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On-farm selection for quality and resistance topest/diseases of cocoa in Sulawesi: (ii) quality andperformance of selections against Phytophthora podrot and vascular-streak diebackPeter McMahon a , Agus Purwantara b , Agung W. Susilo c , Sri Sukamto c , Abdul Wahabd , Hussin bin Purung e , Muhammad Hidayat e , Darna Ismail e , Tap Taproni d , SmiljaLambert f , David Guest g & Philip Keane aa Department of Botany , La Trobe University , Bundoora, 3086, Victoria, Australiab Biotechnology Research Institute for Estate Crops , Bogor, 16151, Indonesiac Indonesian Coffee and Cocoa Research Institute , Jember, Indonesiad BPTP SULTRA , Kendari, Sulawesi Tengarrah, Indonesiae Mars Symbioscience Indonesia, Jl. Kima , Makassar, Sulawesi Selatan, Indonesiaf Mars Australia , Ring Road, Ballarat, 3350, Victoria, Australiag Food and Natural Resources, Faculty of Agriculture , The University of Sydney , Sydney,AustraliaPublished online: 15 Sep 2010.

To cite this article: Peter McMahon , Agus Purwantara , Agung W. Susilo , Sri Sukamto , Abdul Wahab , Hussin binPurung , Muhammad Hidayat , Darna Ismail , Tap Taproni , Smilja Lambert , David Guest & Philip Keane (2010) On-farmselection for quality and resistance to pest/diseases of cocoa in Sulawesi: (ii) quality and performance of selectionsagainst Phytophthora pod rot and vascular-streak dieback, International Journal of Pest Management, 56:4, 351-361, DOI:10.1080/09670874.2010.503284

To link to this article: http://dx.doi.org/10.1080/09670874.2010.503284

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On-farm selection for quality and resistance to pest/diseases of cocoa in Sulawesi: (ii) quality and

performance of selections against Phytophthora pod rot and vascular-streak dieback

Peter McMahona*, Agus Purwantarab, Agung W. Susiloc, Sri Sukamtoc, Abdul Wahabd, Hussin bin Purunge,Muhammad Hidayate, Darna Ismaile, Tap Tapronid, Smilja Lambertf, David Guestg and Philip Keanea

aDepartment of Botany, La Trobe University, Bundoora, 3086, Victoria, Australia; bBiotechnology Research Institute for EstateCrops, Bogor 16151, Indonesia; cIndonesian Coffee and Cocoa Research Institute, Jember, Indonesia; dBPTP SULTRA, Kendari,Sulawesi Tengarrah, Indonesia; eMars Symbioscience Indonesia, Jl. Kima, Makassar, Sulawesi Selatan, Indonesia; fMars Australia,Ring Road, Ballarat 3350, Victoria, Australia; gFood and Natural Resources, Faculty of Agriculture, The University of Sydney,Sydney, Australia

(Received 15 October 2008; final version received 18 June 2010)

The cocoa industry in Sulawesi, the main region of cocoa production in Indonesia, is threatened by destructivediseases, including vascular-streak dieback (VSD) caused by the basidiomycete Oncobasidium theobromae and stemcanker and Phytophthora pod rot (PPR) or black pod, caused by Phytophthora palmivora. Using the considerablegenetic diversity of cocoa on farms, host resistance was identified and tested with the participation of farmers. Forty-nine local and international cocoa selections with promising resistance characteristics (as well as susceptible controls)were side-grafted onto mature cocoa in a replicated trial with single-tree plots. Developing grafts were assessed in thedry season for severity of VSD infection, scored from 0 (no infection) to 4 (graft death). All of the 49 clones in thetrial became infected with VSD in at least some replicates. Average severity varied from 0.2 to 1.6. Potential VSD-resistance was found in eight clones, including DRC 15, KA2 106 and a local Sulawesi selection, VSD2Ldg. Some ofthe most susceptible clones were local Sulawesi selections from areas with a history of little or no VSD. Thirty-fourpod-bearing clones were evaluated over a 2-year period for yield, quality and resistance to natural infections of PPR.Cumulative PPR incidence for all clones was 22% but varied from 8.6 to 43% among clones. Clones with less than15% PPR incidence were designated as resistant, including DRC 16 and local Sulawesi selections, Aryadi 1, Aryadi 3and VSD1Ldg. Scavina 12 was moderately resistant in the trial with a PPR incidence of 23%. Cumulative incidencesof the mirid, Helopeltis spp., determined in the same evaluation period, indicated that DRC16 was the mostsusceptible clone with an incidence of 52% in ripe pods and 23% in immature pods. In comparison, KKM4 showedevidence of resistance to Helopeltis spp., with incidences of 34 and 0.8% in ripe and immature pods, respectively. Theimpact of diseases and pests (including cocoa pod borer) on bean losses and bean quality varied between clones butgenerally the bean size (or bean count) was affected more than the fat content or shell content.

Keywords: cocoa diseases; Phytophthora pod rot; vascular-streak dieback; on-farm selections; resistance; Sulawesismallholders; Helopeltis; bean quality; side-grafted clones

