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Home , Atemoya, Cherimoya

Yield and Quality Traits of also limits fruit set. Nitidulid (Carpophilus sp. and Urophorus sp.) Hybrids Grown in are the single most important polli- nators of atemoya flowers and other annonaceous crops (Nadel and Pena,~ Ricardo Goenaga1 and David Jenkins 1994). Fruit shape varies from conical to ovate; it has slight to pronounced surface protuberances, -to greenish- ADDITIONAL INDEX WORDS. tropical horticulture, tropical , soluble solids concentration, squamosa · A. cherimola yellow skin and contains 10 to 40 dark brown to black . Fruit pulp SUMMARY. As consumers seek healthy and more diverse food products, the demand is white, smooth textured, sweet with for tropical fruits has increased significantly during the last 15 years. There is a lack a custard-like consistency (Campbell of formal experimentation to determine the yield performance and fruit quality · A. cherimola and Phillips, 1980; Crane et al., traits of atemoya ( ) hybrids. Six atemoya hybrids 2013). The fruit is high in dietary (‘Bradley’, ‘Geffner’, ‘Priestly’, ‘Lisa’, ‘47-18’, and ‘75-9’) grown on an Oxisol soil were evaluated for 4 years at Isabela, PR. ‘Geffner’ and ‘Lisa’ had the highest fiber and C and can range in number of marketable fruit averaging 8542 fruit/ha, and the highest yield of weight from 200 to 900 g (Meadows marketable fruit, averaging 1507 kgÁhaL1; they did not differ from each other, but and Oswald, 2012). were greater than all other hybrids. Individual weight of marketable fruit was There is very little information significantly higher in ‘75-9’ and ‘Priestly’ which averaged 264.8 g. Significantly available on total production area of higher soluble solids concentration values were obtained from fruit of ‘75-9’, atemoya worldwide. The largest pro- ‘Bradley’, and ‘Geffner’ which averaged 23.8%; they did not differ from each other, ducer in the United States is , but were greater than all other hybrids. with annual production estimated at 50,000 lb and an average seasonal s consumers seek healthy and The atemoya grows well in trop- price of $4.00/lb (Mossler and more diverse food products, ical and subtropical climates from sea Crane, 2012). In the United States, A the demand for tropical fruit level to an elevation of 1000 m. It small orchards are known to have has increased significantly during the adapts to a wide range of soil types been established in , CA, and last 15 years with an estimated value including sandy or heavy soils; how- Puerto Rico. of production at $18 billion in 2009 ever, it does not withstand water- Commonly used hybrid cultivars (Food and Agriculture Organization logged soils particularly when it is for commercial production include of the United Nations, 2011). Be- grafted onto (Crane Geffner, Page, African Pride, and longing to the family, et al., 2013; Morton, 1987). In Flor- Bradley (Crane et al., 2013). Produc- the atemoya is an interspecific hy- ida orchards, atemoya budwood is tion of fully matured of these brid between the sugar apple (Annona usually grafted onto or hybrids is estimated to range from 75 squamosa) and the (Annona sugar apple rootstocks; however, the to 200 fruit/year (Crane et al., 2013). cherimola) (Nakasone and Paull, 1998). most commonly used rootstock in However, results from long-term rep- The sugar apple is indigenous to the Israel is the cherimoya (Campbell licated field trials to evaluate these and highlands of and , and and Phillips, 1994; Morton, 1987). other hybrids are very limited (Crane the cherimoya is widely distributed Poor fruit set is the key obstacle et al., 2013). The objective of this throughout tropical for the cultivation of atemoya. The study is to evaluate the yield perfor- (Marleretal.,1994).However,the atemoya flowers exhibit protogynous mance and fruit quality traits of six term atemoya has also been used dichogamy (female function precedes atemoya hybrids grown in an Oxisol loosely in the literature for Annona male function). This incompatibility typical of the humid tropics. hybrids resulting from 1) crosses be- problem results in incomplete polli- tween custard apple (atemoya · A. nation and the production of mal- Materials and methods reticulata), 2) cherimoya · A. reticu- formed fruit (Mossler and Crane, This study was conducted in lata, and 3) for hybrids in which either 2012). For this reason, hand pollina- Puerto Rico at the U.S. Department A. squamosa or A. cherimola is used tion is often necessary to achieve of Agriculture, Agricultural Research interchangeably as male or female par- profitable yields. Lack of Service Research Farm in Isabela ents. In this paper, we use the term ‘‘atemoya’’ as the collective term for all Units these Annona hybrids. To convert U.S. to SI, To convert SI to U.S., multiply by U.S. unit SI unit multiply by USDA-ARS, Tropical Agriculture Research Station, 2200 P.A. Campos Avenue, Suite 201, Mayaguez, 0.4047 acre(s) ha 2.4711 Puerto Rico 00680-5470 0.3048 ft m 3.2808 We thank Angel Marrero, Pablo Rios, and Tomas 3.7854 gal L 0.2642 Miranda for their excellent field assistance. 2.54 inch(es) cm 0.3937 Mention of trade names or commercial products in 25.4 inch(es) mm 0.0394 this publication is solely for the purpose of providing 0.4536 lb kg 2.2046 specific information and does not imply recommen- 1.1209 lb/acre kgÁha–1 0.8922 dation or endorsement of the U.S. Department of 28.3495 oz g 0.0353 Agriculture. 1 ppm mgÁkg–1 1 1Corresponding author. E-mail: ricardo.goenaga@ars. 6.8948 psi kPa 0.1450 usda.gov. (F – 32) O 1.8 F C(C · 1.8) + 32

