Market Access of Papua New Guinea Bananas (Musa spp.)...

Market Access of Papua New Guinea Bananas (Musa spp.)

with Particular Respect to Banana Fly (Bactrocera

musae (Tryon)) (Diptera: Tephritidae)

Amanda Mararuai

B.Sc Agriculture, Graduate Diploma in Applied Science

A thesis submitted in fulfilment of the requirements for the degree of

Doctor of Philosophy

School of Natural Resource Sciences

Queensland University of Technology

Brisbane Australia

April 2010

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Keywords

Bactrocera musae, banana fly, bananas, biosecurity, host availability, invasion biology,

invasive, market access, Musa spp., novel environment, Papua New Guinea, pest risk

analysis, population distribution

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Abstract

International market access for fresh commodities is regulated by international

accepted phytosanitary guidelines, the objectives of which are to reduce the biosecurity

risk of plant pest and disease movement. Papua New Guinea (PNG) has identified

banana as a potential export crop and to help meet international market access

requirements, this thesis provides information for the development of a pest risk

analysis (PRA) for PNG banana fruit. The PRA is a three step process which first

identifies the pests associated with a particular commodity or pathway, then assesses

the risk associated with those pests, and finally identifies risk management options for

those pests if required.

As the first step of the PRA process, I collated a definitive list on the organisms

associated with the banana plant in PNG using formal literature, structured interviews

with local experts, grey literature and unpublished file material held in PNG field

research stations. I identified 112 organisms (invertebrates, vertebrate, pathogens and

weeds) associated with banana in PNG, but only 14 of these were reported as

commonly requiring management. For these 14 I present detailed information

summaries on their known biology and pest impact.

A major finding of the review was that of the 14 identified key pests, some research

information occurs for 13. The single exception for which information was found to be

lacking was Bactrocera musae (Tryon), the banana fly. The lack of information for this

widely reported ‘major pest on PNG bananas’ would hinder the development of a PNG

banana fruit PRA. For this reason the remainder of the thesis focused on this organism,

particularly with respect to generation of information required by the PRA process.

Utilising an existing, but previously unanalysed fruit fly trapping database for PNG, I

carried out a Geographic Information System analysis of the distribution and

abundance of banana in four major regions of PNG. This information is required for a

PRA to determine if banana fruit grown in different parts of the country are at different

risks from the fly. Results showed that the fly was widespread in all cropping regions

and that temperature and rainfall were not significantly correlated with banana fly

abundance. Abundance of the fly was significantly correlated (albeit weakly) with host

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availability. The same analysis was done with four other PNG pest fruit flies and their

responses to the environmental factors differed to banana fly and each other. This

implies that subsequent PRA analyses for other PNG fresh commodities will need to

investigate the risk of each of these flies independently.

To quantify the damage to banana fruit caused by banana fly in PNG, local surveys and

one national survey of banana fruit infestation were carried out. Contrary to

expectations, infestation was found to be very low, particularly in the widely grown

commercial cultivar, Cavendish. Infestation of Cavendish fingers was only 0.41% in a

structured, national survey of over 2 700 banana fingers. Follow up laboratory studies

showed that fingers of Cavendish, and another commercial variety Lady-finger, are

very poor hosts for B. musae, with very low host selection rates by female flies and

very poor immature survival.

An analysis of a recent (within last decade) incursion of B. musae into the Gazelle

Peninsula of East New Britain Province, PNG, provided the final set of B. musae data.

Surveys of the fly on the peninsular showed that establishment and spread of the fly in

the novel environment was very rapid and thus the fly should be regarded as being of

high biosecurity concern, at least in tropical areas. Supporting the earlier impact

studies, however, banana fly has not become a significant banana fruit problem on the

Gazelle, despite bananas being the primary starch staple of the region.

The results of the research chapters are combined in the final Discussion in the form of

a B. musae focused PRA for PNG banana fruit. Putting the thesis in a broader context,

the Discussion also deals with the apparent discrepancy between high local abundance

of banana fly and very low infestation rates. This discussion focuses on host utilisation

patterns of specialist herbivores and suggests that local pest abundance, as determined

by trapping or monitoring, need not be good surrogate for crop damage, despite this

linkage being implicit in a number of international phytosanitary protocols.

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Table of Contents

Keywords .................................................................................................................................................. ii

Abstract .................................................................................................................................................... iii

List of Tables ......................................................................................................................................... viii

List of Figures ........................................................................................................................................... x

Supplementary material ....................................................................................................................... xiv

Statement of original authorship .......................................................................................................... xv

Acknowledgements ................................................................................................................................ xvi

Chapter 1. Literature review ................................................................................................................... 1

1.1 Introduction ..................................................................................................................................... 1 1.1.1 Agriculture in Papua New Guinea ........................................................................................... 1 1.1.2 Limitations of market access ................................................................................................... 2 1.1.3 Invasive species and export systems ........................................................................................ 3 1.1.4 Overview of chapter ................................................................................................................ 4

1.2 Invasion biology and its role in biosecurity .................................................................................... 5

1.3 Fruit flies as invasive organisms ..................................................................................................... 8

1.4 The study system: banana and banana fly ..................................................................................... 10

1.5 Thesis structure ............................................................................................................................. 13

Chapter 2. Review of banana (Musa spp.) pests in Papua New Guinea ............................................ 17

2.1 Introduction ................................................................................................................................... 17

2.2 Materials & Methodology ............................................................................................................. 19

2.3 Results ........................................................................................................................................... 22 2.3.1 Pest List ................................................................................................................................. 22 2.3.2 Pest Summaries ...................................................................................................................... 27 2.3.3 Pathogens - Bacteria .............................................................................................................. 28

2.3.3.1 Erwinia chrysanthemi Burkholder et al. ................................................................. 28 2.3.4 Pathogens - Fungi .................................................................................................................. 29

2.3.4.1 Cordana musae (Zimm.) ......................................................................................... 29 2.3.4.2 Mycosphaerella fijiensis Morelet ............................................................................ 31 2.3.4.3 Phyllachora musicola Booth & Shaw ..................................................................... 33 2.3.4.4 Ramichloridium musae de Hoog ............................................................................ 34

2.3.5 Insects & Mites - Coleoptera ................................................................................................. 34 2.3.5.1 Cosmopolites sordidus (Germar) ............................................................................ 34 2.3.5.2 Papuana species ...................................................................................................... 35 2.3.5.3 Rhyparida sobrina Bryant ....................................................................................... 37 2.3.5.4 Scapanes australis grossepunctatus Sternberg ........................................................ 38

2.3.6 Insects & Mites - Diptera ....................................................................................................... 39 2.3.6.1 Bactrocera musae (Tryon)....................................................................................... 39

2.3.7 Insects & Mites - Lepidoptera ............................................................................................... 41 2.3.7.1 Erionata thrax (L.) ................................................................................................... 41 2.3.7.2 Nacoleia octasema (Meyrick) ................................................................................. 43

2.3.8 Nematodes ............................................................................................................................. 44 2.3.8.1 Pratylenchus coffeae (Zimmermann) ...................................................................... 44

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2.3.8.2 Radopholus similis Thorne ..................................................................................... 46

2.4 Discussion ..................................................................................................................................... 47

2.5 Thesis Progress ............................................................................................................................. 49

Chapter 3. Distribution and abundance of five economically important fruit fly species in Papua New Guinea ............................................................................................................................................. 51

3.1 Introduction ................................................................................................................................... 51

3.2 Materials and methods .................................................................................................................. 53 3.2.1 Trapping ................................................................................................................................ 53 3.2.2 Databases and analysis .......................................................................................................... 56 3.2.3 Fly species ............................................................................................................................. 57

3.3 Results ........................................................................................................................................... 59 3.3.1 General Patterns ..................................................................................................................... 59 3.3.2 Bactrocera bryoniae (Tryon) .................................................................................................. 62 3.3.3 Bactrocera cucurbitae (Coquillett) ......................................................................................... 67 3.3.4 Bactrocera frauenfeldi (Schiner) ............................................................................................ 71 3.3.5 Bactrocera musae (Tryon) ..................................................................................................... 75 3.3.6 Bactrocera umbrosa (Fabricius) ............................................................................................. 80

3.4 Discussion ..................................................................................................................................... 85

3.5 Thesis Progress ............................................................................................................................. 87

Chapter 4. Infestation of bananas by Bactrocera musae (Tryon) in Papua New Guinea ................. 88

4.1 Introduction ................................................................................................................................... 88

4.2 Materials and methods .................................................................................................................. 90 4.2.1 Differences in varietal susceptibility ..................................................................................... 90 4.2.2 National Cavendish survey .................................................................................................... 92

4.3 Results ........................................................................................................................................... 96 4.3.1 Differences in varietal susceptibility ..................................................................................... 96 4.3.2 National Cavendish survey .................................................................................................. 102

4.4 Discussion ................................................................................................................................... 103

4.5 Thesis progress ............................................................................................................................ 104

Chapter 5. Host selection and utilisation by Bactrocera musae (Tryon) on two banana varieties at different ripening stages ...................................................................................................................... 106

5.1 Introduction ................................................................................................................................. 106

5.2 Materials and Methods ................................................................................................................ 109 5.2.1 Adult host choice and utilisation ......................................................................................... 109 5.2.2 Larval host utilisation .......................................................................................................... 110 5.2.3 Host use of green banana ..................................................................................................... 110 5.2.4 Host data .............................................................................................................................. 111 5.2.5 Analysis ............................................................................................................................... 111

