Larval Feeding Injury to Citrus Roots and its Relationship to Invasion by Soil-Borne Plant Pathogens
J. H. Graham
Citrus Research and Education Center
University of Florida, IFAS
Lake Alfred, FL 33850
Historical Perspective
As Diaprepes infestations grew in scope over the last two decades, production managers noticed that trees in lower and wetter areas of the groves were the first to decline. They furthermore observed, in certain cases, trees on Phytophthora-susceptible rootstocks, such as sour orange and Cleopatra mandarin, declined more rapidly than in adjacent groves on more Phytophthora-tolerant rootstocks, e.g., Swingle citrumelo. From these observations, some managers assumed that Phytophthora was contributing to the acceleration of decline and began augmenting their IPM program for Diaprepes with one or more fungicide applications.
In 1996 and 1997, a survey of weevil-affected groves confirmed that damaging populations of Phytophthora were associated with the larval feeding damage on structural roots of all commercial rootstocks (Graham et al., 1997). Inspection of excavated root systems revealed sloughing of root bark where Phytophthora spp. entered the wound sites created by larval feeding, referred to as root etching (Color Plate 1). Infection of the wounded bark led to girdling and collapse of roots from the crown of the tree outward. Large roots severely damaged by the weevil alone did not show sloughing of bark. Soon after this discovery, greenhouse studies confirmed that larval feeding on fibrous roots predisposed rootstock seedlings to greater infection by Phytophthora nicotianae, promoted higher soil populations of the pathogen and more severe fibrous root rot (Rogers et al., 1996).
Discovery of Phytophthora palmivora
Constant association of Phytophthora with root damage by larvae led to naming the interaction the Phytophthora-Diaprepes Complex (Graham et al., 1997). The potential importance of the complex in the decline of trees on different rootstocks prompted intensive survey of the east coast near Vero Beach and Ft. Pierce where trees were rapidly declining despite aggressive IPM of the weevil. Surveys identified a far more severe interaction of P. palmivora with Diaprepes than elsewhere where P. nicotianae was the predominant interacting pathogen. The damage caused by P. palmivora was often associated with poorly-drained, fine-textured soils and with the rootstocks normally tolerant of P. nicotianae, Swingle citrumelo and Carrizo citrange. In the more severe form, structural roots collapsed from what appeared to be moderate larval damage followed by aggressive spread of P. palmivora through the roots (Color Plate 1). Bark infection led to rapid collapse and a gummy residue in the bark. Because trees on Swingle citrumelo were more severely affected by the complex than surrounding groves on sour orange there was particular concern about young plantings on Swingle citrumelo that had replaced blocks on sour orange (Graham, 1998). Swingle citrumelo consistently supported higher soil populations of P. palmivora than adjacent blocks on Cleopatra mandarin and sour orange (Fig. 1). This was the initial indication that rootstocks of trifoliate orange hybrid origin might be more susceptible to this newly discovered Phytophthora spp.
Rootstock-Phytophthora spp. Interactions and Tolerance of the Complex
Because Swingle citrumelo and Carrizo citrange appeared vulnerable to attack by P. palmivora, the parent trifoliate orange, as well as known susceptible Cleopatra mandarin were the focus of a detailed study of their relative tolerance to the complex. The interaction of the two Phytophthora species and rootstocks was initially evaluated in the greenhouse. When seedlings were infested with 2 and 5 neonate larvae, damage of Cleopatra mandarin and trifoliate orange seedlings was similar indicating that tolerance to the complex was not based on a unique resistance of these rootstocks to larval feeding. After a range of feeding damage was established, the larvae were removed from the roots and the soil infested with Phytophthora spp. When roots were inoculated with P. nicotianae, subsequent root rot development increased with severity of feeding damage on susceptible Cleopatra but not on trifoliate orange which is highly resistant to this pathogen (Color Plate 2). Thus, tolerance to the P. nicotianae-Diaprepes Complex is based on resistance to the fungus after insect attack. In contrast, when larval-damaged roots of the two rootstocks were challenged with P. palmivora, infection and rot was as severe on trifoliate orange as on Cleopatra mandarin (Color Plate 2). Unlike P. nicotianae, P. palmivora was particularly damaging to the tap root which was also observed in the field survey where P. palmivora was present in high populations (>100 propagules/cm3 soil).
