Ripening and post harvest behaviour of fruits of two Hylocereus species (Cactaceae)

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Postharvest Biology and Technology 17 (1999) 39 – 45 www.elsevier.com/locate/postharvbio Ripening and postharvest behaviour of fruits of two Hylocereus species (Cactaceae) Avinoam Nerd a, Feiga Gutman a, Yosef Mizrahi a,b,* a The Institutes for Applied Research, Ben-Gurion Uni6ersity of the Nege6, P.O. Box 653, Beer-She6a 84105, Israel b Department of Life Science, Ben-Gurion Uni6ersity of the Nege6, P.O. Box 653, Beer-She6a 84105, Israel Received 10 February 1999; accepted 26 May 1999 Abstract Fruit growth and ripening, and the effect on fruit quality of various storage temperatures, were studied with Hylocereus undatus and Hylocereus polyrhizus plants growing in Beer-Sheva (Israeli Negev desert) under greenhouse conditions. Fruit growth was sigmoidal with a strong decline in growth rate after the onset of peel colour change. The ﬁrst change in peel colour was recorded 24–25 days after anthesis in H. undatus and 26 – 27 days in H. polyrhizus. In both species, the peel turned fully red 4–5 days after the ﬁrst colour change (mean temperature for the study period was 26.6 92.1°C). The slow growth phase was characterised by a decrease in the proportion of peel and concomitant increase in that of pulp, increase in the concentration of soluble solids and soluble sugars and a decline in ﬁrmness and the concentration of starch and mucilage. The surge in acidity prior to colour change indicated the beginning of the ripening processes. For H. polyrhizus, which has a red – violet pulp, the increase in pulp pigment paralleled the development of peel colour. Fruits were non-climacteric, and when harvested at close to full colour, they retained market quality for at least 2 weeks at 14°C or 1 week at 20°C. Storage at 6°C is not recommended, because transfer from that temperature to room conditions caused fruits to lose their ﬁrmness and ﬂavour rapidly. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Hylocereus undatus; Hylocereus polyrhizus; Chemophysical changes; Gas production; Pitaya; Storage 1. Introduction known as red pitaya in Latin America, is a medium–large berry bearing large green or red Several species of climbing cacti of the genus scales (Nerd and Mizrahi, 1997). The peel is usu- ally red, and the pulp varies from purple–red to Hylocereus have recently been developed as fruit white. The pulp is delicate and juicy and contains crops (Barbeau, 1990; Reyes-Ramos, 1995; numerous small soft seeds. The plants are grown Mizrahi et al., 1997). The fruit of these species, in the open in tropical areas, but must be pro- tected from intense solar radiation and subfreez- * Corresponding author. Tel.: + 972-7-6461966; fax: + 972- ing temperatures when cultivated under 7-6472984. subtropical conditions such those prevailing in E-mail address: mizrahi@bgumail.bgu.ac.il (Y. Mizrahi) Israel (Mizrahi et al., 1997; Raveh et al., 1997). 0925-5214/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 5 - 5 2 1 4 ( 9 9 ) 0 0 0 3 5 - 6
40 A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 Fruits of cultivated species of Hylocereus are Since both clones were self-incompatible (Weiss picked at various stages of peel colour develop- et al., 1994), the nocturnal ﬂowers, which stayed ment, from ﬁrst appearance to full colour (Bar- open for 1 night only, were hand cross-pollinated beau, 1990; Reyes-Ramos, 1995). However little in the night with pollen of the other species. research has been done on fruit development or Pollinated ﬂowers were tagged to allow calcula- ripening and on the behaviour of the fruit during tion of the number of days elapsed from anthesis or after storage. Studies with yellow pitaya (Se- to various stages of fruit growth and lenicereus megalanthus), a related climbing cactus, development. show that the duration of fruit development de- pends on seasonal temperatures and that the 2.2. Fruit growth and ripening fruits reach the optimal ﬂavour close to full colour stage (Nerd and Mizrahi, 1998). This stage Length and mid-length diameter were measured is also the best time for harvest for short- or with a caliper during fruit development in four long-distance markets (Nerd and Mizrahi, 