréchiga M (2010) seven species of cacti from the by nonphytochrome related pro- Loza-Cornejo S, López-Mata L, Ter- Are cactus growth forms related Zapotitlan Valley in , cess. Biota Neotrop. 10: 114- razas T (2008) Morphological to germination responses to Mexico. J. Arid Env. 44: 85- 119. seed traits and germination of light? A test using Echinopsis 104. Stintzing FC, Carle R (2005) Cactus six species of Pachycereae (Cac- species. Acta Oecol. 36: 339-342. Rojas-Aréchiga MA, Orozco-Segovia stems (Opuntia spp.): A review taceae). JPACD 10: 71-84. Ortega-Nieblas M, Molina-Freaner F, A, Vázquez-Yanes C (1998) on their chemistry, technology, Mandujano MC, Montaña C, Rojas- Robles-Burgueño MR, Vázquez- Seed response to temperature of and uses. Mol. Nutr. Food Res. Aréchiga M (2005) Breaking Moreno L (2001) Proximate Mexican cacti species from two 49: 175-194. seed dormancy in Opuntia ras- composition, protein quality and life forms: an ecophysiological Stintzing FC, Schieber A, Carle R trera from the Chihuahuan Des- oil composition in seeds of co- interpretation. Plant Ecol. 135: (2001) Phytochemical and nutri- ert. J. Arid Env. 62: 15-21. lumnar cacti from the Sonoran 207-214. tional significance of cactus Martínez-Mendoza D, López-Rodrí- Desert. J. Food Comp. Anal. 14: Rojas-Aréchiga M, Casas A, pear. Eur. Food Res. Technol. guez B, Flores-Martínez A, 575-584. Vázquez-Yanes C (2001) Seed 212: 396-407. Manzanero-Medina G (2004) Parker KC (1987) Seed crop charac- germination of wild and culti- Stintzing FC, Herbarch KM, Moss- Evaluación de técnicas de teristics and minimum repro- vated (Cac- hammer MR, Carle R, Yi W, propagación de Mammillaria ductive size of organ pipe cac- taceae) from the Tehuacán-Cui- Sellappan S, Akoh C, Bunch R, oteroi Glass & R. Foster. Nat. catlán Valley, Central Mexico. J. tus () in Felker P (2005) Color, betalain Des. 2: 5-7. southern Arizona. Madroño 34: Arid Env. 49: 279-287. pattern, and antioxidant proper- 294-303. Mcintosh ME (2005) Pollination of Rosas-López U, Collazo-Ortega M ties of cactus pear (Opuntia two species of Ferocactus: inter- Pardo O (2002) Etnobotánica de al- (2004) Conditions for the germi- spp.) clones. J. Agric. Food actions between cactus-specialist gunas cactáceas y suculentas del nation and the early growth of Chem. 53: 442-451. bees and their host plants. Func. Perú. Chloris Chil. 5 (1) www. seedlings of chichipe Ecol. 19: 727-734. chlorischile.cl (Goss.) Backeberg and Echino- Taylor NP, Clark JY (1983) Seed morphology and classification Media Cybernetics (2006) Image cactus platyacanthus Link and Pérez-Gutiérrez RM, Mota-Flores JM in Ferocactus subg. Ferocactus. Pro-Plus. Version 6.1. Spring- Otto (Rose) Bravo-Hollis (Cac- (2010) Attenuation of hypergly- Bradleya 1: 3-16. field, MD, USA. 534 pp. cemia and hyperlipidemia in taceae). Phyton 73: 213-220. Terrazas T, Arias S (2003) Com- Nobel PS (1988) Environmental Biol- streptozotocin-induced diabetic Sáenz C (1997) Usi potenziali del ogy of Agaves and Cacti. Cam- rats by chloroform extract of frutto e dei claddi di ficondidia parative stem anatomy in the bridge University Press. New fruits of nell industria alimentare. Riv. subfamily Cactoideae. Bot. Rev. York, USA. 280 pp. and Ferocactus histrix. Bol. Frutticult. 12: 47-52. 68: 444-473. Nobel PS (2002) Cacti-Biology Latinoam. Car. Plant. Med. Aro- Sáenz C, Estévez AM, Sepúlveda E, Trujillo AS (1982) Estudio de algu- and Uses. University of Cali- mat. 9: 475-484. Mecklenburg P (1998) Cactus nos aspectos ecológicos de fornia Press. Berkeley, CA, Potter RL, Petersen JL, Ueckert DN pear fruit: a new source for nat- Echinocactus platycanthus LK. USA. 290 pp. (1984) Germination res­ponses of ural sweetener. Plant Foods & O. en el estado de San Luis Potosí. Thesis. ENEP Iztacala, Nolasco HF, Vega-Villasante F, Díaz- Opuntia spp. to temperature, Hum. Nutr. 52: 141-149. Rondero A (1996) Seed germi- scarification and other treat- Sánchez-Salas J, Flores J, Martínez- UNAM. Mexico. nation of Stenocereus thurberi ments. Weed Sci. 32: 106-110. García E (2006) Efecto del Vega-Villasante FH, Nolasco C, (Cactaceae) under different solar Quintana SME (1994) Contribución tamaño de semilla en la germi- Montaño Hl, Romero-Schmidt irradiation levels. J. Arid Env. al conocimiento de algunos fac- nación de myrios- A, Vega-Villasante E (1996) 36: 123-132. tores que disparan la germi- tigma Lemaire. (Cactaceae), es- Efecto de la temperatura, aci- Nolasco H, Vega-Villasante F, Rome- nación de Echinocactus platya- pecie amenazada de extinción. dez, iluminación, salinidad, ro-Schmidt HL, Díaz-Rondero A canthus LK & O. Thesis. Interciencia 31: 371-375. irradiación solar y humedad (1997) The effects of salinity, UNAM. Mexico 85 pp. Sánchez-Soto BH, Reyes-Olivas A, sobre la germinación de semi- acidity, light and temperature on Ramírez-Padilla CA, Valverde T García-Moya E, Terrazas T llas de Pachycereus pecten- the germination of seeds of (2005) Germination responses of (2010) Germinación de tres cac- aboriginum “cardón barbón” cardón ( (S. three congeneric cactus species táceas que habitan la región cos- (Cactaceae). Cact. Suc. Mex. Wats.) Britton & Rose Cactace- (Neobuxbaumia) with differing tera del noroeste de México. In- 41: 51-61. ae). J. Arid Env. 33: 87-94. degrees of rarity. J. Arid Env. terciencia 35: 299-305. Wybraniec S, Mizrahi Y (2002) Ortega-Baes P, Rojas-Aréchiga M 61: 331-343. SAS (2000) User´s Guide. Statistics. Fruit flesh betacyanin pigments (2007) Seed germination of Rojas-Aréchiga M, Vázquez-Yanes SAS Institute Inc. Cary, NC, in Hylocereus cacti. J. Agric. Trichocereus terscheckii (Cacta- C (2000) Cactus seed germina- USA 128 pp. Food Chem. 50: 6086-6089.

MAR 2012, VOL. 37 Nº 3 203