5.3 Results ......................................................................................................................................... 112 5.3.1 Adult Choice ........................................................................................................................ 112 5.3.2 Adult no choice .................................................................................................................... 112 5.3.3 Larval performance.............................................................................................................. 114 5.3.4 Green Cavendish as a host of Bactrocera musae ................................................................. 116 5.3.5 Banana attributes ................................................................................................................. 116

5.4 Discussion .................................................................................................................................. 119

5.5 Thesis progress ............................................................................................................................ 121

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Chapter 6. Bactrocera musae (Tryon) in a novel environment: banana fly as an invasive organism on the Gazelle Peninsula, Papua New Guinea ................................................................................... 122

6.1 Introduction ................................................................................................................................. 122

6.2 Materials and Methods ................................................................................................................ 124 6.2.1 Distribution and spread of Bactrocera musae (Tryon) on the Gazelle Peninsula................. 124 6.2.2 Population abundance and phenology ................................................................................. 126 6.2.3 Impact Studies ..................................................................................................................... 127

Market Surveys (2000-2001) ................................................................................................... 127 Bagging trial (2001-2003) ........................................................................................................ 127 Current damage ........................................................................................................................ 127

6.3 Results ......................................................................................................................................... 128 6.3.1 Distribution and spread of Bactrocera musae (Tryon) on the Gazelle Peninsula................. 128 6.3.2 Population abundance and phenology ................................................................................. 130 6.3.3 Impact studies ...................................................................................................................... 131

6.3.3.1 Fruit rearing (2000-2001) ..................................................................................... 131 6.3.3.2 Bagging trial (2001-2002) .................................................................................... 131 6.3.3.3 Current status ........................................................................................................ 133

6.4 Discussion ................................................................................................................................... 134

Chapter 7. Discussion ........................................................................................................................... 136

7.1 Thesis summary ........................................................................................................................... 136 7.1.1 Introduction ......................................................................................................................... 136 7.1.2 Summary .............................................................................................................................. 136

7.2 PRA for PNG Banana .................................................................................................................. 137 7.2.1 Definitive statement of IPPC PRA process ......................................................................... 137 7.2.2 Summary on PNG banana PRA ........................................................................................... 138 7.2.3 Detailed PRA response for banana fly ................................................................................. 139

7.3 Implications of thesis for wider fruit fly market access issues ..................................................... 141 7.3.1 Trap abundance and host use by fruit flies .......................................................................... 142 7.3.2 How does this relate to Market access? ............................................................................... 144

References ............................................................................................................................................. 145

Appendices ............................................................................................................................................ 169

Appendix 1 Fruit flies in Papua New Guinea ................................................................................... 169

Appendix 2 Distribution and biogeography of Bactrocera and Dacus species (Diptera: Tephritidae) in Papua New Guinea ........................................................................................................................ 182

Appendix 3 Introduction and distribution of Bactrocera musae (Tryon) (Diptera: Tephritidae) in East New Britain, Papua New Guinea .............................................................................................. 192

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List of Tables

Table 1.1 Host plants for Bactrocera musae (Tryon) in Australia (Distribution: Torres Strait islands and northeast Queensland, as far north as Townsville). Taken from - The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia (Hancock et al., 2000). ................................................................................................. 12

Table 2.1 Names and history on professional background of formally interviewed agriculture and quarantine field officers ......................................................................................... 20

Table 2.2 Pathogens, arthropods, nematodes and weeds reported associated with banana in Papua New Guinea ....................................................................................................... 23

Table 3.1 Location and number of fruit fly trap sites in four study areas in Papua New Guinea in relation to altitude (m.a.s.l) and annual rainfall (mm) levels used in the Papua New Guinea Resource Information System (PNGRIS) ........................................................ 55

Table 3.2 The monthly trap catch (June 1998 – September 2001) of five economically important fruit fly Bactrocera species in four study areas in Papua New Guinea ....... 60

Table 3.3 Linear regression analysis of the influence of: (i) altitude or (ii) rainfall on the abundance of five Bactrocera species within and across four study areas in Papua New Guinea, or (iii) banana in local cropping systems for B. musae only. Results are R2 values (and probability values in brackets). Note: Analysis not applicable (NA) for altitude in Central because 20 of 21 traps are located at one altitude level, nor for B.musae on the Gazelle due to inconsistent and sporadic sampling (* = P≤0.05). ...... 61

Table 3.4 Multiple regression analysis of the influence of both altitude and rainfall on fly distribution and abundance (P≤0.05) (* = P≤0.05). ..................................................... 61

Table 4.1 Sampling details for the national Cavendish survey ................................................ 94

Table 4.2 Damage assessment records of miscellaneous host records of banana varieties sampled between 1998 and 2000 in Western Highlands, Central, East New Britain, Madang, and Morobe provinces in Papua New Guinea ............................................... 97

Table 4.3 continued…Damage assessment records of miscellaneous host records of banana varieties sampled between 1998 and 2000 in Western Highlands, Central, East New Britain, Madang, and Morobe provinces in Papua New Guinea .................................. 98

Table 4.4 continued…Damage assessment records of miscellaneous host records of banana varieties sampled between 1998 and 2000 in Western Highlands, Central, East New Britain, Madang, and Morobe provinces in Papua New Guinea .................................. 99

Table 4.5 Infestation of Cavendish banana samples for 22 localities in Papua New Guinea. Each sample consisted of about 30 individual fingers collected at mature green stage of ripeness ....................................................................................................................... 103

Table 5.1 Summary two-way ANOVA output table for Cavendish and Ladyfinger fruit attributes at three ripening stages ............................................................................... 117

Table 5.2 continued…Summary two-way ANOVA output table for Cavendish and Ladyfinger fruit attributes at three ripening stages ....................................................................... 118

Table 6.1 Tephritid fruit flies reared from bananas purchased from markets (March to June 2000) or collected from gardens (May to June 2001) on the Gazelle Peninsula, East New Britain, Papua New Guinea ............................................................................... 132

Table 6.2 Infestation of mature green Cavendish banana by Bactrocera musae (Tryon) at four locations on the Gazelle Peninsula, East New Britain, Papua New Guinea, in 2007 . 133

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Table 7.1 Checklist of information available and necessary for carrying out a pest risk analysis of PNG bananas; a pathway initiated analysis ............................................................ 140

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List of Figures

Figure 1.1 (A) The multi-step process of non-native species invasion (Lockwood et al., 2005); and (B) Transitions that non-invasive species must overcome to continue in the invasion process (Kolar & Lodge, 2001) ....................................................................... 6

Figure 1.2 Conceptual model of the process that invasive species go through in their movement from endemic to non-endemic areas ............................................................. 7

Figure 1.3 Pest Risk Analysis process ...................................................................................... 13

Figure 2.1 Report generated by Papua New Guinea Pest List Database in December 2006 of the pests recorded on banana and plantains in Papua New Guinea .............................. 18

Figure 2.2 (A) Fallen banana, cause may be due to rotting of basal pseudostem (sometimes termed ‘tip-over’ by field officers in PNG) (Source: CTAHR Hawaii); and (B) Rotting xylem vessels referred to as internal pseudostem necrosis (Source: CTAHR Hawaii www.ctahr.hawaii.edu/nelsons/banana) ....................................................................... 28

Figure 2.3 Cordana leaf spot on banana leaves (Source: CTAHR Hawaii web site: www.ctahr.hawaii.edu/nelsons/banana) ....................................................................... 29

Figure 2.4 (A) Black Sigatoka on banana leaves (Source: DAFF Australia – AQIS); and (B) Leaf infested with black Sigatoka has yellow transition zones between infected and green uninfected leaf area (Source: CTAHR Hawaii www.ctahr.hawaii.edu/nelsons/banana/) ...................................................................... 31

Figure 2.5 Black-cross on underside of banana leaf of local cultivar. Photo taken at Chanel College, Kokopo, ENB (Source: A. Mararuai) ............................................................ 33

Figure 2.6 (A) Lifecycle and damage caused by banana weevil borer (Source: Cook Islands Biodiversity Database); and (B) Adult banana weevil borer (Source: G McCormack. Cook Islands Biodiversity Database- http://entnem.ufl.edu/creatures/fruit/borers/banana_root_borer.htm) .......................... 34

Figure 2.7 (A) Taro beetle burrows in damaged corm of banana sword sucker (Source: A Mararuai); (B) Adult Papuana woodlarkiana Montrouzier (Source: A Carmichael, PaDIL); and (C) Larvae, pupae and adult taro beetle collected at LAES Keravat, 2005 (Source: A. Mararuai) .................................................................................................. 36

Figure 2.8 Sketch of Rhyparidella sobrina (Bryant) (Source: Gressit (1974)) ........................ 37

Figure 2.9 (A) Pseudostem bore-hole caused by Scapanes australis grossepunctatus (Source: A. Mararuai); (B) S grossepunctatus boring into banana pseudostem (Source: A. Mararuai); and (C) Banana bunch emerging through a hole made by S. grossepunctatus in banana pseudostem (Source: A Mararuai) .................................... 38

Figure 2.10 (A) Adult Bactrocera musae (Source SPC PaciFly); (B) Fruit fly larvae feeding tracks in ripe Cavendish banana variety (Bundun, Morobe Province) (Source: A. Mararuai); and (C) Fruit fly larvae feeding tracks in mature green Cavendish (Kaiapit, Morobe Province) (Source: A. Mararuai) .................................................................... 39

Figure 2.11 (A) Adult Erionota thrax butterfly (Source: K Walker, PaDIL); (B) Caterpillar feeding on leaf (Gazelle Peninsula, ENB) (Source: A Mararuai); (C) Leaves of banana rolled up by banana skipper (Bubia, Morobe province) (Source: A Mararuai); and (D) Pupae in leaf roll (Gazelle, ENB) (Source: A Mararuai) ............................................. 41