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(Coto clay: clayey, kaolinitic isohyper- 2007). Soil ammonium and nitrate shown commercial potential in non- thermic Typic Hapludox). The soil has were determined by steam distillation replicated plots at the nursery. Before a pH of 5.68, 154 mgÁkg–1 ammonium- (Mulvaney, 2007). Originally, the transplanting, the soil was chisel –1 nitrogen (NH4-N), 6.2 mgÁkg experiment was also established at plowed to a depth of 90 cm. Planting –1 nitrate-nitrogen (NO3-N), 5.8 mgÁkg a second location in a clayey, mixed, holes of 1.5-ft depth were dug with an phosphorous (P), 63.5 mgÁkg–1 potas- isohyperthermic Aquic Haplohumults auger connected by a drive shaft to sium (K), 1192 mgÁkg–1 calcium Ultisol soil. However, a combination the power-take-off unit of a tractor. (Ca), 93 mgÁkg–1 magnesium (Mg), of this site having a very heavy, clayey On transplanting day, each grafted 39 mgÁkg–1 iron (Fe), 245 mgÁkg–1 soil and a prolonged wet period due received 11 g granular P provided (Mn), 2.80 mgÁkg–1 to heavy rainfall caused high mortal- in the form of triple superphosphate. (Zn), and 1.42% organic carbon. The ity among forcing us to end Within a replication, plots for each 95-year (1919–2014) mean annual research at this site. hybrid contained two trees spaced rainfall is 1649 mm and Class A Six-month-old trees of hybrids 4 m apart and 6 m between adjacent pan evaporation is 1672 mm. Mean ‘Bradley’, ‘Geffner’, ‘Priestly’, ‘Lisa’, rows in a triangular array, 168 trees/ monthly maximum and minimum ‘47-18’, and ‘75-9’ grafted onto acre. As an effort to identify hybrids temperatures are 29.8 and 19.9 C. ‘Lessard Thai’ sugar apple rootstock not needing artificial pollination, Soil samples were taken 2 months were transplanted to the field on 8 hand pollination was not performed before planting by taking 15 borings Aug. 2001 and were arranged in a in this study. This experiment was at a depth of 0–10 inches from each randomized complete block design surrounded by two guard rows of of the projected hybrid rows. Samples with four replications. ‘Bradley’ is custard apple seedlings. were air-dried and passed through one of the first named selections of Irrigation based on tensiometer a 20-mesh screen. Soil pH in water atemoya. ‘Geffner’ and ‘Priestly’ are readings was provided through drip and 0.01 M calcium chloride (1 soil : Israeli selections (Morton, 1987). irrigation with two 2-gal/h emitters 2 water) were measured with a glass ‘Lisa’ is ‘Libby’ cherimoya · ‘Red per tree spaced 1.8 m apart when the electrode. Exchangeable cations (po- Sugar’ sugar apple, ‘47-18’ and ‘75- soil water tension at a depth of 12 tassium, magnesium, and calcium) 9’ originated from controlled pollina- inches exceeded 50 kPa. Fertilization were extracted with neutral 1 N ammo- tion crosses of ‘Geffner’ atemoya · was provided every 3 months using nium acetate and determined by atomic ‘San Pablo’ A. reticulata, and ‘’ a 15N–2.2P–16.3K–1.8Mg fertilizer absorption spectroscopy (Sumner and cherimoya · ‘Felipe Canul’ A. retic- at a rate of 185 lb/acre. Herbicide Miller, 2007). was ulata, respectively. All material (glyphosate) for weed control was extracted with 1 N ammonium fluo- was obtained from Zill’s High Per- applied only in strips within the plant- ride and 0.5 N hydrochloric acid and formance Plants (Boynton Beach, ing row. Weeds between rows were determined using the ascorbic acid FL) and shipped air freight to Puerto controlled with a tractor mower. method (Benton, 2001). Organic car- Rico. ‘Lisa’, ‘47-18’, and ‘75-9’ are Harvests were initiated in Jan. bon was determined by the Walkley– atemoya hybrids developed in that 2006. At this time, experimental trees Blackmethod(NelsonandSommers, nursery by Mr. Gary Zill and have were 6 years old and producing fruit