1. Introduction

In Sulawesi, Indonesia, cocoa production has ex-panded spectacularly beginning from minor produc-tion in the early 1980s. This expansion has beenoverwhelmingly in the hands of smallholders for whomcocoa provides their main livelihood. As a result,Indonesia is now the third largest cocoa producerglobally (Directorate General for Estate Crops 1999).Following two decades of pioneer planting withminimal problems, the smallholders and the Sulawesicocoa industry now face serious losses in productionand impacts on bean quality due to declining soilfertility and pests and pathogens of which cocoa podborer (CPB, the moth Conopomorpha cramerella), theoomycete Phytophthora palmivora which causes Phy-tophthora pod rot (PPR) and stem canker, and thebasidiomycete fungus, Oncobasidium theobromae,

which causes vascular-streak dieback (VSD) (Keane1992; Wardojo 1992) are the most serious. To addressthese problems, an Australian Centre for InternationalAgricultural Research (ACIAR) project was estab-lished to encourage the use of farmer participatory andlocally applicable methods for the selection, testing anduse of genotypes with better resistance and/or qualityon farms. The project aimed to develop a method ofon-farm selection and clonal testing that could beadopted by farmers with the help of local extension andresearch officers. The possibility of on-farm selectionfor superior genotypes was based on the geneticdiversity found on Indonesian cocoa smallholdings asa result of the several introductions and subsequenthybridization of diverse cocoa types (original Trinitar-io types developed during the early 1900s, Amelonadotypes introduced from Sabah, Upper Amazon x

*Corresponding author. Email: peter.mcmahon@latrobe.edu.au

International Journal of Pest ManagementVol. 56, No. 4, October–December 2010, 351–361

ISSN 0967-0874 print/ISSN 1366-5863 online

� 2010 Taylor & Francis

DOI: 10.1080/09670874.2010.503284

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Trinitario ‘hybrid cocoa’ developed in Java andincluding Upper Amazon and Trinitario materialfrom Malaysia and Papua New Guinea). As well, theproject aimed to build on the particular knowledgeheld by farmers about the performance of genotypes ontheir farms, the existing and widespread network ofgovernment extension services in Indonesia and thepossibility of using clonal propagation (e.g. side-grafting of mature trees) methods for farm improve-ment. To this end, a clone testing trial was establishedin Southeast Sulawesi. Clones collected with theassistance of farmers, as well as international clones,were propagated by side-grafting onto mature trees ona working cocoa farm in an area affected seriously bythe major pest/disease problems typically found inSulawesi cocoa. Pod-bearing clones in this trial wereevaluated for 2 years (2005–2006). McMahon et al.(2009) reported on the CPB incidence among the clonesunder test during this period and the variabilitydetected in CPB incidence both between clones andbetween seasons. Here we report on results for otherdisease or pest problems, especially VSD and PPR.VSD is a new encounter disease of cocoa, apparentlyhaving transferred repeatedly to cocoa from anunidentified host in Southeast Asia (Keane 1992) whilePPR occurs on cocoa worldwide. Host resistance toVSD, at first in Papua New Guinea in the 1960s andlater in Malaysia, proved crucial to overcomingepidemics that decimated the cocoa industries of thosecountries (Zainal Abidin et al. 1984; Keane and Prior1992). Resistance to VSD is partial, limiting infectionto branch tips thus preventing the fungus fromreaching larger branches and killing trees. Hostresistance to PPR appears to be partial and additive(Tan and Tan 1990; Saul 1993; Van der Vossen 1997;Zadocks 1997). Various studies have compared cocoagenotypes for PPR resistance (e.g. see Blaha 1974;Soria 1974; Saul 1993; Iwaro et al. 1997, 1998) andidentified resistance in some clones. The clonal testingtrial conducted at Ladongi indicated that the geno-types, including local farm selections (many of whichwere derived from introductions of Amelonado typesfrom Sabah), varied considerably in incidence andseverity of both PPR and VSD and provided supportto on-farm selection and testing as a promising methodfor direct farm improvement and for identifyingpromising genotypes for breeding programs.

2. Materials and methods

2.1. Selection, collection and propagation of cocoagenotypes and trial establishment

Cocoa genotypes were selected on farms in South,Southeast and Central Sulawesi and East Kalimantanprovinces of Indonesia as budwood sticks, transportedto the farm trial site and side-grafted onto maturecocoa trees as described in McMahon et al. (2009).

International clones and susceptible local selectionswere included in the mixture of genotypes tested. Theclonal testing trial (with a total of 49 clones) was set upin Ladongi in Kolaka District, Southeast Sulawesi on aworking cocoa farm with the cooperation of thefarmer. The design was single-tree plots, randomisedin 20 replicate blocks (McMahon et al. 2009). Due todifficulties encountered in side-grafting mature trees,only 10–18 replicates were achieved for most clonesand 34 clones produced a sufficient number of pods bythe end of 2004 for assessment.

2.2. Severity of vascular-streak dieback (VSD)

The severity of VSD, which infects vegetative shoots,was assessed during the dry season of 2004 ondeveloping grafts in the 49 clones established in thetrial. Severity of infection was assessed on a scale 0–4:0, no infection; 1, signs of chlorosis, little or no leafdrop; 2, distinctive chlorosis and some leaf drop; 3,severe leaf loss, dieback; 4, graft death.

2.3. Incidence of Phytophthora pod rot (PPR)

Pods were assessed for PPR twice per month in a 24-month period from January 2005 to December 2006.All ripe (harvestable) pods and the immature pods thatwere infected with PPR or otherwise infested ordiseased were harvested and separated into healthyand infected/infested pods. Pods affected by cherellewilt could be differentiated from infected/infestedimmature pods by their smaller size and were notincluded in the assessment. The numbers of immatureand ripe pods infected with PPR were counted.Harvested ripe pods with PPR infection (but no CPBinfestation) were evaluated for intensity of infection:either heavily infected (PPR lesion covering over 50%of the pod surface) or lightly infected (lesion coveringless than 50% of the pod). To estimate the incidence ofPPR on a typical smallholding in the area, a plot of 50trees was assessed on a farm 0.75 km from the trial siteusing the same evaluation method as in the trial, exceptthat evaluations were conducted monthly.