Figure 2.12 (A) Adult Nacoleia octasema (NAIC Kilakila, Port Moresby) (Source: A Mararuai); and (B) N. octasema damage on banana fingers (Source: A Mararuai) ..... 43

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Figure 2.13 (A) Female nematode (Source: http://nematode.unl.edu): and (B) Symptoms of Pratylenchus coffeae feeding on banana root (Source: CAB Crop Protection Compendium Module 1) ............................................................................................... 45

Figure 2.14 (A) Illustration of burrowing nematode (Source: http://plpnemweb.ucdavis.edu/Nemaplex); (B) Damage to banana roots caused by the burrowing nematode (Source: http://www.ctahr.hawaii.edu); and (C) Toppled banana (black head) (Source: http://www.ctahr.hawaii.edu/nelsons/banana) ........................... 46

Figure 2.15 Pest Risk Analysis process; with arrow indicating which step in process information generated in this thesis has been collected for .......................................... 50

Figure 3.1 Fruit fly trapping sites used to study the influence of site variables on the distribution and abundance of five economically important fruit fly species in Papua New Guinea .................................................................................................................. 55

Figure 3.2 Fruit fly study species: (A) Bactrocera bryoniae (Tryon) (approximate magnification x5), (B) Bactrocera cucurbitae (Coquillett) (x6), (C) Bactrocera frauenfeldi (Schiner) (x6), (D) Bactrocera musae (Tryon) (x6), and (E) Bactrocera umbrosa (Fabricius) (x5). ............................................................................................. 59

Figure 3.3 Seasonal abundance of Bactrocera bryoniae (Tryon) in four areas in Papua New Guinea between June 1998 and September 2001 .......................................................... 63

Figure 3.4 Mean monthly abundance of Bactrocera bryoniae at different altitude levels in Papua New Guinea between June 1998 and September 2001. ..................................... 64

Figure 3.5 Mean monthly abundance of Bactrocera bryoniae against annual rainfall levels in Papua New Guinea between June 1998 and September 2001 ...................................... 65

Figure 3.6 Seasonal abundance of Bactrocera cucurbitae (Coquillett) in four areas in Papua New Guinea between June 1998 and September 2001 ................................................. 68

Figure 3.7 Mean monthly abundance of Bactrocera cucurbitae at different altitude levels in Papua New Guinea between June 1998 and September 2001 ...................................... 69

Figure 3.8 Mean monthly abundance of Bactrocera cucurbitae against annual rainfall levels in Papua New Guinea between June 1998 and September 2001 ...................................... 70

Figure 3.9 Seasonal abundance of Bactrocera frauenfeldi (Schiner) in four areas in Papua New Guinea between June 1998 and September 2001 ................................................. 72

Figure 3.10 Mean monthly abundance of Bactrocera frauenfeldi at different altitude levels in Papua New Guinea between June 1998 and September 2001 ...................................... 73

Figure 3.11 Mean monthly abundance of Bactrocera frauenfeldi plotted against annual rainfall levels in Papua New Guinea between June 1998 and September 2001 ........................ 74

Figure 3.12 Seasonal abundance of Bactrocera musae in three areas in PNG between June 1998 and September 2001 ............................................................................................. 76

Figure 3.13 Mean monthly abundance of Bactrocera musae at different altitude levels in Papua New Guinea between June 1998 and September 2001 ...................................... 77

Figure 3.14 Mean monthly abundance of Bactrocera musae plotted against annual rainfall levels in Papua New Guinea between June 1998 and September 2001 ........................ 78

Figure 3.15 Mean monthly abundance between June 1998 and September 2001 of Bactrocera musae plotted against the relative importance of banana as a food crop in cropping systems in Papua New Guinea ...................................................................................... 79

Figure 3.16 Seasonal abundance of Bactrocera umbrosa in four areas in PNG between June 1998 and September 2001 ............................................................................................. 81

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Figure 3.17 Mean monthly abundance of Bactrocera umbrosa at different altitude levels in Papua New Guinea between June 1998 and September 2001 ...................................... 82

Figure 3.18 Mean monthly abundance of Bactrocera umbrosa plotted against annual rainfall levels in Papua New Guinea between June 1998 and September 2001 ....................... 83

Figure 3.19 Mean monthly abundance between June 1998 and September 2001 of Bactrocera umbrosa in Papua New Guinea where breadfruit (Artocarpus spp.) is grown ............. 84

Figure 3.20 Pest Risk Analysis process; with arrow indicating which step in process information generated in this chapter has been collected for ....................................... 87

Figure 4.1 Map of harvest spots for Cavendish banana during the fruit fly damage assessment survey (November 2007-January 2008) carried out in five provinces in Papua New Guinea .......................................................................................................................... 93

Figure 4.2 Mean (± SE) fruit fly infestation in finger samples collected from three locations on a banana bunch (top, middle, bottom). Finger samples were from three banana varieties; Kekiau, Vudu Papua, and Tukuru ............................................................... 100

Figure 4.3 Bactrocera species infestation of bunches from four banana varieties (Daru, Kurisa, Kalapua and Babi) grown in a common garden at Laloki, Papua New Guinea ......... 101

Figure 5.1 Number of oviposition events and subsequent number of emergent flies from single ripe fingers of two banana varieties when offered in a choice arena to single female Bactrocera musae (n=16 for each variety) ................................................................. 113

Figure 5.2 Number of oviposition events (darker shade) and subsequent number of emergent flies (lighter shade) from single fingers of Cavendish and Ladyfinger banana varieties at three stages of ripeness when offered in a choice arena to single female Bactrocera musae (n=16 per variety/ ripeness combination) ....................................................... 114

Figure 5.3 Number of emergent flies from single fingers of two banana varieties at three stages of ripeness when offered in a no-choice arena to single female Bactrocera musae (n=16 banana fingers per variety/ ripeness combination) ............................... 114

Figure 5.4 Mean (± SE) number of flies reared from individual fingers of two banana varieties at three ripeness stages when inoculated with 20 Bactrocera musae eggs (n=16 inoculated banana fingers per variety/ ripeness combination, 60 eggs per banana) ... 115

Figure 5.5 Mean (± SE) number of Bactrocera musae emerging from green Cavendish bananas following the exposure of 500gm of banana to 25 gravid female flies (n = 5 replicates). Emergence of flies from ripe fruit (n = 1 replicate) is a positive control, demonstrating that the flies used to run the trial were gravid. It should not be used to compare yield of flies from green versus ripe fruit .................................................... 116

Figure 5.6 Mean (± SE) fruit attributes for two banana varieties at three stages of ripeness. Letters above columns denote significant difference in the fruit attribute between ripeness stages within the one banana variety (based on 1-way ANOVA with a Tukey’s post-hoc test at p < 0.05) .............................................................................. 119

Figure 6.1 The Gazelle Peninsula, East New Britain Province, Papua New Guinea. The three highlighted localities are where impact trials were carried out .................................. 126

Figure 6.2 Distribution of Bactrocera musae (Tryon) on the Gazelle Peninsula, East New Britain, Papua New Guinea in mid 2000. Source: Mararuai et al. (2001) ................. 129

Figure 6.3 Distribution of Bactrocera musae (Tryon) on the Gazelle Peninsula in December 2000. Source: Mararuai et al. (2001) ......................................................................... 129

Figure 6.4 Distribution of Bactrocera musae (Tryon) indicated by red pins on the Gazelle Peninsula in June 2009; pins mark village residential areas surrounded by vegetables gardens, plantations, secondary or primary rainforest ................................................ 130

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Figure 6.5 Phenology curve of Bactrocera musae (Tryon) on the Gazelle Peninsula (East New Britain, Papua New Guinea (PNG)) (from April 2002 to July 2003) compared with curves in three areas on the PNG mainland (from 1999 to 2001) ............................... 131

Figure 6.6 Infestation of banana bunches protected (bagged) or unprotected (unbagged) from Bactrocera musae (Tryon) on the Gazelle Peninsula, East New Britain, Papua New Guinea ......................................................................................................................... 132

xiv

Supplementary material

Attached is a CD-Rom that includes three supplementary appendices: Appendix 1

contains pdf versions of all formally published literature used in developing the list of

organisms associated with banana in PNG; Appendix 2 has pdf versions of all the

informal ‘grey’ information used in that study, while Appendix 3 contains the

questionnaire.

xv

Statement of original authorship

The work contained in this thesis has not been previously submitted to meet

requirements for an award at this or any other higher education institution.

Data and text extracts of the following publication:

Mararuai, A., Allwood, A.J., Balagawi, S., Dori, F., Kalamen, M., Leblanc, L.,

Putulan, D., Sar, S., Schuhbeck, A., Tenakanai, D., & Clarke, A.R. (2001). Introduction

and distribution of Bactrocera musae (Tryon) (Diptera: Tephritidae) in East New

Britain, Papua New Guinea. Papua New Guinea Agricultural Journal, 45, 59-65

have been used in Chapter 6 of this thesis because the paper contains information

which is an integral component of the larger research area that chapter covers. I am the

first author on the publication and took part in all activities reported in it.

To the best of my knowledge and belief, the rest of the thesis contains no material

previously published or written by another person except where due reference is made.