Fig. 1. Representative fruit of six atemoya hybrids grown in Puerto Rico.

548 • August 2016 26(4) in sufficiently large numbers for com- mercial harvest and sale. At each

harvest, number and weight of mar- NS ketable and nonmarketable fruit were *** recorded. Deformed fruit and those solids (%) Total soluble weighing less than 150 g were con- sidered nonmarketable. Representa- tive fruit from each hybrid is shown in Fig. 1. Fruit totaling 10% of those harvested were used to determine Percent total soluble solids using a tempera- fruit (%)

ture-compensated digital refractome- non marketable ter (Pal-1; Atago, Tokyo, Japan) when the fruit ripened at room tem- perature (75 F), 5 d after harvest. After a 4-year harvesting period, the experiment was ended in Dec. 2009. NS NS

Analysis of variance was carried Individual fruit wt (g) out using the GLM procedure of SAS nonmarketable (version 9.1 for Windows; SAS In- stitute, Cary, NC). After significant F test at P = 0.05, means separation was performed using Tukey’s Studentized Individual range test. marketable fruit wt (g)

Results and discussion ) 1 Year, hybrids, and the year · L ha Á

hybrid interaction showed highly sig- Total fruit wt nificant effects (P £ 0.01) on all fruit (kg parameters measured in the study (Table 1). The only exception was ) total soluble solids, which did not 1 L

show a significant year effect. ha As expected, all hybrids exhibited Á (kg an overall increase in the number and fruit yield yield of marketable fruit as trees in- Nonmarketable creased in age (Table 2). However, the z ) magnitude of this response varied 1 among hybrids as expected by the L ha significant year · hybrid interaction Á fruit yield (kg