2.4. Inoculation of detached pods with PPR-infectedpod tissue

Ripe detached pods from a few of the clones in theLadongi trial were wound-inoculated with PPR-in-fected pod tissue. Small discs (5 mm diameter) wereremoved from the mesocarp of a PPR-infected pod andinserted into holes cut with a cork borer in the husks ofhealthy pods of the selected clones with three replicatepods for each clone. The pods were kept in a moistchamber at room temperature. The length and width(cm) of the lesion was measured daily for a weekproviding an estimate of expansion rate of the lesionarea (cm2) for 7 d after inoculation (d.a.i.).

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2.5. Determination of actual and potential pod valuesfor each clone

For each replicate tree, extractable beans wereharvested and separated into two groups: extractablebeans obtained from healthy ripe pods and extractablebeans obtained from infested or diseased ripe pods (seeMcMahon et al. 2009). The wet weight for each groupof beans was recorded. For each clone, the collectedbeans were pooled, dried and the dry weight recorded.

2.5.1. Actual pod value (no. pods per kg dried beans)

Actual pod value was determined as the number ofripe, harvestable pods (both healthy and infested/infected) needed to give 1 kg of dry beans.

2.5.2. Potential pod value and bean losses

The potential pod value was determined from thebeans extracted from healthy pods. Bean losses wereestimated by comparing the bean harvest from all ripepods (from which the actual pod value was determined)with the bean harvest (based on the beans harvestedfrom healthy pods) expected if all the harvested podswere free of pest/diseases. Pod values were calculatedfor clones producing at least 10 healthy ripe pods.

2.6. Bean quality

For the clones that produced a sufficient quantity ofbeans, quality assessments were conducted at theresearch laboratory of PT Effem/Mars in Makassar,Sulawesi. Bean count was determined as the number ofdried beans per 100 g. Shell content and cocoa buttercontent were determined. Shell content was evaluatedby deshelling 100 g of beans and weighing the shells todetermine % shell content. To determine cocoa buttercontent, bean samples were milled on a Retcheplanetary ball mill and the cocoa mass was analysedfor fat content in a Near Infra Red (NIR) highperformance analyser (Foss System II 6500 scanningspectrophotometer, NIR Systems Inc. Silver SpringsMD) fitted with a transport module in reflectancemode. Spectra were recorded in the range 400–2500 nmat 2-nm intervals. Calibrations were developed byusing modified partial least square regressionprocedures.

2.7. Statistical analyses

Means for disease incidence (%) were weighted for thenumbers of pods produced by each replicate tree andsubjected to arc-sign transformations (Zar 1996).Transformed values were subjected to ANOVA fol-lowed by the Games–Howell test (SPPS Ver 11.5).Data are presented in their original (untransformed)form (see McMahon et al. 2009).

3. Results

3.1. VSD severity

Since VSD infects the vegetative shoots of cocoaplants, all the clones initially established in the trialwere able to be assessed for VSD infection prior topod-bearing, when grafts usually still had fewer thanthree branches. VSD infections were detected in all ofthe clones tested in the trial in at least some replicates.Table 1 shows the 49 clones in the trial at Ladongiranked from lowest to highest average VSD severity.Clones varied considerably in average severity ofinfection and in the range of severity among replicatesand by combining these two measurements, the level ofresistance for each clone was estimated (see Table 1legend).

Resistant local selections were identified includingVSD2Ldg, selected from a farm in South-East Sulawesifor potential VSD-resistance. The clones selected assusceptible controls (VSD1Ldg and VSD4Ldg) weresusceptible or moderately susceptible in the trial. Twoclones known for VSD-resistance, DRC 15 from theICCRI collection (Susilo et al. 2009), and KA2 106,closely related to KA2 101, from Papua New Guinea(Keane and Prior 1992), proved to be the mostresistant clones in the trial. In addition, PM 1 andPM 2, originally from an East Kalimantan estate andDarwis 1, a local farmer selection from East Kaliman-tan, appeared to be VSD-resistant. Among the mostsusceptible of the clones were local selections fromSouth and Central Sulawesi. This could reflect theshort time that VSD has occurred at detectable levelson cocoa farms in these areas. For example, VSD wasfirst reported as a problem in Central Sulawesi in 2000.

3.2. Incidence of PPR among clones

For the 34 pod-bearing clones evaluated over the 2-year period, the cumulative incidence of PPR in ripepods did not exceed 45% in any clone. In two clones,AA01 and KKM4, over 40% of the pods evaluatedwere infected. The average PPR incidence for all theclones in the trial was 22.3%. However, at a nearbyfarm where practices typical of the area were con-tinued, cumulative PPR incidence was higher at 28.7%in the same evaluation period. Also, anecdotal reportsfrom farmers in the area suggest that the PPRincidence during the wet season was higher in thesurrounding district than at the trial site: on somefarms, the proportion of harvested pods infected withPPR exceeded 50% during the wet season but onlyreached a maximum of 40% in the trial for all theclones taken together (data not shown).

Figure 1 indicates that the cumulative PPRincidence in ripe pods varied greatly among clonesfrom 8.6% in Aryadi 3 to 43.6% in AA01. In ripe pods,PPR incidence was significantly low in VSD1Ldg,DRC 16 (a PPR resistant clone from the ICCRI

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collection in Java), Aryadi 3, Aryadi 1, Haris 2 and PM2 (Table 2). The most susceptible clones were AA01and KKM 4 while the susceptible controls (Phyt Ldgand Sugeng) proved to be moderately susceptible in thetrial. (Figure 1, Table 2). Four approximate resistancegroupings were designated based on cumulative PPRincidence: resistant (515%), moderately resistant(15–24%), moderately susceptible (25–34%) and sus-ceptible (434%). According to these criteria, the PPR-resistant international clone Scavina 12, demonstrated

only moderate resistance in the trial. Figure 2 indicateschanges in PPR incidence with time for relativelyresistant clones compared to susceptible controls.Generally, in these and other clones (data not shown)the more resistant clones maintained a lower incidencein ripe pods compared to susceptible clones during thisperiod although at times overlap occurred (Figure 2).