1999). fruits of each clone, set at the beginning of Au- With the objective of determining ripening gust 1997. Physicochemical parameters and criteria for Hylocereus undatus and Hylocereus ﬂavour were determined in fruits of both clones polyrhizus, we examined ﬂavour and a number of set between mid-July and mid-August of the same physicochemical parameters during the last stage year. Fruits were harvested at random at 3–4-day of fruit development. In addition, the effect of intervals between 25 and 41 days after anthesis storage temperature on fruit quality was deter- (DAA) for a total of six fruits per clone at each mined for fruits harvested close to full colour. date. At the ﬁrst date the fruits were either green or on the verge of ﬁrst colour; 8–10 days before the last date they were all fully red. 2. Materials and methods 2.1. Plant material and growth conditions 2.3. Storage Studies were conducted in 1997 and 1998 in an Fruits were picked in September 1998, either at orchard of climbing cacti grown in a ventilated ﬁrst colour stage or 2–3 days after appearance of greenhouse in Beer-Sheva (northern Israeli Negev ﬁrst colour (close to full colour). They were desert). The plants had been established from washed with tap water to remove the sugars ex- cuttings in 1992. Clone B of H. undatus (red peel creted from the scales during fruit development, and white pulp) and clone C of H. polyrhizus (red dried with tissue paper and distributed randomly peel and red–purple pulp; Weiss et al., 1994) were among three dark chambers held at 69 1.6°C, used for the study. Each clone sample consisted of 149 1.4°C or 20 9 1°C, and at 65–75% RH. Sixty nine plants. Spaces were 1.5 m within the row and fruits of each species were stored at each tempera- 2.5 m between rows. Plants were trained on a 1.5 ture. Physicochemical parameters and ﬂavour m-high trellis system for support, and the soil was were examined once a week, until the appearance a loamy loess. Since these plants cannot grow in of visible disorders such as scale wilting. Fruits Israel under full sunlight, about 50% shade was stored at 6°C were also analysed after 1 week of provided by black net. Average monthly tempera- further storage at 20°C. Five fruits were analysed ture and relative humidity during the study peri- at each sampling date. ods (July–October 1997 and the same months in 1998) ranged from 25 to 30°C and 49 – 87% RH, 2.4. Fruit analysis respectively. Plants were drip-irrigated once a week, to provide 5 l of water per plant in the Colour values of peel and pulp at the equator summer and 2.5 l in the winter. Fertiliser contain- of the fruit were determined with a Minolta ing 23% N, 3% P, 20% K at a concentration of 70 Chroma Meter CR-200 (Ramsey, NJ) and ex- mg l − 1 was applied with the irrigation water. pressed as hue angles (McGuire, 1992). Fruit ﬁrm-
A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 41 ness was determined at two opposite points on 3. Results and discussion the equator of each fruit with a penetrometer (Faccini, Alfonsine, Italy) ﬁtted with a 2.5-mm plunger. Peel and pulp were separated and 3.1. Fruit growth and ripening weighed, and a sample of each was weighed both when fresh and after drying at 70°C for In both H. undatus and H. polyrhizus, growth of determination of water content. The concentra- fruits attached to the vine exhibited a sigmoid tion of red pigment in H. polyrhizus pulp which pattern (Fig. 1). Peel colour was developed during belongs to the betacyanin group (Forni et al., the last phase which was characterised by a slow 1992), was determined in 1g samples obtained growth rate. First colour (area between the scales from the inner part of the pulp. Tissue was ho- turned faint red) appeared 24–25 DAA in H. mogenised in 80% ethanol and ﬁltered through undatus and 26–27 DAA in H. polyrhizus. Fruits Whatman paper no. 41. The ﬁltrate was mixed of both species turned fully red 4–5 days after ﬁrst with 0.1 M acetate buffer at pH 4.5, and ab- colour. Like the fruit dimensions, fruit fresh weight sorbance determined at 538 nm (umax) with a reached 80% of the ﬁnal maximum weight, before Uvikon 810 spectrophotometer (Kontron, Mi- appearance of ﬁrst colour (Fig. 2(A)). Signiﬁcant lano, Italy). The concentration of pulp pigments