(Table 1). Years of heavy cropping Marketable were followed by lower production and yield of marketable fruit the following year for particular hybrids fruit (Table 2). Most probably, the high Total fruit load in some cultivars resulted (no./ha) in depletion of assimilates, which then caused an ‘‘off-year’’ because of light blooming as trees built up carbohy- drate reserves (Scholefield et al., 0.01 or 0.001, respectively, based on analysis of variance. = 0.05. fruit £ P P

1985). This was particularly the case (no./ha) = 0.8922 lb/acre, 1 g = 0.0353 oz. for ‘Geffner’ in 2007–08 and ‘Lisa’ –1 Nonmarketable ha and ‘75-9’ in 2008–09 (Table 2). Á

‘Bradley’ was the only hybrid showing z relatively stable marketable fruit pro- duction and yield. The fact that it did *** ** ** *** ** ** *** *** ** fruit not have a year of heavy cropping 2,477 3,130 5,022 448 258 622 0.03 0.01 17.8 4.2 (no./ha) supports the hypothesis of assimilate Marketable depletion in other hybrids. y

‘Geffner’ and ‘Lisa’ had the x highest 4-year mean for number and (0.05) H *** *** *** *** *** *** ***

yield of marketable fruit with values , **, ***Non significant or significant at · 1 Fruit/ha = 0.4047 fruit/acre, 1 kg NS Tukey’s honest significant difference test at Table 1. Yield and fruit quality traits of six atemoya hybrids planted in Puerto Rico.Hybrid Values are means of four replications and 4 years (2006–09). HSD Hybrid (H)Y z y ***x *** *** *** *** *** *** *** *** *** Year (Y) being significantly higher than for all GeffnerLisaBradleyPriestly 8,47747-1875-9 2,448 8,607Avg 3,737 13,515 2,604 2,721 3,281 6,419 21,992 4,766 573 2,253 1,409 15,026 5,729 1,250 4,548 4,310 1,605 4,857 478 1,022 3,971 857 9,314 568 580 727 2,430 278 941 187.4 55 207 2,183 117 756 377 192.7 77.7 912 775 208.3 844 1,317 252.2 211.5 91.6 277.4 88.3 221.6 61 94.7 89.1 43 95.6 89.5 57 23.3 13 46 31 19.2 42 24.0 18.5 18.8 24.1 21.6