Table 2 shows that the proportion of PPR-infectedpods also infested with CPB exceeded 75% in most ofthe clones, consistent with the high CPB incidence at

Table 1. VSD infection of clonal grafts in the Ladongi trial ranked from lowest to highest average severity.

Clone No. Clone name Source No. grafts Average severity Range of severity Resistance rating

12 DRC 15 ICCRI, Java 10 0.20 0–1 R37 KA2 106 Papua New Guinea 11 0.27 0–1 R18 PM 2 ICCRI, Kalimantan 17 0.29 0–1 R1 Darwis 1 E. Kalimantan 10 0.30 0–1 R36 KKM 4 Malaysia 13 0.31 0–1 R9 PM 1 ICCRI, Kalimantan 11 0.36 0–1 R16 VSD2Ldg SE Sulawesi 14 0.43 0–1 R10 K 82 Papua New Guinea 14 0.43 0–2 MR23 SCA 12 ICCRI collection 10 0.50 0–2 MR15 AA02 ICCRI collection 18 0.50 0–1 R29 RCC 71 ICCRI, N. Sumatra 13 0.54 0–1 MR13 AA01 ICCRI collection 12 0.58 0–1 MR14 GS 29 Reading, UK 12 0.58 0–1 MR47 PBK 2 SE Sulawesi 12 0.58 0–1 MR8 ICS 13 ICCRI collection 16 0.63 0–1 MR19 KKM 22 Malaysia 16 0.63 0–1 MR20 NIC 4 ICCRI collection 14 0.64 0–2 MR22 Bal 209 Malaysia 11 0.64 0–1 MR28 Sugeng SE Sulawesi 17 0.65 0–1 MR7 NIC 7 ICCRI collection 12 0.67 0–1 MR26 DRC 16 ICCRI, Java 15 0.67 0–2 MR27 NW 6261 ICCRI collection 12 0.67 0–1 MR24 RCC 70 ICCRI, N. Sumatra 11 0.73 0–2 MS41 Baharuddin Central Sulawesi 16 0.75 0–3 S44 Aryadi 2 South Sulawesi 16 0.75 0–1 MS21 VSD3Ldg SE Sulawesi 18 0.78 0–2 MS25 BR25 Malaysia 14 0.79 0–1 MS46 Amiruddin SE Sulawesi 14 0.79 0–2 MS30 RCC 72 ICCRI, N. Sumatra 15 0.80 0–2 MS17 KEE 2 Papua New Guinea 11 0.82 0–1 MS11 M4 Maluku 11 0.82 0–2 MS6 VSD1Ldg SE Sulawesi 11 0.82 0–2 MS40 Asmaun merah South Sulawesi 13 0.85 0–2 MS48 VSD4Ldg SE Sulawesi 10 0.90 0–2 MS32 RCC 73 ICCRI, N. Sumatra 13 0.92 0–2 MS3 Darwis 3 E. Kalimantan 12 0.92 0–3 S42 Ruslan Central Sulawesi 18 0.94 0–2 MS2 Darwis 2 E. Kalimantan 12 1.00 0–2 S31 PBK 1 SE Sulawesi 17 1.00 0–2 S45 Aryadi 5 South Sulawesi 17 1.00 0–2 S5 Anshary 2 Central Sulawesi 16 1.06 0–2 S4 Anshary 1 Central Sulawesi 16 1.25 0–3 S34 Haris 1 Central Sulawesi 11 1.27 0–2 S49 PhytLdg SE Sulawesi 11 1.27 0–3 S35 Haris 2 Central Sulawesi 18 1.39 0–3 S39 Karmono 2 Central Sulawesi 10 1.40 0–2 S33 Ridwan Central Sulawesi 15 1.40 0–3 S43 Aryadi 1 South Sulawesi 14 1.43 0–2 S38 Karmono 1 Central Sulawesi 11 1.64 0–2 S

Notes: Clones in the collection at ICCRI and local farm selections were included in the trial (see section 2). Individual grafts were assessed duringthe dry season for VSD severity by ranking infection as 0, no infection; 1, signs of chlorosis, little or no leaf drop; 2, distinctive chlorosis and someleaf drop; 3, severe leaf loss, dieback; 4, graft death. The resistance rating of clones incorporates both the average severity score and the range ofseverity scores of infection observed among the replicates as follows: R, resistant: 50.50 and 0–1; MR, moderately resistant: 0.50–0.69 and/or 0–2; MS, moderately susceptible: 0.70–0.99 and 0–2; S, susceptible: 40.99 and/or 0–3.

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the trial site (see McMahon et al. 2009). The ratio ofheavy (over 50% of the pod husk infected) to lightinfection (less than 50% of the pod husk infected)varied among the clones, providing evidence of

differential rates of lesion expansion on infected pods.But there was no correlation between total PPRincidence in ripe pods and the incidence of heavyPPR infections (Pearson correlation coefficient,

Table 2. Incidence of PPR in ripe pods, the proportion of PPR-infected pods also infested with CPB and the ratio of heavy tolight infections (assessed only in PPR-infected pods free of CPB) in some of the clones tested at Ladongi (see Figure 1).