Signature

Date

xvi

Acknowledgements

My journey through the making and the telling of this story has not been a ‘magical red carpet’ ride. But like all veteran ships of the seven seas you need a good crew and a wise captain to take it through all the rough and stormy weather. I am not a veteran ship but I have had the privilege of having such a supportive crew and a good captain; if I can put it that way. They’ve held me together and I’ve weathered the storms to reach this port. I am grateful to many for the time, consideration, support and understanding you have all given during my journey. Thank you to the Institutions I have worked with and their staff: PNG National Agriculture Research Institute, Australian Centre for International Agriculture Research, Queensland University of Technology & School of Natural Resource Sciences, PNG National Agriculture and Quarantine Inspection Authority, Fresh Produce Development Authority, Queensland Department of Primary Industries & Fisheries (Indooroopilly & Cairns), and Secretariat of the Pacific Community. To ACIAR, thank you for your faith in me and for the considerable support and understanding along the way, I hope I have fulfilled your aspirations in selecting me for the John Allwright Fellowship Award. To my supervisors: Tony, Grant, Ian, and help from Raghu - I don’t know how to say thank you. There are no words so I simply say ‘bikpela tenkyu tumas’ To my family, thank you, know that I am still the same person. A big thank you to my friends, in particular: Amy, Trish, Helen, ‘Boss man’ David, Fred, Rosa, Roy, Tim, Anna, Sol, Eilish, Aunty Janet and Howard. To my godmother Ena and Tom, thank you for listening and helping me find my wings. And a special thank you to my son Laurence: I wish I had the same courage as you at the age of four to be so brave and understanding in supporting me by living apart at this time.

1

Chapter 1. Literature review

1.1 Introduction

1.1.1 Agriculture in Papua New Guinea

Papua New Guinea (PNG), the largest of the Pacific Island Nations and Territories,

relies heavily on its agricultural sector for both internal food security and export

earnings. Agriculture at the subsistence, semi-commercial and commercial level is

practiced throughout Papua New Guinea (Hanson et al., 2001). Over 80% of the

population of PNG live through subsistence agriculture, while a large percentage of the

remainder practice or partake in commercial agriculture for domestic and international

markets (Allen et al., 1995; Asafu-Adjaye, 1996; Bourke, 2001; Allen et al., 2005).

Agriculture is a main economic activity for rural people (Bourke & Vlassak, 2004),

providing income generation from the sale of crops (fruit, nuts, vegetables, leafy

vegetables) and/or livestock (poultry, pigs) (Thompson, 1986; Allen et al., 1995; Coelli

& Fleming, 2004).

Improvement in production and management activities in the agriculture sector,

particularly that which leads to greater farmer cash incomes, can be a catalyst for

broad-based economic growth and development including enhanced access to health,

education and information (Shack et al., 1990; Duncan & Temu, 1995; Benjamin et al.,

2001; Gwaiseuk, 2001; Allen et al., 2005). Unfortunately, as with many developing

countries, PNG lacks much of the underpinning scientific research which is needed to

drive significant increases in rural agricultural production (Allen et al., 1995; Ohtsuka

et al., 1995). Pest management in agriculture production is an example of one area.

Standardised quantification of pest damage on crops and the proper identification and

collation of pest information is generally lacking, despite this information being

essential in improving harvestable yields and market quality. The country also does not

have an appropriate and recognised pathway through which commodities may be

produced and suitably prepared for market (Wamala, 2001). This is especially true for

fresh commodities.

In January 2006, a national workshop on fresh commodity pathways called

Commodity Pathways for Main Exported Commodities (ginger, taro, banana,

asparagus, etc) was held in Port Moresby, the capital of PNG. The workshop identified

2

problems in commodity supply and infrastructure affecting rural industries in the

country. Through the support of current PNG National and Regional initiatives, it is

considered that long term industry goals targeting international fresh commodity trade

at a regional level are achievable. Biosecurity standards for potential export

commodities are yet to be established and commodity pathways do not exist, but

establishment of fresh commodity export will enhance socio-economic levels in the

country. There is a large range of potential fresh commodity export crops in PNG,

including mango, pawpaw and banana. As part of the commodity pathway workshop it

was decided that a single commodity should be used as a case study upon which to

focus and guide future research and development. The commodity that was chosen was

banana and the research presented in this thesis is directed at supporting that national

initiative.

Banana (Musa spp.) is an important staple food crop in PNG (Bourke et al., 1998;

Gibson, 2001b; Gwaiseuk, 2001; Bourke & Vlassak, 2004). It is cultivated from sea

level to elevations above 2000 meters and is grown in over 300 of PNG’s agricultural

cropping systems (Bellamy & McAlpine, 1995; Bourke et al., 1998; Hartemink &

Bourke, 2001; Gunther et al., 2003). The fruit is sold in almost all rural and urban

markets, with an annual production of about 413,000 tonnes which generates an

estimated PNG Kina 150 million (Gibson, 2001a); hence it is the second most

important national food crop after sweet potato (Ipomoea batatas) (Gibson, 2001a;

Bauer et al., 2003). Banana is a commodity produced and marketed largely in its fresh

state and, therefore, as a potential export commodity it will be subjected to more

stringent trade protocols than those imposed on exported processed commodities (e.g.

coffee and cocoa beans). International market access for PNG bananas is reliant on

knowledge of the biosecurity threats posed by its associated pests. There is, however,

very limited formal literature on the pests of PNG bananas, with most information

being available through unpublished expert knowledge or in non-refereed (and hence

non-verified) “grey literature”.

1.1.2 Limitations of market access

Provision of information on commodity pests by an exporting country is an essential

and compulsory part of trade negotiations prior to gaining export approval for a fresh

commodity (Follett & Neven, 2006). The information provided should include the

3

identification of pest(s) of the commodity and pathways through which the pest(s) may

travel; the assessment and categorisation of a pests’ status; the probability of

introduction, spread and economic impact of the pest(s); and finally risk management

of the pest(s) (IPPC, 2004a, 2006a). Under guidelines of the International Plant

Protection Convention (IPPC, 2004a, 2008), this collection of information is referred

to as the Pest Risk Analysis (PRA). PRA information should be generated using

standardised analytical approaches that produce scientifically credible data and be

reported in a transparent manner to convey accurate understanding (Alvarez-Coque &

Bautista, 1994; Gray et al., 1998; Zepeda et al., 2001; Lugard & Smart, 2006).

Inability to provide sufficient PRA information to trading partners and the lack of

knowledge, awareness and effectiveness in the monitoring and management of pests is

a major limitation for many developing countries (Duncan & Lutz, 1983; Markelova et

al., 2009). This limitation causes difficulty in accessing and maintaining market access

to industrial country markets. Other reasons for poor market access of developing

country fresh commodities include central governing support systems inflexible to

market changes, poorly developed financial systems, high costs in legal or non-legal

transactions and a lack of trust in banking and financial transactions (Margolis et al.,

2005; Schillhorn van Veen, 2005). Papua New Guinea is one country which has yet to

establish some of these systems for fresh agricultural crop commodities (Kannapiran,

2000; Manning, 2001).

1.1.3 Invasive species and export systems

Successfully established invasive pest species can result in negative social (Drew,

1996), economic (Perrings, 2005) and environmental (Usher, 1988; Zavaleta et al.,

2001) impacts in the countries or regions where they establish (Hennessy, 2008).

Biological security (= biosecurity) protocols exist to monitor and regulate trade

pathways to prevent the spread of such potentially invasive pests. International

standards (IPPC, 2006a) exist which, for signatory countries, describe quarantine

protocols that must be followed in order to minimise the risk of movement of plant

pests through trade, while allowing that international commodity trade to continue.

Regulatory biosecurity standards describe a set of procedures or measures established

to safeguard the flora and fauna (both agricultural and native) of a country, or a

particular area within a country, against exotic pests. These standards, in part, draw

4

from research from the scientific field of invasion biology; a field which studies the

[generally human aided] movement and establishment of invasive organisms from

endemic to non-endemic areas. There are generally considered to be four stages in the

invasion process; introduction, establishment, reproduction and spread (Lockwood et

al., 2005). Management of invasives at the introduction phase is identified as being the

most effective, both practically and cost wise (Myers et al., 2000; Maynard et al.,

2004; Hennessy, 2008).

A wide array of diverse fields are encompassed by biosecurity, including higher

education, scientific research, administration and policy, media, politics, trade and

industry (Whittle, 2004). Market access is one component of biosecurity and focuses

on establishing commodity export markets in the presence of biosecurity requirements

(e.g. within-field or post-harvest controls) imposed by an importing nation (Duncan &

Lutz, 1983). Countries may impose different equivalent conditions and systems in

order for an exporter to meet market access requirements.

1.1.4 Overview of chapter

In the absence of biosecurity protocols for market access, PNG will not be able to

market its fresh agriculture produce at an international level. As part of the process for

developing appropriate biosecurity protocols for PNG commodities, especially banana,

this thesis covers and provides components of the total information required for a PNG

banana PRA. The components vary from reviews of existing, but poorly documented

(i.e. “grey”) knowledge, through to the generation of new scientific data. To establish

the context of the thesis, this chapter provides an overview of the biosecurity

requirements required for market access of fresh commodities and the reasons why

they are necessary. It introduces and reviews pertinent aspects of the invasion biology

theory, which provides the scientific underpinning for many biosecurity protocols.

Following from that, fruit flies (Diptera: Tephritidae) are introduced and the reasons

why they are of such high global biosecurity concern and why fruit fly susceptible

commodities are stringently monitored. The review then focuses in on the study

system, introducing PNG bananas and their pests, and explains why particular focus

within the thesis is given to Bactrocera musae (Tryon) (Diptera: Tephritidae: Dacinae),

the banana fly. The last section of this chapter formally outlines the thesis structure.