increase in pulp content (percent of fruit fresh was expressed as betanin using A538 (1%) =1120 weight) occurred several days before, and (Forni et al., 1992). Acid concentration was de- throughout colour change (Fig. 2(B)), while fruit termined from 10 g of pulp macerated in dis- ﬁrmness dropped to less than 1 kg cm − 2 in that tilled water and titrated with 0.05 M NaOH to time (Fig. 2(C)). During the ﬁnal stage, percentage pH 8.0. Ascorbic acid concentration was deter- of water in the peel decreased (more markedly in mined in extracts of fresh pulp by titration with H. undatus) while remaining almost constant in the 2,6-dichloro-indophenol (AOAC, 1990). Soluble pulp (Fig. 2(D)). Calculations based on data solids concentration (SSC) was measured with a refractometer (PR-100, Atago, Japan) in sap pressed from the pulp. The concentrations of total soluble sugars, starch, and mucilage were determined in dry samples of pulp according to a procedure previously reported (Nerd and Mizrahi, 1999). Flavour of fruits was assessed by a panel of ten on a hedonic scale with 1 indicating extreme dislike and 10 indicating strong liking. 2.5. Ethylene and CO2 production rates Fruits picked at ﬁrst colour and 3 and 6 days later (three per species at each date) were weighed and then enclosed individually in jars held at 20°C and under a light regime of 12 h ﬂuorescent light/12 h dark. A continuous air ﬂow at approximately 5 ml min − 1 was passed through the jar. Ethylene and CO2 concentra- tions in the efﬂuent air stream were analysed Fig. 1. Growth (length and diameter) during fruit development with a gas chromatograph (Varian 3300, Sugar- on the vine in H. undatus and H. polyrhizus. Values are land, TX) once a day. means 9SE (n = 4).
42 A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 Fig. 3. Colour changes in H. undatus (red peel and white pulp) and H. polyrhizus (red peel and red-violet pulp) during the last stage of fruit development. Values are means 9 SE (n =6). Fig. 2. Whole fruit fresh weight (A), percentage of peel or pulp of colour change was low in fruits of both species, in fruit by weight (B), ﬁrmness (C), and water percent (FW ranging from 7.0 to 11.4 mg 100 g − 1 fresh weight. basis) (D), during the last stage of fruit development in H. undatus and H. polyrhizus. Values are means 9 SE (n= 6). Changes in the concentration of soluble solids and a number of non-structural carbohydrate compo- presented in Fig. 2 show that during the slow nents of the pulp occurred during fruit develop- growth period (25– 41 DAA), pulp dry weight ment. Both soluble solids and soluble sugars increased signiﬁcantly from 36 to 62 g in H. concentrations increased signiﬁcantly during undatus and from 21 to 48 g in H. polyrhizus, colour development, reaching 16–17 and 8–9%, while peel dry weight (around 18 g in both species respectively, at full colour stage (Fig. 5(A, B)). at 25 DAA) decreased slightly by 4 g in that time. Since changes in the two parameters were highly Hence the peel although accounting for a high correlated, SSC appears to be a reliable indicator proportion of fruit weight 20 – 25 DAA, could not for maturity in the investigated species. The con- have been an important source of assimilates to centrations of starch and mucilage decreased in the developing pulp which presumably received relation to the accumulation of soluble sugars assimilates from the stem. The decreasing values of the peel hue angle during maturation (Fig. 3) reﬂect development of peel colour. In H. polyrhizus, which has a red – vi- olet pulp, the development of peel colour was accompanied by an increase in the content of water-soluble pigment in the pulp (Fig. 3). The maximum concentration of pigment (expressed as betanin) in fruits with fully red peel was 0.24 mg g − 1 fresh weight. Titratable acidity of pulp showed a short-lived surge at the start of colour change, followed by a decline later on to 30 mmol H + kg − 1 in H. undatus and 45 mmol H + kg − 1 in H. polyrhizus (equivalent to 0.22 and Fig. 4. Concentration of titratable acidity (FW basis) during 0.32% citric acid, respectively; Fig. 4). Ascorbic the last stage of fruit development in H. undatus and H. acid concentration of the pulp during the period polyrhizus. Values are means 9SE (n =6).
