Success in citrus production depends on the selection of suitable high-quality scion‒rootstock combinations, which at the same time are adaptable to a wide range of environmental conditions and tolerant to various pests and diseases. No condition is more serious in citrus than Huanglongbing (HLB) disease, a lethal vector-transmitted disease. The causal agent of the disease is the bacterium Candidatus Liberibacter asiaticus
), vectored by the Asian citrus psyllid (ACP), Diaphorina citri
]. Citrus trees infected with HLB present asymmetric foliar chlorosis, acidic fruits, a shortened life cycle, branch dieback, and eventually tree death [2
In Puerto Rico, HLB-ACP was first detected in 2001 in the Agricultural Experiment Substation (AES) of Isabela; the presence of the bacteria CLas
was first identified there in 2009 [2
], in commercial orchards of sweet orange [Citrus sinensis
(L.) Osbeck] and lemon (Citrus latifolia
), and in lemon orchards at AES of Juana Díaz [5
]. From 2012 to 2015, the island experienced a 39% reduction (i.e., 2556 tons to 1557 tons) in citrus production [8
]. In 2012 the citrus industry was ranked second among fruit commodities in PR, with over 7000 ha planted on 2800 farms (~700 producers), most of them located in the mountainous region of the island. Between 2013 and 2014, the citrus industry ranked third, with a net value of $
6 million as reported by the Department of Agriculture of Puerto Rico (DAPR) [9
]. Over 68 million fruits were produced during that year. However, since HLB and CLas
were identified, the disease has spread throughout the entire island and the citrus industry has experienced a steady drop in production, forcing farmers to abandon their land and/or switch to alternate crops, such as coffee or plantains, usually facing high economic losses [11
]. In addition, this decline in citrus production appears to be more severe in orange and mandarin orchards than in lime or lemon orchards [11
The HLB problem may be compounded by the higher susceptibility to certain fungal (i.e., Phythophtora
spp.) diseases that have been found in varietals grafted to Cleopatra mandarin rootstock (Citrus reshni
Hort. Ex Tan) [12
], which until recently (up to 2013) was the predominant rootstock used by farmers in PR [13
]. After 2013, three citrus rootstocks [i.e., Swingle citrumelo, Carrizo citrange, and HRS 812 (also known as US 812)] were highly recommended to farmers by Román-Pérez et al. [14
] after being evaluated for several years at different locations and with diverse scion‒rootstock combinations. These three rootstocks had shown great potential in mainland USA, although little was known of their potential for commercial production in PR. A study driven by Román-Pérez and González-Vélez [13
] found that the three rootstocks had similar horticultural responses to scions on Cleopatra rootstock. However, through the years, Cleopatra showed more susceptibility to P. citrophthora
with increasing tree mortality, and Swingle citrumelo and Carrizo rootstocks have shown some resistance to Citrus Tristeza virus (CTV) and the scion-HRS 812 rootstock exhibited 100% survival with CTV [13
Bowman and Rouse [15
] found that HRS 812 rootstock was highly productive in Florida with high-quality fruits, and exhibited tolerance to CTV. Albrecht and Bowman [16
] found in a laboratory trial that Carrizo and HRS-897 (also known as US 897) were tolerant to HLB, while HRS 812 was considered moderately tolerant to HLB compared to Cleopatra mandarin. The transmission of the HLB causal agent CLas was limited to the plant phloem, and was attributed primarily to ACP and, secondarily, to human-mediated transmission by grafting [17
Spann et al. [18
] attributed nutrient deficiencies to HLB, where infected plants had significantly lower values of the macronutrients calcium (Ca), phosphorus (P), and sulfur (S), and the micronutrients manganese (Mn), iron (Fe), and copper (Cu). Studies by Gottwald et al. [19
] indicated no effective response to insecticide application to reduce ACP population, nor to an enhanced nutritional program on two trials conducted with Valencia orange in Florida. In Brazil, even though infected trees were removed and intensive ACP management practices were performed, the HLB disease has spread exponentially, causing significant yield losses [20
]. Improved plant nutrition may help to slow down HLB disease progression in a tree, but will not cure them of HLB.
Scientifically-based fertilization data for overcoming damage caused by HLB is scarce. Accurate HLB detection requires DNA tests, since visual symptoms are similar to micronutrient deficiencies and other citrus diseases such as citrus variegated chlorosis, citrus cankers, etc. In terms of nutrition, most of the recommendations provided by local Agricultural Extension Services and the Puerto Rico Department of Agriculture are based on data and recommendations gathered from citrus growers from the mainland and Florida‒USA Cooperative Extension Service publications [11
]. However, significant differences exist in soil type, topography, and climate between Florida and Puerto Rico, and so the inherent limitations of such recommendations are a serious concern. For that reason, our objective was to evaluate the role of rootstocks on the performance of two HLB-infected mature citrus orchards established at AES in Isabela in overcoming the effect of this disease.
The ideal soil pH for citrus trees ranges from slightly acidic soil (6) to alkaline (8). Soil acidity (pH less than 6), as found in Coto soils in Isabela, is well known as a major factor resulting in low crop yields due to Al and Mn toxicity, low concentrations of Ca and Mg, and decreasing availability of other nutrients like P [30
]. Junior et al. [30
] emphasized most of the response of citrus to liming agents was due to a high demand for Ca, used to regulate many processes related to both growth and responses to environmental stresses [31
]. Also, liming with dolomitic limestone can satisfy the Mg demand.
Based on our results (Table 2
and data not shown (i.e., for Al, Bo, Cu, Fe, and Zn elements)), all the nutrients and elements were below the adequate ranges established by Mills and Jones [32
] for lime. Although, for Nova mandarin, lower N (i.e., expected—3.0–3.5% versus the present study at 2.3–2.6%) and P (i.e., expected—0.15–0.25 versus this study <0.15) values observed were suggested by Mills and Jones [32
] for mandarins.
When compared with previous results reported by Román-Pérez et al. [22
] for the same orchards, the Tahiti lime trees yielded twice the number of fruit (797 v. 424), while mean fruit weight was less than half what they observed (20.4 g v. 42.7 g). For Nova mandarin orchard, quite low fruit production (~11 fruit/tree) was obtained due to HLB, most of them dried with thick skin. It is well established that HLB affects fruit production, resulting in smaller, evergreen, and dried fruit with an undesirable shape [33
]. HLB can also cause severe tree deterioration until it dies [34
]. Tree mortality by April 2016 was 13% for Tahiti lime grafted to HRS 812, Carrizo, and Rough lemon rootstocks, and 25% for Nova mandarin tree on Rough lemon and Carrizo rootstocks. Unfortunately, final CLas
titers were not determined, as the values could have been a very useful parameter for further explaining rootstock performance.
Although the HLB caused some Tahiti lime tree mortality, Tahiti lime grafted to HRS 812 exhibited greater tree growth (height and diameter), developed greater canopy volume, and had higher tree efficiency as compared with trees on Cleopatra. However, studies driven by Piña et al. [35
] found the opposite response of Tahiti lime growing in Fluventic Haplustolls soils in Venezuela and grafted to 11 different rootstocks. Also, even though our study had 13% tree mortality for Tahiti lime trees after 2013, compared with data collected in 2012–2013 by Román-Pérez et al. [33
], there was a 3-fold increase in tree efficiency of Tahiti limes grafted to Carrizo, Cleopatra, HRS 812, and Rough lemon rootstocks in our study. In both studies, similar tree efficiency was found for limes on Swingle rootstock (~16.9 fruits m−3
). Meanwhile, in the Nova mandarin orchard, tree efficiency was less than 1.