High susceptibility of Swingle citrumelo to the P. palmivora-Diaprepes Complex was confirmed when young trees were interplanted into a grove where P. palmivora was the predominant pathogen in poorly-drained soil high in organic matter, clay content, calcium and pH. These soil stresses in combination with pre-established Diaprepes damage readily broke down tolerance of Swingle citrumelo to P. palmivora root rot (Fig. 2). Root rot damage was only partially controlled by applications of Ridomil Gold under these highly favorable conditions for P. palmivora.
Thus, rootstock susceptibility to the complex depends on which Phytophthora spp. is present and whether the soil and water conditions are conducive to the fungus or to rootstock stress. In most situations, P. nicotianae is the predominant pathogen and Swingle citrumelo appears to perform acceptably as a replant in weevil-infested groves provided soil conditions are suited for this rootstock (e.g., sandy soil texture, well-drained, favorable pH, calcium status, etc.). When P. palmivora is present in poorly-drained soils, high in clay, pH and calcium, Diaprepes renders normally tolerant Swingle citrumelo and Carrizo citrange susceptible to the complex. Thus, tolerance of Swingle citrumelo to the complex is restricted to the ridge and certain flatwoods soils. Under adverse soil and water conditions, new rootstocks resistant to P. palmivora and tolerant of the complex must be sought.
Mechanisms of Rootstock Tolerance/Susceptibility and Damage Thresholds
Observations of feeding damage and subsequent infection of roots by the two Phytophthora spp. indicate that there is a threshold of feeding damage required before the complex develops. Feeding by the larvae creates wounds in root tissue that increase leakage of sugars and other compounds from damaged root cells. These compounds serve as attractants and a food source for Phytophthora spp. and thereby increase the levels and severity of root infection. No difference in resistance of commercial rootstocks to the larvae has been detected (Rogers et al., 2000). After larvae feed, the increase in leakage of compounds from wounded roots of trifoliate orange and Cleopatra mandarin is similar (Fig. 3). Feeding damage of Cleopatra mandarin leads to severe root rot by P. nicotianae above a threshold of root damage and exudation, whereas resistance of trifoliate orange to P. nicoitanae is maintained despite the wounding and greater availability of exudates for fungal growth (Fig. 3). Resistance compounds present in roots of trifoliate orange and the hybrid Swingle citrumelo counteract growth of P. nicotianae into root tissues and allow roots to readily heal and regenerate (Color Plate 1; Graham, 1995). These inhibitory compounds are less active against P. palmivora which infects roots of trifoliate orange at a higher rate than P. nicotianae (Widmer et al., 1998). The breakdown of resistance of both rootstocks to P. palmivora occurs at a substantially lower threshold of larval damage than for P. nicotianae.
Role of Fungicides in Control of the Complex
Selection of tolerant rootstocks for replanting Diaprepes-affected groves aids in management of future losses to the complex. For existing trees, fungicides in conjunction with careful water and fertilizer management have been utilized to maintain tolerance to Diaprepes and Phytophthora damage. Tolerance results when roots regenerate after damage by the complex. Fertigation maximizes efficiency of water and nutrient uptake by the new roots in well-drained soils. However, use of fertigation to regenerate roots in flatwoods is limited in poorly-drained soils and high water tables. In these situations, there is increased reliance on fungicides to control root damage by Phytophthora spp.