A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 43 and SSC and soluble sugars were high. The ratio of percentage of soluble sugars to acidity (in terms of citric acid) in such fruits was 40 in H. undatus and 22 in H. polyrhizus. Thus for both red pitayas, chemical changes during ripening, colour development and palatability were found to coincide, as reported for the yellow pitaya S. megalanthus (Nerd and Mizrahi, 1998). In the cactus pear (Opuntia ﬁcus indica), however, opti- mum eating quality was reached at ﬁrst colour stage (Nerd and Mizrahi, 1997). 3.2. Gas production Production of ethylene and CO2 in fruits har- Fig. 5. Concentration (FW basis) of soluble solids (SSC) (A), soluble sugars (B), starch (C), and mucilage (D), during the vested at various colour stages was low and did last stage of fruit development in H. undatus and H. not peak during 6 days at 20°C. The production polyrhizus. Values are means 9 SE (n= 6). rate of ethylene ranged from 0.025 to 0.091 ml kg − 1 h − 1 and that of CO2 from 0.52 to 0.78 ml (Fig. 5(C, D)). Maximal concentration of starch kg − 1 h − 1. Hence H. undatus and H. polyrhizus was less than half that of the soluble sugars in may be deﬁned as non-climacteric, similar to ripe fruit, and accumulation of soluble sugars other cactus fruit crops that have been investi- during ripening cannot be therefore attributed to gated, namely cactus pears (Opuntia species) and starch degradation alone. The two species differed yellow pitaya (S. megalanthus; Nerd and Mizrahi, with regard to timing of changes in chemical 1997, 1998). constituents and other maturation parameters which coincided with the timing of ﬁrst colour 3.3. Storage appearance. Organoleptic testing indicated that fruits were Fruits were picked close to full colour and most palatable 33– 37 DAA (Table 1). At that examined at the end of 3 consecutive weeks in stage they had turned fully red, acidity was low storage at different temperatures. Distinct disor- ders were observed at the end of week 2 for fruits Table 1 held at 20°C and at the end of week 3 for fruits Flavour rating of fruits of H. undatus and H. polyrhizus held at 14°C. Symptoms consisted of extreme harvested between 25 and 41 DAAa softening, difﬁculty in separation of peel from the DAA Flavour (rating) pulp, and wilting and browning of scales (these phenomena appeared usually together). The con- H. undatus H. polyrhizus centration of soluble solids and soluble sugars remained fairly constant throughout storage at all 25 1.3 db 1.4 d the storage temperatures (Table 2). High storage 29 3.7 c 3.3 c 33 5.7 b 7.0 a temperatures resulted in lower fruit ﬁrmness, wa- 37 6.5 a 6.4 a ter content, acidity and ﬂavour. The two species 41 5.8 b 5.3 b responded to storage in a similar manner, though fruits of H. polyrhizus tended to maintain a higher a Flavour was assessed by a panel of ten according to a level of acidity at 14 and 20°C. This higher acidity hedonic scale with 1 indicating extreme dislike and 10 indicat- ing strong liking. may explain the higher preference rating of H. b Mean separation within column at P50.05 by Duncan’s polyrhizus recorded under these conditions. Some multiple range test. of the fruits stored at 6°C were transferred at
