Scientia Horticulturae 108 (2006) 157161 www.elsevier.

com/locate/scihorti

Phenological stages of the guava tree (Psidium guajava L.)

nez a,*, J.J. Mart nez a, D.M. Salazar b, P. Melgarejo a, R. Mart ndez a, M. Burguera b F. Herna
a

ndez University, Elche (Alicante), Spain Plant Production Department, Miguel Herna b Plant Production Department, Valencia Polytechnic University, Valencia, Spain

Received 10 November 2004; received in revised form 24 January 2006; accepted 26 January 2006

Summary As most fruit tree species, the guava tree (Psidium guajava L.) shows different phenological stages throughout its vegetative period in response to environmental conditions. Sixteen different stages were identied during the annual growing cycle, starting at bud dormancy and ending at fruit ripening. The phenology was coded according to the BBCH General Scale and Fleckingers code. The duration of every phenological stage was measured in both days and as cumulative degree days. # 2006 Elsevier B.V. All rights reserved.
Keywords: Phenological stages; Guava tree; Fleckingers code; BBCH General Scale

1. Introduction The guava tree (Psidium guajava L.) is an evergreen fruit species native to tropical Central America from Southern Mexico to Northern South America (Morton, 1987). Due to its ability to grow in tropical and subtropical climates, the guava tree has been introduced to many countries; it is well adapted to a wide range of soils. Furthermore, the guava tree requires an annual water supply of 10002000 m3/ha-year (Laguado et al., 2002). The best temperature for guava cultivation ranges from 15 to 30 8C, with an annual average temperature of 18 8C (Somarriba, 1985a). These climatic conditions allow growing guavas in singular subtropical areas such as those of Israel, Spain, Italy, Greece and other Mediterranean countries. Worldwide the leading guava producers are Pakistan, Brazil, Mexico, Egypt, India, Colombia, Venezuela and South Africa. Guava yields are obviously based on cultivars, tree age and spacing and range from 5 to 50 MT/ha (Aspra Consultores S.C., 1996). Moreover, guava shows a quite interesting nutritional prole. It is a cheap source of Vitamin C. Its content is 23 times higher than that of orange, ranging from 486 to 871 mg of Vitamin C/100 g of fresh fruit depending on the cultivar. Guava

* Corresponding author. nez). E-mail address: rafa.font@umh.es (R. Mart 0304-4238/$ see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2006.01.022

also contains Vitamin A, phosphorous and calcium. Its iron content is very high (Somarriba, 1985b). As a result of seasonal changes, most fruit tree species show clearly dened phenological stages both during winter dormancy and the active vegetative growth period (Champagnat, 1965). The period of vegetative growth begins at mid spring and nishes in autumn. During this period the guava tree (P. guajava L.) undergoes several physiological changes that are identied because of external signs such as shoot growth, bud swelling and break, increments in trunk diameter as well as reproductive phases like ower initiation, fruit setting and ripening. The growing cycle depends on plant genotype as well as on climatic conditions. Identical genotypes when grown under different conditions may show different developmental stages. To successfully manage both horticultural crops and fruit tree species at specic developmental periods is crucial to know their phenological cycles. The study of the sequence of all periodical events involved in a plant life cycle is called phenology (Volpe, 1992; z, 1993; Schwartz, 1999). Establishing Villalpando and Ru the beginning and end of every developmental phase and stage contributes to evaluate plant growth rates (Torres, 1995). The interval between two different phases is called phenological z, 1993). stage (Villalpando and Ru Several phenological indicators are used to monitor and evaluate plant development. The most signicant ones for fruit

