In 2015, soft citrus (easy peelers) made up 9335 ha of the 68,000 ha within the South African citrus industry and is expected to significantly increase in the next 10 years. Within this group, late mandarin account for 6560 ha and has earned growers in 2015 a gross income of more than R11,000 (South African Rand) per tonne (South African Citrus Growers Association, 2016). Any disease that reduces yield and fruit quality can, therefore, greatly affect the profitability of this high value cultivar. In South Africa, brown rot of fruit is primarily incited by Phytophthora nicotianae or Phytophthora citrophthora (Meitz-Hopkins et al., 2013). It is a disease that can severely reduce yield, fruit quality, or both in the orchard or in the postharvest cold chain (Adaskaveg et al., 2015; Montenegro et al., 2008). The disease is especially severe in areas where rainfall occurs during the late stages of fruit development and maturation (Adaskaveg et al., 2015).
Propagules of the aforementioned two pathogens are present in most orchard soils, from where they are readily splashed onto low-hanging citrus fruit. Sporangia form on the low-hanging fruit from where they can be splash-dispersed to fruit higher up on the tree (Graham et al., 1998; Timmer et al., 2000). Brown rot epidemics are further promoted by periods of prolonged wetness (more than 7 d) and temperatures ranging between 23 and 32 °C (Graham et al., 1998; Timmer et al., 2000). These conditions are often prevalent in the cooler, winter rainfall citrus production areas of South Africa. ‘Nadorcott’ mandarin trees are known to bear heavily, resulting in branches bending down under the fruit weight, with numerous fruit often hanging close to the orchard floor (J. Joubert, personal communication). This characteristic and the fact that it matures during June–August, when rain often occurs in the aforementioned production areas, leads to the increased risk of severe brown rot epidemics occurring in mandarin orchards.
Properly timed foliar applications with phosphonates have been shown to be an excellent preventative control measure for brown rot of citrus fruit and root rot incited by Phytophthora species (Graham, 2011). For brown rot control in South Africa, it is specifically recommended to be applied 1 month or less before harvest (Van Zyl, 2017). Phosphonates are easily absorbed by the leaves of citrus trees from where they are translocated through the phloem to sinks, such as developing fruit and roots (Graham, 2011; Ouimette and Coffey, 1990). At the sites where they accumulate, they have been shown to have a direct fungistatic effect on invading pathogens and activating the plant’s own defense mechanisms (Afek and Sztejnberg, 1988, 1989; Fenn and Coffey, 1984, 1985; Smillie et al., 1989).
This direct and indirect control action combined with a maximum preharvest interval of 28 d makes late-season phosphonate applications an attractive option for citrus growers who are expecting rain close to harvest that could trigger a brown rot epidemic incited by P. nicotianae (warmer production areas) or P. citrophthora (cooler production areas) (Hardman and Hattingh, 2016). However, an increasing number of reports were made by growers in cooler, winter rainfall, production areas of South Africa that they are experiencing phytotoxic damage to mandarin fruit when they applied phosphonates at late fruit developmental stages, when color development is advanced. As this was the first of the reports of such damage on mandarin fruit, further investigation was warranted.
Le Roux (2000) reported that foliar sprays of phosphonates can cause phytotoxic damage to citrus leaves and rapidly developing fruit in the late season if the application rates are high, as well as if spraying is carried out at high ambient temperatures or if the treated trees are under drought stress. However, investigation of the reports from growers indicated that label recommendations regarding application conditions, timing and dosages were strictly adhered to, thereby, eliminating these as possible causes for the observed damage. However, Walker (1989) reported incidences of phytotoxic damage to leaves of small, nonfruiting mandarin trees treated with foliar phosphonate sprays and that the damage increased with increasing dosages. Furthermore, Manrakhan et al. (2015) found similar damage on ‘Nadorcott’ mandarin fruit when spinosad-based bait sprays were applied for the control of fruit flies (Ceratitis sp.). In this study, it was found that damage only occurred on fruit that were at the immature green and color break stage. These findings, therefore, indicate a possible change in susceptibly due to changes occurring during maturation of the rind.
As stated previously, phosphonate foliar applications in the period close to harvest are highly effective for the control of phytophthora brown rot (Graham, 2011). The aim of this study was to verify and quantify any possible phytotoxic damage to ‘Nadorcott’ mandarin fruit caused by phosphonate foliar applications, aimed at phytophthora brown rot control, at various fruit developmental stages, over two seasons (2016 and 2017) in two orchards, located in climatically diverse production areas.