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Table 2. Number and yield of marketable fruit of six hybrids of atemoya grown in Puerto Rico. Values are means of four replications. Marketable fruit (no./ha)z Marketable wt (kgÁhaL1)z Hybrid 4 yr 2006 2007 2008 2009 4 yr 2006 2007 2008 2009 Geffner 8,477 1,875 13,125 7,760 11,146 1,409 440 1,951 1,487 1,757 Lisa 8,607 3,802 5,885 19,323 5,417 1,605 944 959 3,541 977 Bradley 2,448 1,823 2,448 2,552 2,969 478 500 368 512 533 Priestly 3,737 52 2,448 4,167 8,281 857 27 482 1,158 1,760 47-18 2,604 1,302 2,500 5,312 1,302 568 338 475 1,189 272 75-9 2,721 5,365 2,552 2,708 260 727 1,533 568 721 85 Avg. 4,766 2,370 4,826 6,970 4,896 941 631 800 1,435 897 HSD (0.05)y 2,477 2,413 5,330 5,752 7,232 448 665 940 1,110 1,163 z1 Fruit/ha = 0.4047 fruit/acre; 1 kgÁha–1 = 0.8922 lb/acre. yTukey’s honest significant difference test at P = 0.05. other hybrids (Table 2). These two in a concomitant significant increase Significantly higher soluble solids hybrids had the highest number of in fruit yield. For example, ‘Geffner’ concentration values were obtained marketable fruit in 2 of the 4 years the produced over 30% more fruit than from fruit of ‘75-9’ and ‘Bradley’ experiment lasted. However, ‘Brad- ‘Lisa’ but there were no significant which averaged 24.0% (Table 1). ley’ had the lowest 4-year mean for differences in yield of marketable fruit Thesevaluesaresimilartothose number of marketable fruit and mar- between these two hybrids (Table 1). obtained by others (Chiang and ketable yield although values for this The larger number of fruit produced Liu, 2011; Paull, 1996). hybrid were not significantly different by ‘Geffner’ may have resulted in high In conclusion, six atemoya hy- from for ‘Priestly’, ‘47-18’, and ‘75- sink demand and smaller fruit. brids were evaluated for the first time 9’ (Table 2). Fewer fruit and lower fruit yield during 4 years of production. Hybrid Total number of fruit was signif- by ‘Bradley’, ‘Priestly’, ‘47-18’, and cultivars Geffner and Lisa produced icantly different among hybrids ‘75-9’ may have been the result of more marketable fruit and had higher (Table 1). ‘Geffner’ and ‘Lisa’ pro- protogyny (Crane et al., 2013; Mossler marketable fruit yield than the rest of duced a significantly higher number and Crane, 2012) or lack of natural the hybrids used in this study. of total fruit; they did not differ from pollinators (Crane et al., 2013). There each other, but were greater than all has been some success using nitidulid Literature cited other hybrids. There was no statisti- pheromones to attract pollinators into cally significant difference in the atemoya orchards, thereby increasing Benton, J.J. 2001. Laboratory guide for number of total fruit produced by fruit set (Nadal and Pena,~ 1994; Pena~ conducting soil tests and plant analysis. ‘Bradley’, ‘47-18’, ‘Priestly’, and et al., 1999). Preliminary work by the CRC Press, Boca Raton, FL. ‘75-9’ (Table 1). There were no sig- authors indicates that these commer- Campbell, C.W. and R.L. Phillips. 1980. nificant differences in marketable fruit cially available pheromones attract The atemoya. Univ. Florida, Florida Coop. production between ‘Geffner’ and nitidulid species responsible for polli- Ext. Serv., Inst. Food Agr. Sci., Fruit Crops ‘Lisa’ which averaged 8542 fruit/ha. nation in atemoya (Jenkins et al., Fact Sheet FC-64. Their production of marketable fruit 2013, 2015). was significantly higher than those of Individual weight of market- Campbell, C.W. and R.L. Phillips. 1994. The atemoya. Univ. Florida, Florida Coop. all other hybrids, which averaged able fruit averaged over hybrids was Ext. Serv., Inst. Food Agr. Sci., Fact Sheet 2877 fruit/ha (Table 1). As a percent- 221.6 g (Table 1). It is noteworthy HS-64. age of total fruit production, hybrid that the individual weight of mar- cultivars Geffner, Bradley, 47-18, and ketable fruit in ‘Geffner’ (187.4 g) Chiang, S.W. and P.S. Lu. 2011. Char- Lisa produced a significantly higher was significantly lower than those acteristics of growth and development of percentage of nonmarketable fruit for other cultivars supporting the atemoya fruits in Taitung, Taiwan. J. averaging 52% (Table 1). hypothesis that the large number Taiwan Soc. Hort. Sci. 57:9–17. Significantly higher yield of mar- of fruit produced by this hybrid Crane, J.H., C.F. Balerdi, and I. Maguire. ketable fruit was obtained by ‘Geff- resulted in smaller fruit. Individual 2013. Atemoya growing in the Florida ner’ and ‘Lisa’ in comparison with all weight of marketable fruit was signif- home landscape. Univ. Florida, Florida other hybrids; these yields did not icantly higher in ‘75-9’ and ‘Priestly’ Coop. Ext. Serv., Inst. Food Agr. Sci., differ between these cultivars, averag- with fruit weight values of 277.4 and Fact Sheet HS-64. Á –1 ing 1507 kg ha (Table 1). There 252.2 g, respectively. These weights Food and Agriculture Organization of the were no significant differences in mar- were significantly different from each United Nations. 2011. Intergovernmen- ketable fruit yield among ‘Bradley’, other and greater than that obtained tal Group on and Tropical Fruits. ‘Priestly’, ‘47-18’, and ‘75-9’, aver- for all the other hybrids. Individual Committee on Commodity Problems. –1 aging only 657 kgÁha . In spite of weight of nonmarketable fruit was Current situation and short-term out- ‘Geffner’ producing a significantly significantly higher (95.6 g) in ‘75- look. 5th session. Yaounde, Cameroon. higher number of total fruit than 9’ and lower (77.7 g) in ‘Geffner’ 8 Mar. 2016. .