158

D.M. Salazar et al. / Scientia Horticulturae 108 (2006) 157161

tree species are blooming time and fruit ripening. The interval between blooming and fruit set is one of the most important z, 1993). phenological stages (Villalpando and Ru In 1945 Fleckinger dened phenological stages as external physiological changes occurring at specic periods of time, which coincide with the natural growth cycle at each specic moment. Bleiholder et al. (1989) introduced a new nomenclature that described the phenological stages of both herbaceous and woody plants. The new system, the BBCH General Scale, unied previous codes that were specic to different botanical families into a general scale applicable to all plants. Stauss (1994) published a more detailed version of this scale. The new method is basically a decimal system that identies different developmental stages by a two-digit code. While the rst digit refers to its major stages using values between zero and nine, the second digit, also scaled from zero to nine, relates to its secondary stages. The nomenclature has already been used by several authors to classify different plant families: Zadoks et al. (1974) for cereals; Lancashire et al. (1991) for rape, bean and sunower; Meier et al. (1993) for beet; Hack et al. (1993) for potato; Meier et al. (1994) for stone and pip fruits, redcurrant and strawberry; Lorenz et al. (1994) for vine; Feller et al. (1995) for several et al. (1995) for citrus species, and Mart nezvegetables; Agust Calvo et al. (1999) for the Japanese loquat tree (Eribotrya japonica Lindl). The objective of this study was to describe the phenological stages of the guava tree (P. guajava L.) using the traditional nomenclature for fruit tree species described by Fleckinger (1945) and several other authors, and then to relate them to the worldwide currently used BBCH General Scale. And this is crucial since many phenological studies are still coded according to Fleckinger nomenclature. Even now, eld technicians and growers follow Fleckingers code to schedule the best timing for eld treatments. So that establishing a relationship between both phenological scales would provide valuable data that might contribute to expand the culture of this fruit tree species to areas other than its native habitats.

2. Materials and methods A guava orchard was selected to provide the plant material for the study. The orchard was located in Denia (Alicante, (753 m above Spain) at a specic location called Mount Mongo sea level). The orchard was planted on the southern slope 15 years ago grafting the cultivar Ruby (reddish pulp) onto guava seedlings. The soil showed a loam texture, and the orchard covered an area of 2.15 ha with a tree spacing of 5 m 5 m. The guava trees were drip irrigated with four drippers per tree (4 l/h each). A subtropical to tropical climate is typical of the area (Anon., 1986). The average rainfall for the 2-year study (2001 and 2002) was about 827 mm per year (8270 m3/hayear), with an average relative humidity of 67%. The average annual temperature was 17.04 8C, with mild winters and warm summers (average temperatures of 11.89 and 23.83 8C, respectively). The techniques of recording the phenological stages permitted the study of growth and development of vegetative and reproductive organs of different plant species, allowing the exact stage of evolution to be determined at any time during these physiological changes (Gil-Albert, 1989). Within the experimental plot, trees and branches were marked. Seven healthy trees were randomly selected, and one branch from each tree was studied and recorded. Then, three replicates of the experimental plot were conducted. In addition, all trees in the orchard were monitored to ascertain the predominant developmental stage. The rst visit to the orchard started on August the 1st of 2001. The frequency of the visits ranged from every two weeks to once a week, depending on how quickly the guava trees changed their phenology. With each visit to the orchard photographs were taken for later analysis. Due to the rapid physiologycal changes that occurred between budbreak and fruit enlargement, visits to the orchard were required every one or two days. From fruit growth to maturity it was sufcient to visit and photograph once a week. Guava fruit equatorial diameter (mm) was weekly measured with a Mitutoyo CD15DC Digimatic calipper (0.02 mm accuracy). The last visit to

Table 1 Phenological stages, phenological codes and duration of guava tree (threshold temperature: 12 8C) Phenological stages Winter bud Bud swelling Bud growth begins First leaves sprouting More leaves unfolded Leaves completely developed Appearance of ower buds Flower buds visible Flower petals elongating Sepals totally opened 50% open owers Petal fall Fruit setting Fruit growth (80% nal size) Fruit colour changing Fruit ripening Fleckinger code A B1 B2 C D2 D4 E1 E2 E3 E5 F G H1 I1 J K BBCH General Scale 00 01 02 11 15 19 51 55 57 59 65 67 71 78 81 89 Duration (days) 167 8.1 2 0.6 7 1.2 2 0.7 3 0.7 9 1.2 1 0.3 1 0.2 18 1.8 9 1.4 2.1 0.4 2 0.5 1 0.5 109 4.5 5 1.0 12 1.6 Duration (8C days) 5.5 0.86 43.5 8.4 11.0 2.3 21.0 2.8 62.8 7.9 10.2 1.6 18.3 2.7 170.1 14.5 105.0 13.9 24.0 5.1 24.5 5.1 13.2 5.2 1155.3 39.65 29.7 5.4 18.3 2.9 Accumulation (8C days ) 5.5 49 60 81 143.8 154 172.3 342.4 447.4 471.4 495.9 509.1 1664.4 1694.1 1712.4

Average values standard deviation.