Clone no. Clone name% Ripe podswith PPR

Proportion infestedwith CPB (%)

Ratio of heavy/lightPPR infection

2 Darwis2 11.4ab 88.5 2.06 VSD1Ldg 8.6ab 75.0 3.09 PM 1 31.4d 85.7 2.713 AA01 43.6e 82.4 2.714 GS29 19.3c 87.1 2.018 PM 2 10.5b 73.9 3.619 KKM22 20.3c 82.5 4.021 VSD3Ldg 31.3d 74.7 4.723 SCA12 20.4c 83.5 4.024 RCC70 31.7d 86.8 1.525 BR25 30.1d 80.0 3.826 DRC16 11.0ab 90.0 1.128 Sugeng 30.4d 85.5 2.631 PBK 1 21.0c 90.2 4.534 Haris1 21.9c 66.7 6.035 Haris2 11.1b 86.8 0.436 KKM4 42.3e 91.5 3.040 Asmaun merah 23.3c 85.7 1.041 Baharuddin 23.2c 91.9 9.043 Aryadi1 10.9ab 100.0 745 Aryadi3 8.6a 86.1 1.546 Amiruddin 21.1c 91.8 1.7

Note: Means within a column followed by the same letter are not significantly different (P � 0.05, ANOVA, Games-Howell).

Figure 1. Cumulative PPR incidence (%) in ripe pods in the trial at Ladongi, determined over a 2-year period (January 2005 toDecember 2006). Ripe pods (both healthy and infected) were harvested twice per month and evaluated individually for presenceor absence of PPR infestation. Each bar represents the mean PPR incidence (with SE bars), weighted for the numbers of ripe podsharvested, for the 2-year period in an individual clone.

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r ¼ 0.205, P ¼ 0.126). Also, there was no correlationbetween PPR incidence in ripe pods and the heavy/light infection ratio (Table 2) (Pearson correlationcoefficient, r ¼ 0.175, P ¼ 0.224).

Figure 3 indicates that the clones varied in percentPPR infection at the immature stage of pod develop-ment. Losses at the immature stage exceeded 20% ofthe total harvest in the susceptible controls, PhytLdgand Sugeng, and also in a number of other clones (e.g.PM 1, RCC 70). The PPR incidence in ripe pods(Figure 1) was positively correlated with incidence inimmature pods (Figure 2) (Pearson correlation coeffi-cient, r ¼ 0.399**, P ¼ 0.01).

3.3. Lesion expansion in pods artificially inoculatedwith PPR-infected tissue

Although PPR infections developed in most of thewound-inoculated pods, the rate of expansion oflesions (data not shown) proved to be highly variablebetween replicates as well as clones. However, con-sistent with the field results, DRC 16 showed evidenceof resistance with a relatively low average lesion area at7 d.a.i. (550 cm2) compared to Sugeng, a susceptiblecontrol, which had a higher average lesion area(4130 cm2). However, lesion expansion data for otherclones tested were not so consistent with the field datae.g. the clone VSD1Ldg, resistant in the field trial, hadmoderate-large lesions 7 d.a.i. (averaging 92 cm2) andPM 1, was quite resistant in the inoculation trial(average lesion area at 7 d.a.i. 550 cm2) yet moder-ately susceptible in the field trial (Figure 1).

3.4. Other pests and diseases

The most important pest at the trial site after CPB wasthe mirid, Helopeltis spp. Figure 4 shows the cumula-tive average incidence of this pest on total podsharvested over the evaluation period. Losses due toHelopeltis were especially high in DRC 16 with 23%pods lost at the immature stage and a ripe podincidence of 52% (Figure 4). Losses out of the totalharvest at the immature stage of pod development werebetween 10 and 20% in Darwis 2, Anshary 1 and PBK2, while the highest total incidence (88%) occurred inPBK 1, a CPB-susceptible control (see McMahon et al.2009). Particularly resistant clones were KKM4 (with

Figure 3. PPR incidence (%) determined from the total pod harvest (immature and ripe pods) at Ladongi from 2005 to 2006.Ripe pods (healthy and infected) and all infected immature pods were harvested twice per month. Differential shading in barsindicates PPR incidence in immature pods (lower, darker shading) and in ripe pods (upper, lighter shading) as a proportion of allthe pods harvested. Values shown are means (with SE bars for each category) weighted for the number of pods harvested in eachclone.

Figure 2. Changes in PPR incidence during 2005 and 2006in the ripe pods of relatively PPR-resistant clones, Aryadi 3and PM 2 (continuous lines, solid symbols) and susceptiblecontrol clones, Phyt Ldg and Sugeng (broken lines, opensymbols) identified at Ladongi (see Figure 1).

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an incidence of 34% in ripe pods and 0.8% inimmature pods) and PM 1, PM 2 and AA01.Colletotrichum sp. was detected at negligible levels inripe pods, and was more common in immature pods.However, incidence even in immature pods was lessthan 1% of the total pod harvest for most of the clones(data not shown). Damage by rodents (squirrels andrats) was higher in ripe pods than immature pods. Evenso, incidence of damage (out of the total pod harvest)at the ripe pod stage were less than 2% for most clones(data not shown): only in KKM 22 (2.3%) andAmiruddin (4.6%) were ripe pod losses due to rodentactivity higher.

3.5. Pod values and bean quality

Table 3 shows pod values for all the harvested pods(actual pod values) as well as pod values determinedfrom healthy pods only (potential pod values) forselected clones. Potential pod values were lower thanactual pod values in most clones, as expected, reflectingthe impact of pests and diseases. However, thepotential pod values determined in the Ladongi cloneswere generally high and were much higher thanexpected in some of the international clones. The smallbean size of Scavina 12 was reflected in its high podvalue but this was exceeded greatly by the Kalimantanclone, PM 2, which had a remarkably high pod value(172.5) consistent with the very small pods and beansof this clone.

Bean losses due to pest/diseases in ripe pods werecalculated by comparing the bean harvest obtained

Figure 4. Incidence of Helopeltis spp. (%) determined from the total pod harvest (immature and ripe pods) at Ladongi from2005 to 2006. Ripe pods (healthy and infested) and all infested immature pods were harvested twice per month. Differentialshading in bars indicates Helopeltis incidence in immature pods (lower, darker shading) and in ripe pods (upper, lighter shading)as a proportion of all the pods harvested. Values shown are means (with SE bars for each category) weighted for the number ofpods harvested in each clone.

