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© 2007 Plant Management Network.
Accepted for publication 15 March 2007. Published 26 July 2007.


Temporal Dynamics of Septoria Leaf Spot of Blueberry and its Relationship to Defoliation and Yield


Peter S. Ojiambo, International Institute of Tropical Agriculture (IITA), Oyo Road, PMB 5320, Ibadan, Nigeria; and Harald Scherm and Phillip M. Brannen, Department of Plant Pathology, University of Georgia, Athens 30602


Corresponding author: Peter S. Ojiambo p.ojiambo@cgiar.org


Ojiambo, P. S., Scherm, H., and Brannen, P. M. 2007. Temporal dynamics of Septoria leaf spot of blueberry and its relationship to defoliation and yield. Online. Plant Health Progress doi:10.1094/PHP-2007-0726-05-RS.


Abstract

In field trials on Premier rabbiteye blueberry in Georgia, onset of Septoria leaf spot (caused by Septoria albopunctata) occurred between late April and mid-June. Average disease severity increased sigmoidally until late September, after which it declined due to the abscission of severely affected leaves. Disease severity was highest on early-emerging leaves and on those located on shoots closer to the ground. Pycnidiospore inoculum was present throughout the season, and leaves became infected by S. albopunctata season-long. Disease severity, defoliation, flower bud set, and next season’s yield were interrelated; severely affected leaves abscised earlier in the fall than those with low disease severity, and shoots with severely diseased leaves and/or high levels of defoliation had reduced flower bud set. Furthermore, such shoots consistently had low yields the following year. The results form the basis for identifying disease levels that can be tolerated during specific periods of crop development without negatively impacting flower bud set and yield.


Introduction

Georgia ranks between fourth and fifth in the production of cultivated blueberries in the United States. Production is centered in the southeastern parts of the state, where both rabbiteye (Vaccinium virgatum) and, on a smaller but rapidly increasing scale, southern highbush (V. corymbosum hybrids) cultivars are grown (18).

In a producer survey focusing on blueberry production problems in Georgia, about 50% of growers reported that leaf spots were moderately or highly important constraints (18). A subsequent field survey documented that leaf diseases are prevalent on both rabbiteye and southern highbush cultivars, and that Septoria leaf spot, caused by Septoria albopunctata, is the most commonly encountered leaf disease in the region (17). Symptoms of Septoria leaf spot consist of small, circular leaf lesions with white to tan centers and purple margins (Fig. 1). The fungus overwinters asexually in stem lesions and in leaf litter on the ground (12).


 

Fig. 1. Symptoms of Septoria leaf spot on Premier rabbiteye blueberry (left) and Star southern highbush blueberry (right). Note the typically larger lesion diameter on the southern highbush cultivar (17).


Leaf spot diseases constitute about 30% of the total disease-related blueberry losses in Georgia (23). Given the high prevalence of Septoria leaf spot in the state (Table 1), it is likely that a large proportion of these losses is due to infection by S. albopunctata. However, no studies have been conducted to quantify the effects of Septoria leaf spot on yield, and data on the incidence and severity of foliar diseases is needed to quantify the relationship between yield and disease intensity. There is also a lack of basic epidemiological information for S. albopunctata, such as data on disease progression and inoculum dynamics. As a result, current management practices rely primarily on calendar-based fungicide applications after harvest of the crop in summer and early fall, incorporating only limited information about pathogen biology and disease ecology.


Table 1. Prevalence of Septoria leaf spot symptoms on selected rabbiteye (RE) and southern highbush (SH) blueberry cultivars, based on a disease survey in Georgia in 2002 and 2003 (Brannen, Scherm, and Krewer, unpublished).

Cultivar Type 2002 2003
Disease
prevalence

(%)
n Disease
prevalence
(%)
n
Brightwell RE 73.3 15 62.5 16
Climax RE 22.2 18 25.0 20
Powderblue RE 40.0 10 50.0 10
Premier RE 40.0 10 42.9 14
Tifblue RE 37.5 16 57.9 16
Bluecrisp SH  —x  0 62.5  8
O’Neal SH 0  4  —x  0
Star SH 100  5 75.0 12

 x Not included.