D.M. Salazar et al. / Scientia Horticulturae 108 (2006) 157161

159

Fig. 1. Psidium guajava phenology.

160

D.M. Salazar et al. / Scientia Horticulturae 108 (2006) 157161

the orchard for measuring and recording took place after harvest on November the 20th of 2002. The duration of every phenological stage was measured in both days and degree days starting at the beginning of bud development. Degree days were calculated as the summation of the differences between mean daily temperatures and a base temperature of 12 8C (53 8F) at which guava bud development area. The use of degree days allows was promoted in the Mongo for comparisons to be made among different years and nez-Valero et al., 2001; Melgarejo geographical areas (Mart et al., 1997). The different phenological stages of plant and bud development as well as fruit growth were described and dened using the traditional nomenclature of Fleckinger (1945). In this system the general stages are designated by letters followed by a number between one and four to designate secondary ones. These stages were also related to the BBCH General Scale. 3. Results The different phenological stages as well as the phenological codes and duration of guava tree phenology are shown and described on Table 1 and Fig. 1. The pattern of development of individual buds from selected trees generally matched that of the whole orchard even though owering was dependant on the position and orientation of the branches on the tree. There was no appreciable difference between buds for the duration of the successive phenological stages. The experimental plot was denitively replicated. Each of the three replicates held seven healthy trees, so a total of 21 branches were monitored. The data in this study strictly refer to average values of monitored branches for every single experimental tree. Table 1 refers to the average values of every developmental area (Alicante, stage for the guava cultivar Ruby in the Mongo Spain). A: 00: Winter bud. The bud is greenish brown and completely closed. It is closely linked to the twig. B1: 01: Bud swelling. The bud swells and becomes greenish. B2: 02: Bud growth begins. The bud gets longer, and scales start opening. C: 11: First leaves sprouting. The rst leaf appears and becomes visible. D2: 15: More leaves unfolded. Not yet at full size. D4: 19: Leaves completely developed. Leaf growth completed. E1: 51: Appearance of ower buds. Calyx becomes visible. Internode lengthening stops. E2: 55: Flower buds visible. Sepals still closed. E3: 57: Flower petals elongating. Sepals slightly open, petals just visible. E5: 59: Sepals totally open. Sepals fully extended so that petals can open. F: 65: Full owering. At least 50% of owers open. First petals falling. G: 67: Petal fall. Flowers fading and most petals collapse.

Fig. 2. Guava fruit growth until full ripeness.

H1: 71: Fruit setting. Fruit size up to 10 mm. I1: 78: Fruit growth. Fruit increase up to 80% of nal size. J: 81: Fruit scolour changing. Beginning of ripening; fruit reaching its nal volume. Colour changing from green to yellowish pale green. K: 89: Fruit ripening. Fruit reached nal volume and become completely yellow. Releasing pleasant aroma, and fruit right for consumption. Guava growth was monitorised from fruit set to full maturity. Fig. 2 shows a double sigmoid curve similar to that of stone fruit. The cycle lasted 128 days, and three different stages were identied. The rst one went on for 56 days, and it was characterised by an exponential growth due mainly to fruit cell s, 1987); at the end of this period guava reached division (Garce an average fruit diameter of 29 mm. Stage II took place from 56 to 84 days after fruit set; guava growth clearly slowed down (up to 33 mm) because of cell division and enlargement reductions et al., 1992). Guava caused by endocarp hardening (Barcelo physiological maturity came 128 days after fruit set. The largest growth increments took place during stage III; these size increases obeyed to water and solutes accumulations within cell s, 1987). Guava reached a nal vacuoles (Coombe, 1976; Garce size of 59.6 mm. 4. Discussion et al. (1992), Araujo et al. (1997), According to Barcelo Mercado-Silva et al. (1998) and Selvaraj et al. (1999) guava growth shows a double sigmoid pattern. Likewise, Fig. 2 displays the same growth pattern for guava equatorial diameter (mm). Furthermore, Laguado et al. (1999) and Mercado-Silva et al. (1998) found that the stage from fruit set to guava physiological maturity lasted 119 and 130 days, respectively; Somarriba (1985a) also indicated that guava reaches maturity 90150 days after anthesis. As shown in Fig. 2, guava reaches its full maturity 128 days after fruit set, which perfectly agrees with previous results. Once the phenological stages of guava (P. guajava L.) are clearly identied, it will be easier to assess the best date to apply pesticides and growth regulators. A detailed phenology will provide precise information for treatment applications. In fact this is crucial when growth regulators are involved; the applications of these exogenous chemicals are more successful