Potential for Ridomil Gold and phosphite-containing fungicides to control root infections of Phytophthora palmivora and P. nicotianae after larval damage was evaluated at the Kerr Center in Vero Beach, FL in Ruby Red grapefruit on Swingle citrumelo planted in 1987. Soils series are Winder, and Manatee that vary widely in sand, clay and organic matter when formed into raised beds. The site was infested with Diaprepes several years ago and for the last five years has been under an aggressive IPM program with biocontrol nematodes to control the root feeding larvae and adulticide and ovicide sprays to control the weevil above ground. Soils have restrictive drainage that promote very high populations (>40 propagules/cm3 soil) of both P. palmivora and P. nicotianae, particularly on Swingle citrumelo (Fig. 1). Soil surface application of fungicides were made in May and September of 1997 and 1998 with Ridomil Gold (2.25 g a.i./tree/application) and a phosphite salt (12.36 g a.i./tree/application) with an herbicide boom with 8 ft. band @ 40 gal/acre treated area.
In 1997, populations of P. palmivora and P. nicotianae exceeded 200 and 60 propagules per cm3 soil, respectively, before and after fungicide treatment. Ridomil Gold significantly increased the number of leaf flushes in the canopy and increased root mass density 30% by July. Phosphite treatment showed minimal responses. In the first season, Ridomil Gold increased yield and fruit size of grapefruit by 14% and 4%, respectively, compared to the untreated control. In June 1998, P. nicotianae increased to over 100 propagules per cm3 soil and by November 1998 P. palmivora rose to >300 propagules (Fig. 4). In no instance did fungicide treatments reduce propagules compared to the untreated control. In November, Ridomil Gold treated trees had greater fibrous root density that supported significantly higher propagules of P. palmivora. In 1998, Ridomil treatment increased yield of grapefruit by 45% compared to the control, but did not affect grapefruit diameter. However, overall yields dropped 90% from the previous year, indicative of the rapid decline of the trees in 1998.
In spring 1999, trees had declined to a stage where it was decided to remove the block. Canopy condition of each tree was rated on a scale of 1-3 where: 1= mild (slight thinning and chlorosis of leaves), 2 = moderate (canopy with some dieback of branches and most leaves showing moderate chlorosis), and 3 = severe (canopy stunted, twig dieback substantial, remaining leaves with severe chlorosis). After removal of the root system from the ground, necrosis on each tree in the trial was rated on 8-10 structural roots extending from the trunk plus distal roots down to 1 cm in diameter. On a scale of 1-3, 1 = 2-3 roots with weevil etching and Phytophthora induced necrosis and girdling of roots, 2 = 4-5 roots of the same condition, and 3 = 6 or more roots of the same condition. There was a close relationship (R2 = 0.81) between canopy decline and root condition. Damage by larvae was prominent on structural roots, but not heavy compared to other locations in the state where root damage from Diaprepes alone was assessed. Bark collapse caused by Phytophthora infections was severe enough to cause girdling of structural roots >0.5 in. diameter on most trees. There was no fungicide treatment effect on the condition of the structural roots.
This study confirms that severe infections by Phytophthora spp. follow larval damage from Diaprepes root weevil feeding on structural roots. P. palmivora is present in very high populations under conditions of fine-textured soils and restricted drainage. Tree decline is accelerated by excessive rainfall and wet soil conditions like those that occurred during El Nino. Also confirmed is that Phytophthora infection and girdling of roots contributes as much to the damage of the root system as larval feeding at advanced stages of decline. Based on population dynamics, P. palmivora may be more damaging to structural roots than P. nicotianae, although the level of both pathogens is usually high in these cases. Ridomil Gold at the full rate (1 qt./acre area/application) twice a year is effective for controlling both Phytophthora spp. resulting in an immediate improvement in tree vigor, root growth and higher yield even though tree health was declining. This paradox may be explained by the differential activity Ridomil Gold has in controlling fibrous root damage compared to larger roots. At advanced stages of the complex, Ridomil Goldmay not be effective enough to control Phytophthora-induced girdling of structural roots.