A first step in elucidating the epidemiology of any plant pathogen is to characterize the temporal disease progress on its host. In the Septoria-blueberry pathosystem, this has not been done previously. Key information as to when disease onset occurs and how fast the epidemic progresses on leaves that emerge at different times during the season can guide management decisions, for example the number and timing of fungicide sprays. Knowledge of the seasonal dynamics of inoculum, also unavailable for Septoria leaf spot, can help explain temporal disease progress.

On blueberry, as on many other deciduous fruit crops, it is advantageous to retain leaves late into the fall to enhance the ability of the plants to generate next season’s flower buds (6), thereby increasing next season’s yield (referred to as return yield henceforth) (10,24). This indicates that leaf diseases that cause premature defoliation during summer and fall need to be controlled effectively during this period. Recent fungicide efficacy trials showed that untreated plots with severe levels of Septoria leaf spot had the highest levels of fall defoliation (1,2,5). However, there is no quantitative information on how the temporal dynamics of disease affects the timing and magnitude of premature defoliation.

In mechanical defoliation experiments on rabbiteye (10) and southern highbush blueberry (24), premature leaf loss resulted in reduced flower bud set and decreased return yield. If Septoria leaf spot does induce premature defoliation, it is very likely that this disease-induced leaf loss will also negatively affect these two yield variables. However, no research has been carried out to determine the quantitative effects of Septoria leaf spot severity on flower bud set and return yield. Studies on the effect of disease on yield variables are critical to derive disease severity or defoliation thresholds above which yield losses are likely to manifest themselves.

The overall goal of this study was to fill critical knowledge gaps regarding the epidemiology of Septoria leaf spot as a basis for improved management of the disease. Specific objectives were to: (i) characterize the temporal progress of the disease and determine the effects of inoculum dynamics and selected leaf attributes on disease progression; (ii) determine the relationship between disease severity and premature defoliation, and establish how the temporal dynamics of disease affect the timing and magnitude of defoliation; and (iii) quantify the effect of Septoria leaf spot on flower bud set and return yield. The conceptual framework for this study, showing the interactions among these objectives, is presented in Fig. 2.


   
 

Fig. 2. Conceptual framework illustrating our hypotheses regarding the relationship among disease and yield-related variables in the Septoria leaf spot pathosystem on blueberry. Disease severity is affected by leaf location on the shoot and shoot location within the canopy, all of which influence the timing of defoliation in the summer and fall. Reproductive development in the fall and winter (flower bud set) and the following spring and summer (return yield) is affected via reductions in healthy leaf area and via the negative effects associated with premature defoliation.

 

General Methodology

The experiments reported here were carried out on the susceptible cultivar Premier in a mature rabbiteye blueberry planting at the University of Georgia Horticulture Farm near Athens from fall 2001 to fall 2004. Plants remained untreated with fungicides throughout this entire period. Experimental units consisted of individual 20-cm shoot segments selected early in the season and monitored regularly for growth and leaf emergence (primarily in the spring), number of Septoria leaf spot lesions on individual leaves (spring through fall), defoliation (summer and fall), flower bud set (in the winter), and return yield (in the following summer) (13,14,15). Rain-dispersed pycnidiospore inoculum was monitored with funnel traps located near the crown of the plants.

The resulting data set was subjected to various types of analyses. Disease progress curves, based on lesion density data from individual leaves, were plotted and compared for leaves with different attributes (i.e., leaves on the upper half of the shoot vs. those on the lower half; shoot segments in the lower canopy vs. those in the upper one) (14). The numbers of pycnidiospores present during different leaf phenology windows (primarily in relation to the time when leaves were completely unfolded) were summed up and correlated with lesion density to determine empirically whether leaves are infected preferentially when they are young, as has been suggested previously (7). Survival analysis (19) was applied to determine how lesion density and plant attributes (leaf position on the shoot and shoot position in the canopy) influence the timing and magnitude of premature defoliation (13). Patterns in the relationships among lesion density, flower bud set, and return yield were interpreted graphically with box-whisker plots and statistically using the Kruskal-Wallis test (15).