550 • August 2016 26(4) Jenkins, D.A., A.R. Cline, B. Irish, and R. sarasota.ifas.ufl.edu/fcs/FlaFoodFare/ matter, p. 961–1010. In: D.L. Sparks Goenaga. 2013. Attraction of pollinators Atemoya.pdf>. (ed.). Methods of soil analysis. Part 3. to atemoya (: Annonaceae) in Chemical methods. Soil Sci. Soc. Amer., Puerto Rico: A synergistic approach using Mossler, M.A. and J. Crane. 2012. Florida Amer. Soc. Agron., Madison, WI. multiple nitidulid lures. J. Econ. Entomol. crop/pest management profile: Atemoya 106:305–310. and sugar apple. Univ. Florida, Florida Paull, R.E. 1996. Postharvest atemoya Coop. Ext. Serv., Inst. Food Agr. Sci., fruit splitting during ripening. Post- Jenkins, D.A., C. Millan-Hernandez, A.R. Document CIR 1417. harvest Biol. Technol. 8:329–334. Cline, T.C. McElrath, B. Irish, and R. ~ ~ Goenaga. 2015. Attraction of pollinators Mulvaney, R.L. 2007. Nitrogen: In- Pena, J.E., A. Castineiras, R. Bartelt, and to atemoya (Annona squamosal x Annona organic forms, p. 1123–1184. In: D.L. R. Duncan. 1999. Effect of pheromone cherimola Sparks (ed.). Methods of soil analysis. bait stations for sap beetles (Coleoptera: ) in Puerto Rico using com- Annona mercial lures and food attractants. J. Part 3. Chemical methods. Soil Sci. Soc. Nitidulidae) on spp. fruit set. Fla. Econ. Entomol. 108:1923–1929. Amer., Amer. Soc. Agron., Madison, Entomol. 82:475–480. WI. Scholefield, P.B., M. Sedgley, and D. Marler, T.E., A.P. George, R.J. Missen, ~ and P.C. Andersen. 1994. Miscellaneous Nadel, H. and J.E. Pena. 1994. Identity, McE. Alexander. 1985. tropical fruits, p. 200–205. In: B. Schaffer behavior, and efficacy of nitidulid beetles cycling in relation to shoot growth, floral (Coleoptera: Nitidulidae) pollinating initiation and development and yield in and P.C. Andersen (eds.). Handbook of Annona environmental physiology of fruit crops: commercial species in Florida. the avocado. Sci. Hort. 25:99–110. Environ. Entomol. 23:878–886. II. Subtropical and tropical crops. CRC Sumner, M.E. and W.P. Miller. 2007. Press, Boca Raton, FL. Nakasone, H.Y. and R.E. Paull. 1998. Cation exchange capacity and exchange Morton, J.F. 1987. Fruits of warm cli- Tropical Fruits. CAB Intl., Wellingford, coefficients, p. 1201–1230. In: D.L. mates. Media Inc., Greensboro, NC. UK. Sparks (ed.). Methods of soil analysis. Part 3. Chemical methods. Soil Sci. Soc. Meadows, J. and M.J. Oswald. 2012. Nelson, D.W. and L.E. Sommers. 2007. Amer., Amer. Soc. Agron., Madison, Atemoya. 1 Feb. 2016.

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