Adaskaveg, J.E., Hao, W. & Förster, H. 2015 Postharvest strategies for managing phytophthora brown rot of citrus using potassium phosphite in combination with heat treatments Plant Dis. 99 1477 1482
Afek, U. & Sztejnberg, A. 1988 Accumulation of scoparone, a phytoalexin associated with resistance of citrus to Phytophthora citrophthora Phytopathology 78 1678 1682
Afek, U. & Sztejnberg, A. 1989 Effects of fosetyl-Al and phosphorous acid on scoparone, a phytoalexin associated with resistance of citrus to Phytophthora citrophthora Phytopathology 79 736 739
Albrigo, L.G. 1972 Distribution of stomata and epicuticular wax on oranges as related to stem end rind breakdown and water loss J. Amer. Soc. Hort. Sci. 97 220 223
Agustí, M., Almela, V., Juan, M., Alférez, F., Tadeos, F.R. & Zacarías, L. 2001 Histological and physiological characterization of rind breakdown of ‘Navelate’ sweet orange Ann. Bot. 88 415 422
El-Otmani, M., Arpaia, M.L. & Coggins, C.W. 1987 Developmental and topo physical effects on the n-alkanes of Valencia orange fruit epicuticular wax J. Agr. Food Chem. 35 4246
El-Otmani, M. & Coggins, C.W. 1987 Fruit age and growth regulator effects on the quantity and structure of the epicuticular wax of ‘Washington’ navel orange fruit J. Amer. Soc. Hort. Sci. 110 371 378
Fenn, M.E. & Coffey, M.D. 1984 Studies on the in vitro and in vivo antifungal activity of fosetyl-Al and phosphorous acid Phytopathology 74 606 611
Graham, J.H. 2011 Phosphite for control of phytophthora diseases in citrus: Model for management of Phytophthora species on forest trees? N. Z. J. For. Sci. 41S S49 S56
Graham, J.H., Timmer, L.W., Drouillard, D.L. & Peever, T.L. 1998 Characterization of Phytophthora sp. causing outbreaks of citrus brown rot in Florida Phytopathology 88 724 729
Hardman, P. & Hattingh, V. 2016 Recommended usage restrictions for plant protection products on Southern African export citrus. Dec. 2016. Citrus Research International, Nelspruit, South Africa
Iglesias, D.J., Cercos, M., Colmenero-Flores, J.M., Naranjo, M.A., Rios, G., Carrere, E., Ruiz-Rivero, O., Lliso, I., Morillon, R. & Tadeo, F.R.M.T. 2007 Physiology of citrus fruiting Braz. J. Plant Physiol. 19 333 362
Knight, T.G., Klieber, A. & Sedgley, M. 2002 Structural basis of the rind disorder oleocellosis in Washington navel orange (Citrus sinensis L. Osbeck) Ann. Bot. 90 765 773
Le Roux, H.F. 2000 Physiological interactions of phosphorous acid and control of root pathogens. Proc. Intl. Citricult. IX Congr. II:926–928
Manrakhan, A., Stephen, P.R. & Cronje, P.J.R. 2015 Phytotoxic effect of GF-120 NF fruit fly bait on fruit of mandarin (Citrus reticulata Blanco cv. Nadorcott): Influence of bait characteristics and fruit maturity stage Crop Protection 78 48 53
Medeira, M.C., Maia, M.I. & Vitor, R.F. 1999 The first stages of pre-harvest ‘peel pitting’ development in ‘Encore’ mandarin. A histological and ultrastructural study Ann. Bot. 83 667 673
Meitz-Hopkins, J.C., Pretorius, M.C., Spies, C.F.J., Huisman, L., Botha, W.J., Langenhoven, S.D. & McLeod, A. 2013 Phytophthora species distribution in South African citrus production regions Eur. J. Plant Pathol.
Montenegro, D., Aguín, O., Pintos, C., Sainz, M.J. & Mansilla, J.P. 2008 A selective PCR-based method for the identification of Phytophthora hibernalis Carne Span. J. Agr. Res. 6 78 84
Muramatsu, N., Takahara, T., Ogata, T. & Kojima, K. 1999 Changes in rind firmness and cell wall polysaccharides during citrus fruit development and maturation HortScience 34 79 81
Schneider, H. 1968 The anatomy of citrus, p. 1–85. In: H.J. Weber and L.D. Batchelor (eds.). The citrus industry. Univ. California Press, Los Angeles, CA
Smillie, R., Grant, B.R. & Guest, D. 1989 The mode of action of phosphite: Evidence for both direct and indirect modes of action on three Phytophthora sp. in plants Phytopathology 79 921 926
South African Citrus Growers Association 2016 Key industry statistics for citrus growers 2016. South African Citrus Grower’s Assn., Hillcrest, South Africa
Timmer, L.W., Zitko, S.E., Gottwald, T.R. & Graham, J.H. 2000 Phytophthora brown rot of citrus: Temperature and moisture effects on infection, sporangium production, and dispersal Plant Dis. 84 157 163
Van Zyl, K. 2017 The chemical control of plant diseases in South Africa. AVCASA, Halfway House, South Africa