Temporal Progress, Inoculum Dynamics, and Infection Windows

Symptoms of Septoria leaf spot were first observed between the end of April (2002) and mid-June (in both 2003 and 2004). Disease severity increased sigmoidally during the summer to reach an average maximum lesion density by late September of 60 spots per leaf in 2002 and 2003 and 16 spots in 2004; thereafter, average lesion density per leaf decreased due to the abscission of the most severely affected leaves. Lesion density at the end of the assessment period in November (referred to as final lesion density henceforth) was correlated negatively with leaf position on the shoot and with shoot position in the canopy, indicating that lower (older) leaves on a shoot and those on shoots in the lower canopy had higher disease levels (14).

Pycnidiospore inoculum was present throughout the season, and final lesion density correlated most strongly (r = 0.21 to 0.44; P < 0.05 in all 3 years) with the cumulative number of S. albopunctata pycnidiospores dispersed from the time when leaves were fully unfolded until the end of the season; correlations with cumulative spore numbers during shorter temporal windows (particularly those during the period of leaf expansion) were weaker and/or not significant (14), indicating that multiple cycles of infection occur on leaves season-long, rather than leaves becoming infected preferrentially when they are young (7).


Relationship Between Disease and Leaf Abscission

Low levels of leaf abscission were observed before the end of August; this was followed by a rapid increase in defoliation until the end of the assessment period, at which time >80% of the leaves had dropped (Fig. 3). Final density of Septoria leaf spots was highest for leaves that abscised early and lowest for leaves that had not dropped by the end of the assessment period. Leaves with intermediate values of time to abscission also had intermediate levels of disease (13).


 

Fig. 3. Temporal progress of defoliation of Premier rabbiteye blueberry in field trials in Athens, Georgia in 2002 (solid circles) and 2003 (open circles).

 

Survival analysis indicated that lesion density (Table 2) and leaf position on lower vs. upper sections of the shoot significantly affected the risk of defoliation (P < 0.0001), whereas shoot location in lower vs. upper parts of the canopy had an inconsistent effect (13). On average, leaves with greater than or equal to 5 spots per leaf at the time of fruit harvest in mid-June abscised about 3 weeks earlier than those having less than 5 spots at the same time (Table 2).


Table 2. Mean times to defoliation (T) of individual leaves of Premier rabbiteye blueberry in field trials in Athens, Georgia in 2002 and 2003 as determined with survival analysis (13).

Lesion
density
class
a
2002 2003
n T (days)b Pr > χ2 n T (days) Pr > χ2
<5 spots/leaf 173 87.9 ± 1.61 < 0.0001 423 64.3 ± 1.32 < 0.0001
≥ 5 spots/leaf 210 68.4 ± 2.01 36 42.6 ± 4.12

 a Septoria leaf spot lesion density at the time of fruit harvest in mid-June.

 b Values are means ± standard errors. Counting for T began on 25 August 2002 and 28 August 2003, which marked the transition from a period of negligible, sporadic leaf loss to the onset of more sustained levels of defoliation (Fig. 3).


The ability of foliar diseases to incite premature defoliation has been documented for a number of fruit crop pathosystems (16,20). In deciduous fruits, a large proportion of leaf carbohydrates and nitrogenous compounds move into the woody parts of the trees during autumnal senescence (4). These reserves play an important role in early growth of shoots and fruit the following spring (9). In mechanical defoliation experiments (10,24), partial or complete premature defoliation inhibited flower bud set and resulted in lower fruit yields of blueberry in the next season. Thus, the disease-induced premature leaf loss associated with Septoria leaf spot epidemics is likely to lead to reduced vegetative and reproductive growth and development in blueberry crops.


Relationships Among Disease, Flower Bud Set, and Return Yield

An examination of plots of flower bud numbers or return yield versus final lesion density the previous fall revealed considerable scatter in the data (results from 2001/2002 shown in Fig. 4). Specifically, whereas shoots with high disease levels always had low flower bud numbers or yields, those having low disease levels had highly variable bud numbers or yields in the following season. The lack of a simple statistical relationship should not be surprising, given that numerous biological and environmental factors (3,6) in addition to disease can affect flower bud set and return yield in fruit crops. Even in annual crops, relationships between disease and yield variables are often weak due to the complex interactions between these factors (21,22). In perennial fruit crop pathosystems, factors such as nutritional status and biennial bearing pattern complicate the relation between disease and yield even further (3,8,11,16).