D.M. Salazar et al. / Scientia Horticulturae 108 (2006) 157161

161

depending on plant physiological stages. Therefore this research will contribute to increase treatment efciencies. The major phenological stages shown in this study z (1991) in Me xico. completely agree with those found by Ru Moreover, and in contrast to the Mexican study, the current phenology is more elaborated since several sub-stages are also described. Finally, guava tree phenology is described here according to the traditional Fleckinger Code and to the new BBCH General Scale for the rst time. References
, M., Zaragoza, S., Bleiholder, H., Buhr, L., Hack, H., Klose, R., Stauss, Agust n de los estados fenolo gicos del R., 1995. Escala BBCH para la descripcio n Citrus). Levante Agr cola 332, 189199. desarrollo de los agrios (Ge tico nacional de Espan a. MAPA Madrid. Tomo III Anon., 1986. Atlas agroclima 819. Araujo, F., Quintero, S., Salas, J., Villalobos, J., y Casanova, A., 1997. n de nutrientes del fruto de guayaba (Psidium Crecimiento y acumulacio guajava L.) del tipo Criolla Roja en la planicie de Maracaibo. Rev. Fav. Agron. (LUZ) 14, 315328. Aspra Consultores, S.C., 1996. Estudio de Mercado Mundial de la guayaba. n Agropecuaria (ASERCA). Apoyos y Servicios a la Comercializacio , J., Nicola s Rodrigo, G., Sabater Garc a, B., y Sa nchez Tame s, R., 1992. Barcelo a Vegetal Ciencia y Te cnica. Pira mide, Madrid, pp. 412584. Fisiolog ddeke, P., Stauss, R., 1989. EinheiBleiholder, H., van den Boom, T., Langelu nologischen Stadien bei Kultur-und Schadpantliche Codierung der pha zen. Gesunde Panzen 41, 381384. ` res de la ramication du rameau dun Champagnat, P., 1965. Quelques caracte getaux ligneux. In: 96 Congres Societe Pomologique de France. an des ve pp. 933. Coombe, B., 1976. The Development of Fleshy Fruits. Ann. Rev. Plant Physiol. 27, 507528. Feller, C., Bleiholder, H., Buhr, L., Hack, H., Mess, M., Klose, R., Meier, U., nologischen EntwickStauss, R., van den Boom, T., Weber, E., 1995. Pha se. l.Zwiebel-. Wurzel-, knollenund Blattgemu se. lungsstadien von Gemu Nachrichtenblatt Deutsche Panzenschutzd 47, 193206. nologiques et repre sentations graphiques du Fleckinger, J., 1945. Notations phe veloppment des bourgeons de poiriers. In C.R. Congre ` s de Paris de de lAssociation franc aise pour lavancement des Sciencies. Bibliographical reference in Fruticultura de Coutanceau. 1971. Barcelona: Oikos-tau, p. 118. s, G.E., 1987. Estudio anato mico y de los procesos de crecimiento del Garce fruto del guayabo (Psidium guajava L.) Agron. Colomb. 4, 2330. a Gil-Albert, F., 1989. Tratado de arboricultura frutal, Aspectos de la Morfolog a del a rbol Frutal, third ed., vol. 1. Ediciones Mundi-Prensa, y Fisiolog Madrid, 104 pp. Hack, H., Gall, H., Klemke, T., Klose, R., Meier, U., Stauss, R., Witzenberger, A., 1993. The BBCH Scale for phenological growth stages potato (Solanum tuberosum L.) In: Proceedings of the 12th Dreijahrestagung European Geesellschaft, Kartoff, Paris, pp. 153154. rez, E., Alvarado, C., y Mar n, M., 1999. Caracter sticas Laguado, N., Pe micas y siolo gicas de frutos de guayaba de los tipos Criolla Roja sicoqu y San Miguel procedentes de dos plantaciones comerciales. Rev. Fav. Agron. (LUZ) 16, 382397.