44 A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 Table 2 Effect of storage temperatures on fruit attributes in H. undatus and H. polyrhizus a Storage Firmness Water loss SSC Soluble sugars Acidity mmol H+ Flavour (kg cm−2) (%) (%) (%) kg−1 (rating) °C Weeks H. undatus Initial 2.4 ab 14.0 a 6.6 a 93 a 6.2 a 6 1 2.4 a 1.8 c 13.6 a 6.6 a 62 b 5.2 a 6 2 2.3 a 2.8 c 13.7 a 6.7 a 61 b 5.9 a 6 3 0.3 b 5.8 a 13.7 a 6.7 a 65 b 5.9 a 14 1 2.4 a 2.7 c 13.3 a 6.0 a 37 c 5.9 a 14 2 2.0 a 4.4 b 12.2 a 5.4 a 17 d 2.8 b 20 1 1.8 a 4.2 b 13.4 a 6.2 a 16 d 2.6 b H. polyrhizus Initial 2.5 a 13.2 bcd 6.3 ab 93 ab 6.1 a 6 1 2.7 a 2.2 d 12.7 cd 5.2 b 100 a 5.8 a 6 2 2.4 a 4.0 c 13.0 bcd 6.3 ab 84 abc 6.4 a 6 3 0.4 c 5.4 a 14.5 a 5.4 b 81 bc 5.6 ab 14 1 1.8 b 2.5 d 13.4 bc 6.8 a 71 cd 6.9 a 14 2 1.5 b 4.5 bc 12.0 d 5.9 ab 51 e 5.3 ab 20 1 1.7 b 4.9 ab 13.9 ab 6.8 a 58 de 4.4 b a Fruits were harvested close to full colour and analysed prior to appearance of distinct disorders such as extreme softening and scale wilting. Values are means 9 SE (n= 5). b Mean separation within column at P50.05 by Duncan’s multiple range test. different times to 20°C and their attributes exam- Acknowledgements ined 1 week later (data not shown). Fruits trans- ferred at the end of week 1 were similar to those The authors thank the Fleischer Foundation and stored immediately after harvest for 1 week at 20°C the Israel Ministry of Agriculture for a partial (Table 2). However fruits transferred to 20°C at the ﬁnancial support, Dorot Imber for editing the end of week 2 or 3 at 6°C became soft ( B 0.3 kg manuscript and Josef Mouyal and Eyal Naus for cm − 2), had high water loss (8 – 11%), low acidity their technical assistance. (B 25 mol H + kg − 1) and poor ﬂavour ( B2.5). Fruits of H. undatus developed chilling injury symptoms such as wilting and darkening of the References scales and browning of the outer layer of the pulp AOAC, 1990. Ofﬁcial Methods of Analysis, 15th ed. Associa- upon transfer to 20°C after 2 weeks at 6°C. tion of Ofﬁcial Analytical Chemist, Arlington, VA. To summarise, fruit harvested close to full colour Barbeau, G., 1990. La pitahaya rouge, un nouveau fruit kept their visual acceptance, i.e. marketing quality exotique. Fruits 45, 141 – 147. for at least 3 weeks at 6°C, 2 weeks at 14°C or 1 Forni, G., Polesello, A., Monteﬁori, D., Maestrelli, A., 1992. High-performance liquid chromatographic analysis of the week at 20°C. Fruits stored at 6°C maintained their pigments of blood-red prickly pear (Opuntia ﬁcus indica). eating quality (ﬂavour) for a longer period but lost J. Chromatogr. 593, 177 – 183. quality rapidly when transferred to room tempera- McGuire, R.G., 1992. Reporting the objective colour measure- ture. The effect of harvesting at an earlier ripening ments. HortScience 27, 1254 – 1255. Mizrahi, Y., Nerd, A., Nobel, P.S., 1997. Cacti as crops. Hort. stage (ﬁrst colour) on fruit quality during or after Rev. 18, 292 – 320. storage should be examined with a view to extend- Nerd, A., Mizrahi, Y., 1997. Reproductive biology of fruit ing the shelf life of these pitayas. cacti. Hort. Rev. 18, 322 – 346.
A. Nerd et al. / Posthar6est Biology and Technology 17 (1999) 39–45 45 Nerd, A., Mizrahi, Y., 1998. Fruit development and ripening shade. Sci. Hort. 53, 115 – 122. in yellow pitaya. J. Am. Soc. Hort. Sci. 123, 560–562. Reyes-Ramos, V., 1995. El Cultivo de las Pitahayas y sus Nerd, A., Mizrahi, Y., 1999. The effect of ripening stage on Perspective de Desarrollo en Mexico. Reyes-Ramos, fruit quality after storage of yellow pitaya. Postharvest Tabasco, Mexico. Biol. Technol. 15, 99–105. Weiss, J., Nerd, A., Mizrahi, Y., 1994. Flowering behavior Raveh, E., Nerd, A., Mizrahi, Y., 1997. Responses of two and pollination requirements in climbing cacti with fruit hemiepiphytic fruit-crop cacti to different degrees of crop potential. HortScience 29, 1487 – 1492. .