Table 3. Actual pod values (no. ripe pods (infected andhealthy)/kg dry beans), potential pod value (no. healthy podsper kg dry beans) and bean losses in ripe pods harvested fromsome of the cocoa clones in the trial at Ladongi, SoutheastSulawesi.

Clone no.Clonename

Actualpod value

Potentialpod value

Beanlosses(%)

2 Darwis 2 47.5 43.6 8.36 VSD1Ldg 49.1 34.8 29.211 M4 37.1 27.0 27.213 AA01 39.0 30.1 22.915 AA02 46.0 36.2 21.216 VSD2Ld 82.7 55.7 32.617 KEE 2 52.0 31.2 40.118 PM 2 172.5 152.7 11.519 KKM 22 45.2 36.2 20.021 VSD3Ldg 45.1 28.7 36.422 BAL 209 51.0 40.1 21.323 SCA 12 98.8 100.9 72.125 BR 25 42.5 35.2 17.128 Sugeng 40.3 30.1 25.330 RCC 70 50.6 37.0 26.931 PBK 1 53.4 44.3 17.134 Haris 1 52.1 44.6 14.435 Haris 2 53.0 39.9 24.741 Baharuddin 46.0 43.1 6.342 Ruslan 57.5 44.9 21.843 Aryadi 1 38.0 27.0 28.944 Aryadi 2 40.6 33.4 17.745 Aryadi 3 43.6 37.8 13.446 Amiruddin 46.5 22.8 50.949 PhytLdg 42.6 45.0 75.5

Notes: Pods were harvested twice per month over a 2-year period.Beans were collected separately from healthy pods and pods affectedby pest/diseases, dried and weighed. Pod values are given for clonesproducing at least 10 healthy ripe pods.

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from all harvested pods with that of healthy pods(Table 3). Bean losses can be attributed to thecombined effect of pests and diseases, mainly CPBand PPR. Losses varied considerably among theclones. Generally, the clones with apparent CPB-resistance (McMahon et al. 2009) had relatively lowbean losses compared to other clones. For example,Darwis 2, Aryadi 2, Scavina 12 and PM 2 showed beanlosses of less than 20%. However, clones with low PPRincidence in the field did not follow this pattern asPPR-resistant clones such as VSD1Ldg had high beanlosses (29.2%) while some more PPR susceptible clones(e.g. Baharuddin, Haris 1) had lower losses.

Table 4 presents data on bean quality analyses for26 of the clones tested in Ladongi. Most of these clonesdid not meet the Standard National Indonesia (SNI)specifications of quality (see Table 4 legend). Fewclones met the minimum fat content of 51% preferredby industry. Pests or diseases seemed to have no effecton the fat content of some clones (e.g. KKM 22, GS29, Aryadi 1) but had a greater effect on others (e.g.PM 1, Baharuddin). The highest fat content was inPBK 2, a CPB-susceptible control. Bean count wasaffected considerably by pests and diseases in someclones. Of the 26 clones tested, 9 clones had a beancount in healthy pods exceeding the industry thresholdrequirement of 115, and this increased to 14 clones in

beans from infected pods (Table 4). In most clones,beans extracted from damaged pods had a higherproportion of flat beans and placental waste and highershell content than beans from healthy pods (Table 5).

4. Discussion

As evaluated in grafts at a relatively early stage ofdevelopment, a number of clones in the trial atLadongi showed a degree of VSD resistance. Some ofthese, e.g. Sugeng and KKM 22, with relatively lowpod values and moderate resistance, could be immedi-ately useful in VSD-affected areas. However, the VSD-resistant clones, PM 2 and VSD2Ldg, had very highpod values. These clones, particularly PM 2 with itsstrikingly small pods and beans, would not be useful onfarms. However, the strong resistance characteristics ofthese clones could make them valuable parentalmaterial for cocoa breeding. Eight of the 14 clonesassessed as VSD-susceptible at Ladongi (Table 1) werelocal selections from Central Sulawesi (see Table 1).This province was largely unaffected by VSD at thetime the selections were made, and therefore the cocoagenotypes grown in Central Sulawesi had not beenselected by farmers under pressure from VSD. Theapparently greater level of partial resistance amonggenotypes selected from parts of South and Southeast

Table 4. Bean quality characteristics of some of the clones evaluated in the trial in Ladongi, Southeast Sulawesi.

Clone

Bean count Shell content (%) Fat content (%) Water content (%)