n, M., Arenas de Moreno, L., Araujo, F., Castro de Rinco n, Laguado, N., Mar n, A., 2002. Crecimiento del fruto de guayaba (Psidium guajava C., y Rinco L.) del tipo Criolla Roja. Rev. Fav. Agron. (LUZ) 19, 273283. ddeke, P., Stauss, Lancashire, P.D., Bleiholder, H., van den Boom, T., Langelu R., Weber, E., Witzenberger, A., 1991. A uniform decimal code for growth stages of crops and weeds. Ann. Appl. Biol. 119, 561601. Lorenz, D.H., Eichorn, H., Bleiholder, H., Klose, R., Meier, U., Weber, E., 1994. nologische Entwicklungsstadien der Weinrebe (Vitis vinifera L. ssp. Pha vinifera) Codierung und Bescheribung nach der erweiterten BBCH-Skala. Viticulture Enol. Sci. 49, 6670. nez-Calvo, J., Badenes, M.L., Lla cer, G., Bleiholder, H., Hack, H., Meier, Mart U., 1999. Phenological growth stages of the loquat tree. Ann. Appl. Biol. 134, 353357. nez-Valero, R., Melgarejo, P., Salazar, D.M., Mart nez, R., Mart nez, J.J., Mart ndez, F., 2001. Phenological stages of the quince tree (Cydonia Herna oblonga). Ann. Appl. Biol. 139, 189192. rla nder, B., Weber, Meier, U., Bachmann, L., Buhtz, E., Hack, H., Klose, R., Ma nologische Entwicklungsstadien der Beta-Ru ben (Beta vulE., 1993. Pha garis L.). Codierung und Bescheribung nach der erweiterten BBCH-Skala mit Abbildungen. Nachrichtenblatt Deutsche Panzenschutzd 45, 3741. Meier, U., Garf, H., Hack, H., Hess, M., Kennel, W., Klose, R., Mappes, D., nologische Seipp, D., Stauss, R., Streif, J., van den Boom, T., 1994. Pha Entwicklungsstadien der kernobstes (Malus domestica Borkh. und Pyrus communis L.), des steinobstes (Prunus-Arten), der johannisbeere (RibesArten) und der erdbeere (Fragaria x ananassa Duch.). Codierung und Bescheribung nach der erweiterten BBCH-Skala, mit abbildungen. Nachrichtenblatt Deutsche Panzenschutzd 46, 141153. nez-Valero, R., Guillamo n, J.M., Miro , M., Amoro s, A., Melgarejo, P., Mart 1997. Phenological stages of the pomegranate tree (Punica granatum L.) Ann. Appl. Biol. 130, 135140. a-Velasco, M., 1998. Fruit Mercado-Silva, E., Benito-Bautista, P., y Garc development harvest index and ripening changes of guavas produced in Central Mexico. Postharv. Biol. Tech. 13, 143150. Morton, J.F., 1987. Fuits of warm climates. Creative Res. Syst. Inc. 91102. z, A., 1991. Caracterizacio n fenolo gica del guayabo (Psidium guajava L.) Ru sis de Maestr a en Ciencias. Colegio de Postgraduados, Montecillo, In: Te xico, 78 pp. Me Schwartz, M.D., 1999. Advancing to full bloom: planning phenological research for the 21st century. Int. J. Biometeorol. 42 (3), 113118. Selvaraj, Y., Pal, D., Raja, M., Rawal, R., 1999. Changes on chemical composition of guava fruits during growth and development. Indian J. Hort. 56 (1), 1018. rboles de guayaba (Psidium guajava L.) en pastizales. Somarriba, E., 1985a. A n de fruta y potencial de dispersio n de semillas. Turrialba 35 1. Produccio (3). rboles de guayaba (Psidium guajava L.) en pastizales. Somarriba, E., 1985b. A n de semillas. Turrialba 35 (4). 2. Consumo de fruta y dispersio Stauss, R., 1994. Compendium of growth stage identication keys for monoand dicotyledonous plants. Extended BBCH scale. Postfach, Basel: CibaGeigy AG. ISBN 3-9520749-0-x. xico, a. Editorial Trillas, S.A. de c. v. Me Torres, R.E., 1995. Agrometeorolog D.F. 154 pp. z, A., 1993. Observaciones Agrometeorolo gicas y su uso en Villalpando, J., Ru xico, 133 pp. la Agricultura. Editorial Lumusa, Me Volpe, C.A., 1992. Citrus Phenology. In: Proceedings of the Second International Seminar on Citrus Physiology. pp. 103122. Zadoks, J.C., Chang, T.T., Konzak, C.F., 1974. A decimal code for the growth stages of cereals. Weed Res. 14, 415421.