 

Fig. 4. Relationship between Septoria leaf spot severity in the fall of 2001 and flower bud numbers (top) and yield (bottom) in 2002 on shoots of Premier rabbiteye blueberry in a field trial in Athens, Georgia. Disease severity is expressed as the number of spots per leaf prior to defoliation of that leaf and averaged for all leaves on a given shoot.

 

Despite this overall variability, a negative relationship between flower bud set and disease was evident from box-whisker plots showing the distribution of final lesion density values for shoots having different numbers of flower buds (Fig. 5). For return yield, scatter plots indicated a drop in return yields as lesion density reached about 50 to 60 spots per leaf (15). When shoots were grouped into two severity classes having less than 60 and greater than or equal to 60 spots per leaf on average, mean return yield was higher for the former class (19.1 g per 20-cm shoot segment, n = 88) than for the latter one (9.5 g, n = 62). Based on a Kruskal-Wallis test, the null hypothesis of no significant difference between the distributions of return yields between the two lesion density classes was rejected (chi square = 18.5, P < 0.0001). Thus, there may be a threshold effect whereby return yield drops significantly when final lesion density during the previous fall reaches about 60 spots per leaf on cultivar Premier.


 

Fig. 5. Box-whisker plots showing the distribution of Septoria leaf spot severity values on shoots of Premier rabbiteye blueberry that subsequently formed different numbers of flower buds in field trials in Athens, Georgia from 2001-2002 to 2003-2004. Disease severity is expressed as the number of spots per leaf prior to defoliation of that leaf and averaged for all leaves on a given shoot. The boxes represent the interquartile range, with the whiskers indicating the 5 and 95 percentiles. Lines and circles within the boxes represent median and mean disease severity values, respectively.

 

Conclusions

This project addressed selected aspects of the Septoria-blueberry pathosystem in an effort to fill critical gaps in knowledge on disease ecology and epidemiology. Although the experiments described here did not develop or test specific management guidelines, they provide the basic information needed to critically evaluate currently used disease control practices.

Temporal progress of Septoria leaf spot was typical of polycyclic epidemics in which secondary cycles of the pathogen are produced, resulting in continuous infection of the leaves. Pycnidiospore inoculum was present throughout the season, and leaves were infected by S. albopunctata season-long. Thus, it is clear that multiple fungicide applications are needed for effective disease suppression. Furthermore, given the early disease onset observed in spring of 2002, fungicide sprays may have to be initiated earlier than the current practice of beginning applications after fruit harvest in the summer. In this context, it would be important to determine potentially beneficial side effects against Septoria leaf spot of early-season fungicide applications made to control of mummy berry disease, blossom blight, and fruit rots.

Disease severity, defoliation, flower bud set, and return yield were found to be interrelated. Leaves with high lesion densities at harvest abscised earlier in the fall than those with low disease severity, and shoots with severely diseased leaves and/or high levels of defoliation had a reduced potential to set flower buds. Furthermore, such shoots consistently had low return yields the following year. With further research, it may be possible to identify specific disease severity or defoliation levels that can be tolerated during specific periods of crop development without impacting flower bud set and return yield negatively. Return yield data for Premier indicated that yield potential dropped markedly as final lesion density the previous fall exceeded about 60 spots per leaf. Based on typical disease progress curves for this cultivar (14), a final lesion density of 60 spots per leaf in the fall corresponds to a disease level of 5 to 10 spots per leaf earlier at harvest. Thus, field experiments could be designed to test whether treatments that maintain disease below this threshold at harvest can indeed prevent losses in return yield. Such experiments would have to be carried out at multiple sites, in different years, and for cultivars differing in susceptibility in order to capture a wide range of biologically relevant conditions.


Acknowledgments

Funded in part by MBG Marketing, the Southern Region Small Fruit Consortium, and the USDA-CSREES Pest Management Alternatives Program (grant no. 01-34381-11181). We thank Albert Culbreath, Scott NeSmith, and Katherine Stevenson (members of the first author’s Ph.D. committee) for their excellent guidance, and Henry Ngugi and Amy Savelle for assistance with various aspects of this study.


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