Healthy Damaged Healthy Damaged Healthy Damaged Healthy Damaged

Darwis 2 nd 135 nd 16.5 nd 48.9 nd 3.3Anshary 1 143 86 13.7 13.3 47.9 47.2 2.9 3VSD1Ldg 86 106 18.9 15.1 50.5 49.1 3.2 3PM 1 123 151 14.6 16.8 51.4 47.3 2.9 3.1M4 108 128 12.8 17.4 48 46.4 2.5 2.6GS 29 79 100 8.4 17 50.5 50.5 2.9 3.1AA02 91 nd 12.1 nd 50.2 nd 3.1 ndVSD2Ldg 90 115 12 15.3 49.5 49.6 2.9 2.7PM 2 178 244 19.2 20.7 47.7 46.8 3.1 3.3KKM 22 89 108 10.8 14 49.8 51.2 2.8 2.7VSD3Ldg 119 166 19.2 18.5 48 46.5 2.6 2.8Bal 209 109 107 11.1 14.2 50.9 51.6 3 2.7RCC 70 85 128 10.8 14.7 50.9 48.3 2.8 2.1DRC 16 81 99 10.1 12.6 47.8 45.5 2.9 2.7Sugeng 94 111 10.9 15.2 50.3 48.5 3.1 2.8RCC 72 127 117 10.8 16.4 49.5 48.3 2.7 2.7PBK 1 88 nd 13.8 nd 48.1 nd 3.1 ndHaris I 98 130 12.6 15.5 48.9 47.8 2.9 2.7Baharuddin 117 117 14.8 16.9 49.5 45.9 2.6 2.9Ruslan 1 109 141 11.7 17.2 50.9 49.2 2.6 3.8Aryadi 1 121 153 11.1 19.6 50.8 52.3 2.7 2.5Aryadi 2 132 173 12.2 19 49.6 47.9 3.1 2.6Aryadi 3 124 152 13.2 15.5 49.9 48.5 2.7 2.7Amiruddin 115 163 13.1 18.8 49.7 48 2.8 3PBK 2 nd 81 nd 13.6 nd 53 nd 2.8PhytLdg 92 111 14.7 13.1 49.5 50.1 2.6 2.4

Notes: Beans harvested from healthy pods and pods damaged by pest/diseases were analysed separately and results from each category are shownin separate columns. SNI specifications: max. bean count (no. dried beans in 100 g) ¼ 115, max. shell content ¼ 13% and minimum fatcontent ¼ 51%. nd, not determined.

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Sulawesi (e.g. VSD2Ldg), where VSD has beenprevalent at least since the early 1980s, could beexplained by the longer period of time over which theyhave possibly been selected under VSD pressure. Thisindicates the capacity of the genetically diverse cocoain Sulawesi for adaptation to factors in the localenvironment (e.g. pest and disease pressure) and thepotential value of employing locally adapted genotypesfor farm improvement, either by selection of resistantclones or for breeding programs.

In the 2-year evaluation period, the clones tested inLadongi, including the on-farm selections, variedconsiderably in their cumulative incidence of PPR,enabling the identification of potential PPR-resistancein some clones. These results support on-farm selectionas a useful way of identifying potential resistance incocoa genotypes but also re-affirm the necessity ofconfirming identifications by farmers in systematictrials (see McMahon et al. 2009). The field trialindicated that the most PPR-resistant of the cloneswere the local Sulawesi selections, Aryadi 3 andVSD1Ldg. The former selection was identified ashaving a low PPR infection rate by a farmer, Aryadi,while the latter was a VSD-susceptible control. Aryadi1, selected for CPB-resistance, also demonstratedpotential PPR resistance in the trial. While PPRincidence fluctuated seasonally, the incidence in the

more resistant clones was generally lower than insusceptible clones over the 2-year evaluation period(Figure 2). Saul (1993) also found that lower PPRincidence was maintained in PPR-resistant clones,compared to more susceptible clones, during bothwet and dry seasons, and was especially evident duringwet seasons. The maintenance of a low incidence inresistant types irrespective of the season suggests thatthe PPR-resistance observed in the field at Ladongi wasconstitutive to pods rather than being a seasonal effecte.g. rainfall patterns or pod numbers. The PPR-resistant Trinitario clone developed in Java, DRC 16,proved to be one of the most PPR-resistant clones atthe ripe pod stage, but not at the immature stage.Possibly, the high incidence of PPR infection inimmature pods of this clone might have been anindirect effect of infestation by Helopeltis spp., whichoccurred at a particularly high rate in the immaturepods of this clone (Figure 4). Except for DRC 16, PPRincidence in immature pods was positively correlatedwith that in ripe pods, evidence that similar resistancemechanisms are operating at both stages of poddevelopment.

Harvested ripe pods infected with PPR (but free ofCPB infestation) were evaluated for intensity ofinfection: heavily infected or lightly infected. Sinceevaluations were conducted at regular time intervals

Table 5. Bean waste (% dry weight of beans harvested) categorised as flat beans, clustered beans or placental waste from someof the clones evaluated in the trial at Ladongi.

Clone

Healthy (%)

Total

Damaged (%)

TotalFlat Clustered Placental Flat Clustered Placental

Darwis 2 nd nd nd nd 1.0 0.0 0.8 1.8Anshary 1 13.7 0.0 0.0 13.7 5.3 0.0 0.0 5.3VSD1Ldg 2.7 0.0 0.0 2.7 1.1 0.0 0.7 1.8PM 1 1.0 0.0 0.0 1 3.0 0.0 0.0 3M4 2.7 0.0 0.0 2.7 3.0 0.0 2.1 5.1GS 29 0.0 0.0 0.0 0 4.5 0.0 7.6 12.1AA02 0.2 0.0 0.0 0.2 nd nd nd ndVSD2Ldg 2.8 0.0 0.0 2.8 8.2 0.0 0.0 8.2PM 2 1.5 0.0 0.2 1.7 8.0 0.0 2.8 10.8KKM 22 0.2 0.0 0.0 0.2 0.2 0.0 0.2 0.4VSD3Ldg 8.8 0.0 0.0 8.8 14.9 0.2 2.0 17.2Bal 209 0.0 0.0 0.0 0 0.7 0.0 0.6 1.3RCC 70 0.0 0.0 0.0 0 6.8 0.0 0.3 7.2DRC 16 0.2 0.0 0.0 0.2 4.1 0.4 1.6 6Sugeng 2.5 0.0 0.0 2.5 4.7 0.0 0.9 5.5RCC 72 0.4 0.0 0.0 0.4 1.9 0.0 0.8 2.7PBK 1 2.6 0.0 0.1 2.7 nd nd nd ndHaris I 0.0 0.0 0.0 0 4.7 1.4 0.7 6.8Baharuddin 0.1 0.0 0.0 0.1 4.1 0.3 0.6 5Ruslan 1 2.7 0.0 0.0 2.7 5.7 0.0 8.6 14.3Aryadi 1 0.0 0.0 0.0 0 0.0 0.0 0.0 0Aryadi 2 0.5 0.0 0.0 0.5 5.4 0.0 0.9 6.3Aryadi 3 19.5 0.0 0.0 19.5 0.0 0.0 0.0 0Amiruddin 7.8 0.0 0.0 7.8 10.0 0.0 3.5 13.5PBK 2 nd nd nd nd 0.4 0.0 0.0 0.4PhytLdg 6.6 5.8 0.1 12.5 7.9 0.9 1.5 10.3Mean 3.0 0.2 0.0 3.4 4.4 0.1 1.5 6.0

Notes: Beans harvested from healthy pods and pods damaged by pest/diseases were analysed separately and results are shown in separatecolumns. nd, not determined.

