Experimental
In March 2013, an aberrant fructification was observed on the cacao (Theobroma cacao L.) accession CL 19/51 at St Augustine, Trinidad. Two mature fruits were observed on the same pedicel, instead of one fruit per pedicel (Fig. 1). The two fruits ripened together, attained normal dimensions and each had five loculi as usual. Fruit qualitative and quantitative traits used for characterization (Bekele and Butler, Reference Bekele, Butler, Eskes, Engels and Lass2000) were similar (Table 1). In April 2013, 24 individually stalked fruits, of varying maturity, were present on the tree. Four visits at 3-d intervals were then made. On each visit, mature opened flowers were examined in situ along a 150 cm cylindrical length of the trunk from above the graft and along a 50 cm cylindrical length on each of the two lowermost branches. The gynoecia of 15 flowers, randomly selected from the upper canopy, were also isolated and examined. All the 68 flowers from the trunk and lower branches showed a normal single-style/single-ovary/single-pedicel arrangement as did the 60 flowers from the upper canopy. Maximum temperatures of 32–34°C were recorded during floral counts in the field. The aberration was not observed on any of the 15 genetically distinct and adjacent trees, or on any of the other 326 trees in this field. The aberration has not been encountered on any of the 11,902 trees of over 2000 accessions at the International Cocoa Genebank, Trinidad.
Fig. 1 Fruiting and flowering patterns in Theobroma cacao L. (a)–(c) – Double fructification observed on the cacao accession CL 19/51; note the individual vascular strands merging into the central vascular supply of the single pedicel. (d) – Two mature unripe fruits from the same cushion observed on the cacao accession CRU 116; note the individual stalks. (e) – Immature individually stalked fruits observed on CL 19/51. (f) – Flowers and buds on two producing cushions observed on the trunk of CL 19/51. (g) – Mature, ripe individually stalked fruits, one fruit per cushion observed on the cacao accession CRU 64. Scale bar = 2 cm.
Table 1 Characterization of the fruits of the CL 19/51 accession of Theobroma cacao L
Discussion
A lone, rare, double fructification was observed on the cacao accession CL 19/51. Each fruit was similar to CL 19/51 in the International Cocoa Germplasm Database (Turnbull and Hadley, Reference Turnbull and Hadley2013) and in prior records of this accession (Table 1). Continual observations of the tree have so far not shown any similar aberration. Cacao exhibits cauliflory and compact, cymose inflorescences are present on the older wood of the main stem and fan branches, but not on recent flushes (Purseglove, Reference Purseglove1974). Over time, a thickened area (cushion) is formed in which floral primordia are initiated. The peduncle of the inflorescence is not apparent and each flower is individually stalked. Differing numbers of flowers and buds of varying maturity per cushion can be formed simultaneously on the same tree, even under differing environmental conditions and among different genotypes. Generally, one to three fruits are present per cushion, but as many as six fruits may be set on each cushion. Each fruit is attached to the tree by the pedicel of the flower, from which it developed, rather than by the peduncle of the inflorescence. However, multiple fruits developing on the same cushion are not fused to each other along the stigma, style, ovary or pedicel of the fertilized flowers.
A single-seeded fruit can become a double fruit if two seeds develop in the same ovary. However, this is inapplicable as a cacao fruit has 20–60 seeds (Purseglove, Reference Purseglove1974). Two distinct ovaries were involved in the observed double fructification since two independent placental strands were present (Fig. 1). Double fruits occur from flowers with two carpels (Philip, Reference Philip1933). Hence, the aberration observed in cacao, in this instance, probably resulted from two pistils on the same pedicel of a flower.
Double fruits are naturally observed in tropical and semi-tropical plants such as avocado (Persea americana), pineapple (Ananas comosus), double coconut (Lodoicea maldivica), Musa spp. and navel oranges (Citrus sinensis) as well as temperate plants such as apple (Malus spp.), cherry (Prunus avium; Philip, Reference Philip1933) and fig (Ficus carica; Çalişkan and Polat, Reference Çalişkan and Polat2012). Double fruit in cucumber occurred as two separate pistillate flowers with partially joined ovaries on a single peduncle (Klosinska et al., Reference Klosinska, Kozik and Wehner2006), but had dissimilarly sized fruits unlike the aberration observed here in cocoa. Double fruit in peach was due to (1) water stress from drought (Garcia, Reference Garcia1980; Patten et al., Reference Patten, Nimr and Neuendorff1989) or deficit irrigation (Larson et al., Reference Larson, DeJong and Johnson1988; Johnson et al., Reference Johnson, Handley and DeJong1992) and (2) high temperature during carpel differentiation (Johnson et al., Reference Johnson, Handley and DeJong1992). Water stress during the initiation of flower bud development was highly and significantly correlated with double fruiting in nectarine (Naor et al., Reference Naor, Stern, Peres, Greenblat, Gal and Flaishman2005). Double fruit in sweet cherry was related to high temperature (above 30°C) during sepal and petal differentiation (Beppu et al., Reference Beppu, Ikeda and Kataoka2001) or carpel differentiation (Philip, Reference Philip1933; Tucker, Reference Tucker1934), but there was a strong genetic influence (Roversi et al., Reference Roversi, Fajt, Monteforte, Folini and Panelli2008; Garcia-Montiel et al., Reference Garcia-Montiel, Serrano, Martinez-Romero and Alburquerque2010).
The double fructification in cacao, observed in March 2013, indicated that the flower was naturally pollinated in September to October 2012, since cacao requires 5–6 months from pollination to ripening (McKelvie, Reference McKelvie1956). Maximum temperatures had a mode of 33°C, a mean of 32.5 ± 0.2°C and ranged from 30–36°C in September 2012 in St. Augustine, while rainfall averaged 2.9 ± 1.2 mm (0–35 mm) with modal and total values of 0 and 89.6 mm, respectively (Reynold Stone and Premnath Bissoon, pers. commun.). Meteorological data collected at Piarco (9.65 km away from St Augustine) for the period 1985–2012 indicated that there were only 2 years with high temperature and low rainfall in September, namely 2002 (28.6°C and 55.5 mm) and 2012 (29.0°C and 77.8 mm) (Trinidad and Tobago Meteorological Services unpublished bulletins). Since the plant was immature in 2002, the combination of high temperature and particularly water deficit, in 2012, may be implicated in the aberrant floral morphogenesis that resulted in double fruit.
Another mitigating factor may be boron deficiency. Boron is required for flowering (Cakmak and Römheld, Reference Cakmak and Römheld1997), and boron deficiency is implicated in the fruiting abnormalities of grape (Scott, Reference Scott1944) and cacao (Wessel, Reference Wessel, Wood and Lass1985). However, each of the double fruit was normal, and double fructifications were not observed on the same or surrounding trees. Therefore, boron deficiency probably did not cause the observed double fruiting in cacao.
The double fructification on the CL 19/51 cacao tree probably arose from a chance effect since the aberration was unknown on any of the ca. 12,000 trees in the germplasm collection. Further studies are planned to determine whether heat stress and water deficit can induce double fructifications in cacao. Understanding the phenomenon is encouraged as increasing its frequency could possibly increase productivity.
Acknowledgements
We thank Prof. P. Umaharan, the Director of the Cocoa Research Centre, for his comments and support and Ms Sheeba Sreenivasan for reviewing the manuscript.