5

1.2 Invasion biology and its role in biosecurity

Invasion biology covers the processes which occur when an organism moves from an

endemic to a non-endemic area, establishes in that new area, and then spreads out from

that area. The organism involved in such a process is called an invasive species and

there is often a need for its management as many invasive species often have negative

environmental or economic impacts in the new area (Higgins et al., 1999; Parker et al.,

1999; Park, 2004). Biosecurity protocols aim for entry prevention, monitoring, post-

entry management and/or eradication of a potential or actual invasive organism and

only through understanding the processes involved in biological invasions can

appropriate international protocols be established (Myers et al., 2000).

Several descriptions of the process of biological invasion have been published: all have

in common an initial movement of an invasive species into a new area, where the

invasive subsequently settles and, if successful, establishes and spreads. I cover three

such descriptions of biological invasions to illustrate their commonalities and relatively

minor differences. Lockwood et al. (2005) proposed what they termed ‘the multi-step’

invasion process (Figure 1.1A). This model identifies an initial phase of the invasion

where the invasive organism is transferred by a vector from its native habitat into a

non-native habitat. During the second phase of ‘establishment’ the invasive organism

acclimatises to the new local environment and likewise the environment to the

invasive. Successful establishment then leads to the third phase, ‘population growth’.

As the population increases and secondary natural and/or anthropogenic dispersal

occurs, the fourth phase may be reached when invasive individuals disperse from the

initial area of introduction. Vermeij (1996) divided the invasion process into three

successive stages: arrival, establishment, and integration. Arrival (analogous to the

Transfer and Release stages in the Lockwood et al. (2005) model) is defined by the

dispersal of individuals to the recipient region, occurring naturally or with the aid of

humans. Establishment implies that the new population can sustain itself through local

reproduction and/or recruitment. Integration occurs when, as the invading species

forges ecological links with other species in the recipient region, local adaptive

evolution occurs, reflecting a changed selective regime in the recipient community.

The invasion model of Kolar & Lodge (2001) has similarities to the above two models,

but additionally describes the invasion process as having ‘transition’ periods and the

authors assert that each stage is discrete (Figure 1.1B). Invasive species must

6

successfully pass through the different transition stages of transportation, release,

establishment and spread to continue through the invasion process. Incorporating all

three of the invasion process models into a single consensus model confirms the

following four basic stages: arrival, establishment, population growth and range

expansion (Figure 1.2). A conceptual model which breaks the invasion process into

discrete successive stages has both theoretical and applied benefits. From a

management perspective, targeting the early stages of arrival and establishment has

been deemed most effective when developing management strategies against invasive

species (Ruesink et al., 1995; Carey, 1996; Kolar & Lodge, 2001).

Species entrained in transport pathway

Fails in transport

Survives transport and introduction

Fails to establish

Establishment

Non-invasive

Invasive

Uptake from native range

Transfer via vector

Population increase and range expansion

Establishment

Release; arrival

A B


Fails in transport


Fails to establish

Establishment

Non-invasive

Invasive


Fails in transport


Fails to establish

Establishment

Non-invasive

Invasive


Transfer via vector


Establishment

Release; arrival


Transfer via vector


Establishment

Release; arrival

A B

Figure 1.1 (A) The multi-step process of non-native species invasion (Lockwood et

al., 2005); and (B) Transitions that non-invasive species must overcome to

continue in the invasion process (Kolar & Lodge, 2001)

7

Arrivaldispersal routes, human transport

Establishmentacclimatisation, breaking down ecological resistance

Population growthhave a minimum viable population, reproduction increases

Expansionspread and in the process influences the new environment for support

Arrivaldispersal routes, human transport

Establishmentacclimatisation, breaking down ecological resistance

Population growthhave a minimum viable population, reproduction increases

Expansionspread and in the process influences the new environment for support

Figure 1.2 Conceptual model of the process that invasive species go through in their

movement from endemic to non-endemic areas

Within the invasion process, arrival and establishment have been found to be the two

areas which, when targeted, are most likely to give positive outcomes in management

(Drew, 1996; Williamson & Fitter, 1996; Maynard et al., 2004; Hochberg & Gotelli,

2005). This is because populations are generally small and can be controlled or

potentially eradicated. The arrival stage describes the natural or anthropogenic

movement of an organism from an endemic area to the non-endemic area (Vermeij,

1996), while establishment refers to the persistence of an immigrant population by

means of local reproduction and recruitment (Vermeij, 1996). Establishment may be

accompanied by sporadic spreading of the population in the recipient region

(Ebenhard, 1989).

Successful establishment of an invasive organism is commonly related to positive

propagule pressure (Kolar & Lodge, 2001; Lockwood et al., 2005). Propagule pressure

is a measure of the number of individuals released into a region to which they are not

native (Carlton, 1996) (also termed ‘introduction effort’, (Blackburn & Duncant,

2001)) and incorporates estimates of the absolute number of individuals involved in

any one release event (propagule size) and the number of discrete release events

(propagule number). Propagule pressure increases as the number of releases and/or the

8

number of individuals released increases (Lockwood et al., 2005; Memmott et al.,

2005). Many invasive species have low establishment success, but once introduction

succeeds then there may be rapid population growth (Shigesada & Kawasaki, 1997;

Christian & Wilson, 1999; Sax & Brown, 2000). Reducing the chance of entry or

establishment by reducing propagule pressure and/or initial population size is the key

objective of trade related biosecurity measures.

The spread of invasive species is related to international trade and travel and the likely

continuity of new invasions is linked to the increasing demand, efficiency and ever

shortening travel times of the global transport industry (McAusland & Costello, 2004;

Perrings, 2005; Cook & Fraser, 2008). Management and monitoring of invasive

organisms in such situations becomes difficult, but the utilisation of the invasion

process identifies optimum stages where control and monitoring activities are best

applied (Everett, 2000; Hall & Hastings, 2007). Identification of pests and the likely

pathways through which they can move is therefore an essential investigatory

component in the management of invasive species.

Numerous global invasions have occurred in the area of agriculture and horticulture

which have negatively affected agricultural communities and associated stakeholders

(Allwood & Leblanc, 1996; Drew, 1996; Maynard et al., 2004). The trade of export

commodities in agriculture requires the establishment of globally accepted standards of

pest management before acquiring, and then while maintaining, market access (Follett

& Neven, 2006). Such standards often require regulating local biosecurity measures,

including pre-harvest control methods such as pesticide use (Vargas et al., 2002; Wang

et al., 2005; Stonehouse et al., 2007; Burrack et al., 2008) and integrated pest

management options (Meats et al., 2003; Follett & Hennessey, 2007; Narrod et al.,

2009), and post-harvest control methods such as packaging and storage of commodities

(Moy & Wong, 2002; Hofman et al., 2003; Follett, 2004; Birla et al., 2005). The more

serious the known impacts of the pest, the more stringent such biosecurity measures

tend to be.

1.3 Fruit flies as invasive organisms

Global monitoring and management of one particular group of crop pests, the true fruit

flies (Diptera: Tephritidae) is especially stringent (Aluja & Mangan, 2008). Within the

9

Tephritidae, members of the subfamily Dacinae are particularly important as one of the

most globally recognised groups of insect pests attacking fruit and vegetable crops

(Fletcher, 1987; Aluja & Mangan, 2008). Dacine fruit flies are frugivorous insects, the

immature life stages of which feed and develop in fruit and seed pods (Fletcher, 1987).

Most dacine species are monophagous (feed on one host species) or oligophagous

(narrow range of related hosts), while a few, commonly the serious pest species, are

polyphagous (wide range of hosts) (Christenson & Foote, 1960). The Dacinae are

recognized for their invasiveness in tropical, sub-tropical and temperate regions of the

world, although not all species are invasive (Hardy, 1991; Carey, 1996; Drew, 1996).

For the remainder of this thesis, unless otherwise specifically referred to, the term

“fruit fly” refers to members of the Tephritidae, sub-family Dacinae.

Fruit flies possess morphological and biological characteristics that are thought to

increase their invasive potential. For example, some species (e.g. Bactrocera dorsalis

(Hendel), B. carambolae Drew & Hancock, B. philippinensis Drew & Hancock, and B.

papayae Drew & Hancock) have longer and stronger ovipositors than other related

species (Drew et al., 2008), enabling female flies to penetrate thicker and denser

epidermal layers of host fruits, resulting in a broader host range than related flies

(Drew & Hancock, 1994; Allwood et al., 1999). Aggressive territorial behaviour also

allows populations to dominate the areas they invade (Christenson & Foote, 1960),

creating aggressive competition for resources that have also been speculated to drive

fruit fly invasions (Duyck et al., 2004). Flexibility in temperature requirements for life

stage development may also enable adaptation and survival of fruit flies in different

regions with different temperature regimes (Zhou et al., 1994). For example,

Bactrocera cucurbitae (Coquillett) and B. dorsalis are able to reproduce and survive in

both low and high temperature environments (Vargas et al., 2000b; Vayssieres et al.,

2008).

Commodities susceptible to fruit fly (generally fresh fruits and some vegetables) are

internationally traded on a routine basis and the detection of infested commodities

often only occurs after the commodity has entered the area into which it is being

imported. Non-commercial carriage of fresh fruits (i.e. fruit carried by passengers on

boats or planes) poses the same potential risk (Putulan et al., 2004). Establishment of

exotic fruit flies in new agricultural production areas are costly. For example, the

detection of Bactrocera papayae (Asian papaya fruit fly) in Cairns, North Queensland,

10

was detected about two years after introduction. Eradication was achieved but the

exercise involved entire community efforts and direct eradication costs of about

AUD$33M (Drew, 1996; Maynard et al., 2004). This case emphasises the necessity of

ensuring that incursions be prevented and detections be immediately managed.