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(approximately fortnightly) it would be expected thatin cumulative data for the 2-year evaluation period alow ratio of heavy to light infections would be theresult of a slower expansion rate of pod rot lesions. Theratio of heavy to light infections did vary betweenclones (see Table 2) suggesting that the time taken forPPR to spread though a pod may vary between clones.However, these ratios were not correlated with theincidence of PPR in ripe pods (Figure 1). Undoubtedlypod size would affect the proportion of the pod affectedby PPR, with small pods being consumed by PPR morerapidly than larger pods. For example, the resistant/moderately resistant clones PM 2 and Scavina 12 bothhad relatively high heavy/light infection ratios, perhapsreflecting their small pod size. Evaluation only of PPR-infected pods that were also free of CPB greatlydecreased the numbers of pods sampled (as most PPR-infected pods also had CPB) making the data lessreliable. Nevertheless, the lack of correlation betweenintensity of infection and incidence could be due todifferent types of PPR-resistance mechanisms in pods.Iwaro et al. (1997) identified two possible mechanismsof resistance to PPR, the first at the stage of initial podinfection (pre-penetration) and the second at the stageof growth and spread of the pathogen followinginfection of the pod (post-penetration). Possibly,pods in the Ladongi trial with high heavy/light ratiosin infected pods, but relatively low PPR incidences (e.g.Haris 1, PBK 1, KKM22, Scavina 12, Baharuddin),were susceptible at the post-penetration but not thepre-penetration stage of infection. Wound-inoculationresults for detached pods were inconsistent with thefield data in most of the clones, as clones that showedapparent resistance in the field developed relativelylarge lesions after artificial inoculation with infectedtissue. DRC 16 proved to be an exception, demonstrat-ing a high level of resistance both in the field andinoculation experiment. Possibly, some of the otherclones are resistant at the pre-penetration stage but notat the post-penetration stage (and are susceptible toartificial wound-inoculation), while DRC 16 is resistantat both stages. Also, while PPR-resistance in someclones might be attributable to a constitutive mechan-ism (see above), variation in the cropping times ofother clones could account for their low PPRincidence, especially if the peak crop falls outside thewettest periods. Such clones might escape high levels ofPPR infection, but still be susceptible to artificialinoculation. However, the high variability in lesionexpansion rates between replicates means nostrong conclusions can be drawn from the detachedpod tests.

The lower average incidence of PPR in the clones inthe Ladongi trial compared to trees on the nearby farmplot assessed monthly, could be a result of the frequentand complete harvesting method of both healthy anddiseased pods in the trial (twice per month in the trialcompared to once a month in the local area). This

observation was supported by anecdotal evidence fromnearby farmers. The higher frequency of harvestingmight have decreased the amount of inoculum avail-able for new infections. In Cameroon, for example,Ndoumbe-Nkeng et al. (2004) showed that regularremoval of pods infected with Phytophthora megakaryaat two sites in a 2-year period resulted in substantialdecreases in disease incidence.

Bean losses, estimated from the actual and poten-tial pod values, would be expected to reflect the impactof pests and diseases. However, losses varied consider-ably between the clones and were not necessarilygreater in the more pest/disease susceptible clones(Table 3). Nevertheless, the data suggest a closercorrespondence of bean losses with cumulative CPBincidence (see McMahon et al. 2009) than with PPRincidence. Possibly tolerance to infection/infestationinfluenced bean losses. In the case of CPB infestation,Teh et al. (2006) suggested that some clones, despitebeing infested with CPB, exhibit relatively low beanlosses due to tolerance to infestation.

While pest/diseases clearly affected pod values andbean quality parameters (especially bean counts) in theLadongi trial, even the healthy pods of many of theclones tested had high pod values and bean qualityparameters that were below the industry minimumstandard. This could be a reflection of the condition ofthe farm, which was located in an area of generallypoor soils, and also of the age and generally poorcondition of the rootstock trees. The trial at Ladongienabled identification of resistance in some clones butin most cases this was to particular pest/diseaseproblems. Also, most of the potentially resistant cloneshad high pod values or poor bean quality character-istics. This was also the case for PM 2 and Scavina 12,which showed evidence of potential resistance to morethan one pest/disease, but had unacceptable pod valuesand bean quality characteristics. Clones such as these,which have valuable resistance characteristics asso-ciated with poor yield and/or quality, could be used asparents in a cocoa breeding program to obtain hybridprogeny with resistance as well as good quality andyield characteristics.

Acknowledgements

The work presented in this paper was funded by theAustralian Centre for International Agricultural Research(ACIAR Project CP/2000/102). Yohannes Junianto, formerlyplant pathologist at ICCRI, Jember, East Java, selected theVSD resistant and susceptible local selections. Many thanksare due to Pak Suntoro, former head of the Plant Protectiondepartment, Dinas Perkebunan, Kendari, for his help infacilitating the field trials established at Ladongi, SoutheastSulawesi.

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