Another, but slightly different example is the continued presence of invasive Ceratitis

capitata (Weidemann) populations in orchard areas in California. Studies have

determined that the continued presence of C. capitata in closely managed fruit and

vegetable growing areas is due to isolated re-introductions or pockets where

populations have evaded control efforts (Carey, 1996). Management of this pest in

California, which has a US$17 billion fruit industry, requires and drives continued

research into finding solutions to maintain low infestation levels and international

market access (Headrick & Goeden, 1996). In the Pacific, fresh commodity exports of

mango and papaya from countries such as Fiji and Samoa are acceptable only with the

continuous management of invasive fruit fly pests such as B. passiflorae (Froggatt) and

B. xanthodes (Broun) (McGregor, 1996; McLeod, 2005). Such management requires

the use of control methods such as fruit fly trapping networks that keep populations at

low levels, or provide ongoing evidence of ‘area freedom’ status (Allwood, 1996b;

Papadopoulos et al., 2001). Orchard areas in the southern states of Australia also

maintain market access based on area-free zones, which are tightly regulated and

actively managed (Fletcher, 1974; Maelzer et al., 2004).

1.4 The study system: banana and banana fly

Bananas (Musa spp.) are endemic to Southeast Asia and the Pacific. Papua New

Guinea is geographically located at the centre of that diversity range and has the

highest banana diversity of any nation in the Pacific region (Kingwell et al., 2001). The

diversity of banana in PNG consists of over 200 genetic variations identified to be pure

or hybrid varieties of Musa acuminata and other wild Musa species. There are diploid,

triploid, tetraploid and fe’i varieties cultivated throughout the country (Arnaud &

Horry, 1997).

Cultivation and production of banana in PNG is continuously and negatively affected

by pests. There is little formal information available on the pests of bananas in PNG.

Informal pest reports commonly document the following: Nacoleia octasema

(Meyrick) (banana scab moth), Erionota thrax (Linnaeus) (banana skipper),

11

Bactrocera species (fruit flies), nematodes and numerous fungal pests such as

Mycosphaerella musae (leaf speckle), Cordana musae, Deightoniella torulosa,

Guignardia musae (freckle disease of banana), Mycosphaerella fijiensis (black leaf

streak) and Phyllachora musicola (Pone, 1994; Waterhouse, 1997; Kambuou, 2003).

The generation of an entire list of pests of PNG bananas is essential in helping define

which are major or minor, exotic or endemic, and will indicate areas for further

research. Currently there is a lack of research into the quantitative damage levels for

banana pests, their spatial and temporal distribution, and economic impact. Field

observations and reports show the presence of pests in different parts of the country but

evaluation of damage or economic impact with the use of non-standardised survey

methods do not allow for national or regional comparison.

Substantial informal knowledge (e.g. (Pone, 1994; Waterhouse, 1997; Leblanc et al.,

2001; Kambuou, 2003) and limited formal research (Smith, 1977b; Fletcher, 1998)

indicate one fruit fly species, B. musae, as perhaps the most important insect pest of

cultivated bananas in PNG. Bactrocera musae occurs in far northern Queensland,

Australia, and PNG (Drew, 1989). The species is not uniformly distributed in PNG

(pers. obs.) and it is invasive in some PNG island provinces (Mararuai et al., 2001).

Detailed spatial and temporal distribution information for the fly is limited, but fruit fly

surveys in PNG show that it is widespread on the mainland (Clarke et al., 2004).

Distribution of the fly in the island provinces of PNG is less clear, but it has been

trapped and bred from bananas in East New Britain where it is becoming widespread

over most of the Gazelle Peninsula; this population is recently invasive (Mararuai et

al., 2001). Banana fly specimens have been collected on Lihir Island (New Ireland

Province) and Manus, but it is not confirmed whether permanent breeding populations

occur there (Leblanc et al., 2001).

In its natural range, the primary host of B. musae is banana, with a single record only

from papaya. In PNG the fly causes commercially significant damage to eating and

cooking bananas. In Australia, B. musae has been recorded from 12 host species, from

10 genera and nine families (Hancock et al., 2000), but the majority of records are

from banana (Hancock et al., 2000; Leblanc et al., 2001) (Table 1.1). Banana fly has

been demonstrated in the laboratory to show a high preference for bananas over other

fruit (Fitt, 1986) and field officers in PNG have observed that there may be preferential

selection of banana varieties, based on varying infestation levels (Smith, 1977b).

12

Table 1.1 Host plants for Bactrocera musae (Tryon) in Australia (Distribution: Torres

Strait islands and northeast Queensland, as far north as Townsville). Taken

from - The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in

Australia (Hancock et al., 2000).

Host species Common name

Reference Comments

CAPPARACEAE Capparis lucida coast caper Hardy 1951 one specimen only CARICACEAE Carica papaya pawpaw Hardy 1951, QDPI Papaya fruit

fly database (1995-1999) occasional host

MUSACEAE Musa banksii native banana Hardy 1951, May 1953, QDPI

Papaya fruit fly database (1995-1999)

major host

Musa x paradisiaca (=acuminata)

banana Hardy 1951, QDPI Papaya fruit fly database (1995-1999)

not known from hard green

Musa x paradisiaca dwarf banana May 1953, QDPI Papaya fruit fly database (1995-1999)

Musa x paradisiaca lady finger banana

QDPI Papaya fruit fly database (1995-1999)

Musa x paradisiaca sugar banana QDPI Papaya fruit fly database (1995-1999)

Musa x paradisiaca plaintain May 1953, QDPI Papaya fruit fly database (1995-1999)

MYRTACEAE Psidium guajava guava Hardy 1951,May 1960, QDPI

Papaya fruit fly database (1995-1999)

occasional host

Syzygium bamagense Drew 1989 OLACACEAE Ximenia amerciana putit QDPI Torres Strait database

(1993-1995)

PASSIFLORACEAE Passiflora edulis passionfruit QDPI Papaya fruit fly database

(1995-1999) two records

RUBIACEAE Lasianthus strigosus blue rubi QDPI Papaya fruit fly database

(1995-1999) one specimen only

RUTACEAE Citrus paradisi grapefruit QDPI Papaya fruit fly database

(1995-1999) one specimen only

Citrus reticulata mandarin QDPI Papaya fruit fly database (1995-1999)

one record from ripe fruit

SOLANACEAE Solanum lycopersicum

tomato QDPI Papaya fruit fly database (1995-1999)

one record from ripe fruit

13

1.5 Thesis structure

The information presented in this thesis aims to provide some of the underpinning

scientific knowledge required to set up biosecurity standards for PNG bananas,

information which is essential for gaining international market access for one or more

varieties of this commodity. The term ‘PNG bananas’ is used throughout the thesis and

where it is used it refers to the fruit of the banana, unless specified otherwise. One

thesis alone can never supply all that information, for there are a large number of

potential pest species associated with this commodity. This thesis does, however,

initially identify and categorise the status of all pests associated with the banana plant

in PNG, before focusing towards one major insect pest, the banana fly. The research

approach used here follows the Pest Risk Analysis (PRA) process as defined by the

International Standards for Phytosanitary Measures presented by the Food and

Agricultural Organisation of the United Nations (IPPC, 2006a) (Figure 1.3). While I

will not address all components of a PRA, I have identified key components, within

each of the three stages that make up the PRA process, thus helping focus my research.

The three stages in the PRA process are: (i) Risk Initiation [Identify pest(s) and

pathways of concern, and consider whether the pest should be considered for risk

analysis in relation to the area at risk]; (ii) Risk Assessment [Assess (a) the risk of

entry; (b) the risk of establishment; and (c) the risk of economic and other impacts];

and (iii) Risk Management [Review risk management options (e.g. import

restrictions, invasion tactics)].

RISK MANAGEMENTReview risk management options (e.g. import

restrictions, invasion tactics)

RISK ASSESSMENTAssess (a) the risk of entry; (b) the risk of establishment; and (c)

the risk of economic and other impacts

RISK INITIATIONIdentify pest(s) and pathways of concern, and consider whether the pest should

be considered for risk analysis in relation to the area at risk

3

2

1







3

2

1

Figure 1.3 Pest Risk Analysis process

14

In addressing the initial step in the PRA process, Risk Initiation, Chapter 2 of this

thesis is a review of the pests of PNG bananas. While the thesis subsequently focuses

on B. musae, as a major pest of PNG banana fruit, there are no available collations,

reports, or lists of all other known banana pests. This chapter is therefore aimed at

identifying and collating as much information as is possible on banana pests in PNG.

The chapter is more than a simple, desk-based literature review, as it utilises, in

addition to refereed literature, structured interviews with PNG researchers and

“investigative” research sorting through personal unpublished files and grey-literature

kept by individuals or PNG field research-station libraries. The outcome of this chapter

showed that while there are over 100 organisms associated with the banana plant in

PNG, only 14 are of sufficient concern that they are regularly managed. Of these 14,

13 already have significant existing information which can be used towards a PNG

banana fruit PRA. In contrast to those 13, required information for the banana fly,

Bactrocera musae, is almost entirely lacking. As a result of this review, the decision

was made to focus the remainder of the thesis on banana fly.

Thesis chapters’ three to six provide new information on B. musae pertinent to

providing information required by a PRA. Information covered includes distribution

and abundance, crop impacts and invasive potential (detailed more fully below). The

information provided in any one chapter does not easily slot into one particular step of

the PRA as does Chapter 2. Rather, chapters’ three to six provide information which

can be applied to different facets of both steps two and three of the PRA. The pulling

together of this information for a PRA is undertaken in the final Discussion chapter.

While Bactrocera musae is endemic to PNG, this need not imply that banana fly is

uniformly distributed or abundant within PNG. Knowledge of the distribution and

abundance of a pest species is important within a PRA both to gauge potential risk.(e.g.

assessing areas where crop infestation is most likely) and also for risk management

(e.g. growing crops within areas of low pest pressure). Chapter 3 uses an existing, but

previously unanalysed data set to investigate the spatial and temporal distribution of B.

musae and four other pest fruit flies in PNG and factors influencing that distribution.

The detailed local distribution of banana fly in PNG is unknown and without this

information identifying production areas which may be at a higher or lower risk from

the fly is impossible. The other pest fruit fly species are included as they allow a

15

comparative study, of broader ecological and applied interest, about factors impacting

on the abundance of fruit flies in tropical regions.

Following from Chapter 3, Chapter 4 investigates if the same banana variety,

Cavendish, grown in different geographic areas of PNG has higher or lower risk of

banana fly infestation. Cavendish is an economically important banana variety in PNG

and is a variety likely to be considered for export from PNG. As such, it is a basic

requirement for Stages 1 and 2 of the PRA process that banana fly infestation levels

suffered by fruit of this variety in PNG are documented. Further, if in different PNG

agro-ecological regions Cavendish fruit suffer significantly less from banana fly

infestation, then export only from such regions could be used as a risk mitigation step

(PRA Step 3). The Cavendish data is supported by other PNG field data, on the

infestation levels of other banana varieties.

The results of Chapter 4 showed very low field levels of banana fly infestation in

Cavendish fruit, a particularly unexpected result given the general abundance of

banana fly in PNG (Chapter 3) and the perceived pest status of the insect (Chapter 2).

To further investigate host usage by banana fly, and thus better quantify the biological

and economic threat posed by the insect, detailed laboratory studies were undertaken.

Better knowledge of host use is not only important for assessing risk, but also for risk

management. Commodities which are non-hosts, or poor hosts, may have reduced, or

even no risk reduction treatments imposed upon them. Host status, however, can vary

depending on ripening stage of a commodity, or vary between cultivars/varieties of a

commodity, and this needs to be known. In Chapter 5, I use laboratory trials to

investigate host choice and utilisation of B. musae for two economically important

banana varieties, Cavendish and Ladyfinger. I also investigated the influence of fruit

ripening stages on host-use. Key fruit traits (e.g. peel thickness, fruit toughness, etc)

were recorded to investigate if such traits correlate with host use.

A Pest Risk Analysis is an attempt to identify the risks associated with transporting a

commodity, particularly with respect to the likely introduction, establishment, spread

and impact of pests associated with that commodity. By the nature of biosecurity, i.e.

aimed as preventing incursive events, most PRAs can only hypothesise about the likely

impact of an exotic pest. A real incursion, however, gives an opportunity to study a

pest’s post-incursion distribution and abundance, that insect’s economic impact in a

16

novel area, and options for management. In PNG, B. musae was detected as a new

incursive on the Gazelle Peninsula of East New Britain Province in mid 2000. In

Chapter 6 I present information on this incursion, including the flies changing

distribution and, abundance over time, it’s phenology in the novel environment

compared to its phenology in its endemic range, and its crop impacts. The study

provides new information, or supporting information, for all three steps of the PRA

process.

The final discussion chapter (Chapter 7) brings together the results obtained throughout

the thesis by summarising them within the PRA framework, specifically with respect to

a PNG banana fruit PRA. The apparently unusual observation of very high pest

abundance, but very low crop infestation, is also discussed in detail. I conclude that for

specialist herbivores, such as B. musae, such a result should not be unexpected. The

implications of this conclusion for international market access protocols are raised,

specifically that pest trap catch should not be automatically used as a surrogate for crop

risk.

17

Chapter 2. Review of banana (Musa spp.) pests in Papua New Guinea

2.1 Introduction

Banana is an important food and commodity crop in Papua New Guinea (PNG), being

widely cultivated from sea level to above 2000 meters above sea level (m.a.s.l)

(Hartemink & Bourke, 2001; Gunther et al., 2003). Production, however, is often

affected by damage to plant parts caused by pests, or through competition with weeds.

This is a major concern when trying to obtain cross-border market access for PNG

banana because the unrestricted presence of pests of quarantine concern will stop trade.

Globally, plant pathogens are considered the major pests of banana production,

followed by nematodes, insects and mites (Gold et al., 2002). In PNG, there is a range

of pathogens, arthropods and nematodes reported on banana (Kumar, 2001), but only a

few are commonly observed and reported as having an impact on the amount and

quality of bananas produced (Pone, 1994; Waterhouse, 1997; ACNARS, 2003;

Kambuou, 2003). Some of these are endemic while others are not (Shivas & Philemon,

1996; Davis et al., 2000). Schuhbeck (1996), from his surveys in PNG’s island

provinces in the Bismarck Archipelago (i.e. West New Britain, East New Britain,

Manus, New Ireland, and Bougainville), further reported that some PNG banana pest

species endemic to the mainland, are exotic to the islands. Earlier surveys and

publications on PNG banana pests are dominated by insects (O'Connor, 1949; Szent-

Ivany & Barrett, 1956; Szent-Ivany & Catley, 1960; Ostmark, 1974; Smith, 1976) and

some of those insects remain important (Wilkie et al., 1993; Lubulwa & McMeniman,

1998; Mararuai et al., 2001). In more recent reports, pathogens and nematodes have

been added to the national banana pest list (Bridge & Page, 1982; Tomlinson, 1984;

Philemon, 1986; King et al., 1988; Tomlinson et al., 1988). Most of the publications

cited here that list putative pest species on banana are informal (e.g. unpublished

reports of limited circulation), often scarce and difficult to access in either paper or

electronic format. Further, the literature on PNG banana pests is scattered and the few

available summative lists are out dated, incomplete, or both. For example, the work

done by Szent-Ivany and his colleagues is half a century old and was not exhaustive

even when published, but is the most recently prepared formal summative publication

of the insects of banana in PNG.

18

Research conducted as part of this chapter showed that official national records on the

pests found on banana are incomplete and do not even reflect known research done on

banana crop management and plant protection within PNG, let alone representing an

authorative national pest list. Official national records are maintained on the PNG Pest

List Database (PLD). The PLD is an information system that records pest occurrences

within a country, provides reports on their occurrences and is held by the National

Agriculture and Quarantine Inspection Authority (NAQIA) (Masamdu, 2006).

Extraction of records from the PLD, however, found that the database held only six

records, five of these were fungal pathogens, and did not include even well

documented PNG banana pests (Figure 2.1). It was therefore of little use, even as a

starting point, for developing a PRA.

Page 1 of 1 Papua New Guinea Pest Lists Database 22-Dec-06 Hosts with Recorded Pest

Host Pest Literature

.../ ..common Order / common name reference

Musa sp / banana and f Mycosphaerella musae Leaf speckle PNG Plant Protection DB

plantain a Bactrocera bryoniae (Tryon) Drew, 1989

f Cordana musae PNG Plant Protection DB

f Deightoniella torulosa Hyde KD & Philemon E, 1994

f Guignardia musae freckle disease of banana Hyde KD & Philemon E, 1994

f Mycosphaerella fijiensis Black leaf streak PNG Plant Protection DB

f Phyllachora musicola PNG Plant Protection DB

Total number of host-pest: 7

Prepared in collaboration with the:

Plant Protection Service, Secretariat of the Pacific Community

This information is provided in good faith from the best records available at the time. The Secretariat of

the Pacific Community cannot accept responsibility for an consequences arising from the use of this

data. For further information please contact the Government Department and/or the SPC Plant Protection Service.

By request from users, where more than one occurrence of a

Pest has been recorded on the same host,

only a single occurrence is displayed

Figure 2.1 Report generated by Papua New Guinea Pest List Database in December

2006 of the pests recorded on banana and plantains in Papua New Guinea

The obvious incompleteness of official records will seriously impede the processes

involved in acquiring market access for PNG bananas. With PNG’s intention to

investigate the potential of banana as an export commodity, it is an international

requirement to supply an authorative list of the pests of the commodity within the

19

country: defining the pests of a commodity is the first step in the Pest Risk Analysis

(PRA) process, a key element of market access protocols. The primary goal of this

chapter was therefore to document all the pests reported and recorded on banana in

PNG. Further, I review the known biological research and economic impact data of the

most commonly reported organisms as a mechanism of prioritising where further

research is required if market access for PNG bananas is to be gained.

2.2 Materials & Methodology

Sources of Information. Refereed literature on pests of PNG bananas is limited,

restricted in the taxa covered and most of the papers document aspects of the biology

and management of individual pest species. A comprehensive list would require

information from additional sources and thus a search for literature was done and was

able to find formal literature, informal ‘grey’ information and knowledge from local

experts.

The informal ‘grey’ information was not electronically accessible and was collected by

individually visiting and searching the small libraries associated with agricultural

research stations across PNG. Station specific reports were numerous but cataloguing

systems were different in each of the libraries in their level of comprehensiveness and

the individual knowledge of the local librarian proved to be the most useful “search

tool”. As a PNG scientist, I am aware that a great deal of expert knowledge has not

been captured on paper and to overcome this I developed a questionnaire and formally

interviewed agriculture and quarantine field officers (Table 2.1). The surveyed officers

were all internationally and/or locally recognised scientists with research experience in

PNG bananas and most of the grey literature that I accessed in the research station

libraries was authored by individuals from this group. Individual questioning of these

scientists thus not only allowed me to gather new information, but also to clarify any

issues or questions I may have had arising from the reports. The information gathered

from these various sources is presented as a comprehensive list of organisms

associated with banana in PNG. To be included in that list, an organism’s association

with banana had to be confirmed through a primary research paper, research report, or

through consensus with one or more of local scientists.

20

Table 2.1 Names and history on professional background of formally interviewed

agriculture and quarantine field officers

Name Research experience John Bokosou

Over ten years of collective experience in entomological research with the Department of Agriculture and Primary Industry in PNG. A Senior Research Associate with the Entomology section at the National Agriculture Research Institute. Currently based in Keravat (East New Britain).

Fred Dori

Over twenty years of collective experience in entomological research with the Department of Agriculture, Primary Industry and the Coconut Research Institute in PNG. A Senior Entomologist specialised in integrated bio control and pest control research. Is currently retired.

Elick Guaf

Over ten years of experience in food crop agronomy with the Department of Agriculture and Primary Industry in PNG. A Senior Agronomist with the National Agriculture Research Institute based in Lae, Morobe Province. Has acted in the role of Research Programme Leader on several occasions.

Tony Gunua Over ten years of experience in plant protection and pathology research with the Department of Agriculture and Primary Industry in PNG. Now a Senior Plant Pathologist with the PNG National Agriculture and Quarantine Inspection Authority. Was interviewed while on study leave at University of Queensland.

Rosa Kambuou

Over ten years of collective experience in entomological research with the Department of Agriculture and Primary Industry in PNG. A Senior Agronomist specialised in biological science and germplasm conservation. Currently based at the National Agriculture Research Institute at Laloki (Central Province). Extensive knowledge and experience on agronomy, genetic and plant protection aspects of banana research in PNG.

Annastasia Kawi

Over ten years of experience in applied technical plant protection research with the Department of Agriculture and Primary Industry in PNG. At time of interview was on study leave at University of Queensland (Gatton Campus). Now a research Entomologist with the Entomology section at the National Agriculture Research Institute.

Tim Knox and Peter Sale

Tim is a food crop Agronomist with over 20 years experience in semi-commercial farming of fruit and vegetables in PNG. Is currently the Farm manager of a semi-commercial fruit and vegetable farm at the Pacific Adventist University (PAU) located at 12 mile outside Port Moresby on road to Sogeri, Central Province). Peter has a bachelor’s degree in Agriculture from PAU and specialises in food crop agronomy. He has worked at the PAU farm for 10 years.

Kiteni Silvia Kurika

Over ten years of collective experience in entomological research with the Department of Agriculture, Primary Industry and the Coconut Research Institute in PNG. A Senior Research Associate with the Entomology section at the National Agriculture Research Institute and based in Keravat (East New Britain).

Table continued overleaf

21

Table 2.1 continued - Names and history on professional background of formally

interviewed agriculture and quarantine field officers

Name Research experience Louis Kurika

Over ten years of collective experience in entomological research with the Department of Agriculture, Primary Industry and the Coconut Research Institute in PNG. A Senior Agronomist with the National Agriculture Research Institute. Currently based in Keravat (East New Britain). Knowledgeable on island and atoll farming systems.

Gadi Ling

Over ten years of experience in food crop agronomy with the Department of Agriculture and Primary Industry in PNG. Specialised in integrated farming systems particularly the intercropping of cocoa with dominant staple crops such as banana, fruit trees and spice crops. A Senior Agronomist with the National Agriculture Research Institute. Based in Keravat (East New Britain) where he has acted in the role of Research Programme Leader on several occasions.

Meli Lolo

Over ten years of collective experience in entomological research with the Department of Agriculture, Primary Industry and the Coconut Research Institute in PNG. An Agronomist working on a European Union funded project on Atoll agriculture. Based at the National Agriculture Research Institute at Keravat (East New Britain). Extensive experience in germplasm collection on food crops such as banana and green leafy vegetables

Sim Sar

Over ten years of collective experience in entomological research with the Department of Agriculture and Primary Industry in PNG. Senior Entomologist with the PNG National Agriculture Research Institute.

David Tenakanai

Over ten years of experience in entomology research with the Department of Agriculture and Primary Industry in PNG. Now a Senior Entomologist with the PNG National Agriculture and Quarantine Inspection Authority. Was on study leave at University of Queensland at time of interview

Pest Summaries. A comprehensive pest list for PNG bananas has not been previously

generated but there have been partial lists published (Pone, 1994; ACNARS, 2003;

Kambuou, 2003). I have used the “consensus” outcomes of these publications

(specifically if a specific organism is referred to in at least two of these publications),

and the reporting of taxa by multiple local experts during interview, to generate a list

of 14 taxa which are the most commonly observed and managed organisms on banana

in PNG. Investigative research and reporting of these 14 would have been due to them

causing damage to the banana plant or the fruit bunch which would have caused a

reduction in yield and raised farmer concerns. I specifically do not use the term most

“pestiferous”, as in a number of cases the true pest status of an organism is unknown

and guilt is by association, rather than through documentation of impact. Even if some

of these organisms are not true pests, their repeated mention in the literature means

22

they will be priority organisms to be dealt with in any PRA. For these 14 taxa I provide

“pest summaries”, which detail the taxonomy, distribution, accomplished national

biological research and economic impact of these species. This process helps identify

priority areas for further research, as well as providing the type of information needed

to be supplied within a PRA. Economic impact is a crucial section in a PRA however

little information is provided for the 14 taxa and therefore this section is not included

in the pest summaries.

2.3 Results

Supporting Information. The information collected during this review is unlikely to

be gathered again due to the difficulty in accessing the majority of reports and re-

interviewing individuals (some of whom are near retirement age). Due to their

importance as supporting material for the summary information provided in this

section and their importance in the PNG banana PRA and for trade negotiation, the raw

“data” on literature and interview information are provided on a CD-Rom (attached

inside back-cover) as electronic appendices. The CD includes three appendices folders:

Appendix 1 contains pdf versions of all formally published literature; Appendix 2 has

pdf versions of all the informal ‘grey’ information, while Appendix 3 contains the

questionnaire; its format, list and technical qualifications of each interviewed officer,

and recipient answers. The appendices amount to over 150 pages of new, “lost”, or

hard to access information on PNG pests of bananas collated into a single source.

2.3.1 Pest List

There are 112 species of pathogens, arthropods, nematodes and weeds reported to be

associated with banana in PNG. The majority are fungal pathogens, Coleoptera,

Lepidoptera and nematodes. The taxa list is presented in detail in Table 2.2. Some of

the 112 species are known pests of bananas in countries other than PNG (e.g.

Bactrocera papayae Drew and Hancock (Asian papaya fruit fly) (Allwood et al.,

1999)), but their pest status on bananas in PNG is still to be determined. Diseases have

only in more recent years become identified as a problem but banana genetic diversity

may be providing resistance against many pathogens such as the serious pathogen pest

Mycosphaerella fijiensis Morelet (black Sigatoka). The inclusion of nematodes as an

organism associated with PNG bananas originates from a survey by Bridge and Page

(1982). The only nematode species they indicate to be important are Pratylenchus

23

coffeae Goodey (lesion nematode) and Radopholus similis Thorne (burrowing

nematode). Weeds have been included but these have not often been observed as being

a problem for fully established banana plants, particularly in managed gardens

(interviewed officer comments from T. Gunua and D. Tenakanai). They do however

pose problems during the establishment phase of banana plants. Such weeds include:

Mimosa invisa Mart (giant sensitive plant), Rottboellia cochinchinensis (itch grass),

Imperata cylindrical Beauv. (blady grass) and Piper aduncum Linnaeus. Mimosa

invisa and P. aduncum are invasive species in PNG (Orapa, 2006).

Table 2.2 Pathogens, arthropods, nematodes and weeds reported associated with

banana in Papua New Guinea

Pest/ Pathogen Common name Information source

Bacteria Enterobacteriales Entobacteriaceae

Erwinia chrysanthemi Burkholder et al rhizome rot (Tomlinson, 1984)

Erwinia carotovora carotovora (Pectobacterium carotovorum)

(Tomlinson, 1984)

Chromista Pythiaceae

Trachysphaera fructigena Abor & Bunting

cigar end rot Expert opinion (T Gunua)

Fungi

Agaricales Marasmiaceae

Marasmiellus inoderma Singer Marasmius semiustus Berk. & Curtis

Marasmiellus rot Expert opinion (T Gunua)

Botryosphaeriales Botryosphaeriaceae Guignardia musae Racib. banana freckle Hyde & Philemon 1994, PNG

Pest List Database (NAQIA)

Lasiodiplodia theobromae (Pat.) Griffon & Maubl. (syn. Botryodiplodia theobromae Pat.)

finger rot Expert opinion (T Gunua)

Phyllostictina musarum freckle (ACNARS, 2003), Shaw 1984,

Kokoa 1991

Capnodiales Mycosphaerellaceae

Mycosphaerella musae (Speg.) speckle, leaf speckle

PNG Pest List Database (NAQIA)

Ceratobasidiales Ceratobasidiaceae

Ceratocystis paradoxa (Dade) crown rot Expert opinion (T Gunua)

Hypocreales Nectriaceae

Fusarium oxysporum f. sp. cubense Schltdl

Panama disease, Fusarium wilt

(Shivas & Philemon, 1996), Expert opinion (T Gunua)

Incertae sedis Incertae sedis

Cordana musae (Zimmermann) Cordana leaf spot PNG Pest List Database (NAQIA)

Deightoniella torulosa Ellis Deightoniella fruit speckle

Hyde & Philemon 1994, PNG Pest List Database (NAQIA)

Ramichloridium musae (de Hoog) tropical speckle (ACNARS, 2003; Kambuou, 2003)

Uredo musae Cummins leaf rust (ACNARS, 2003)

Mycosphaerellales Mycosphaerella (Genus)

Mycosphaerella fijiensis Morelet black Sigatoka PNG Pest List Database (NAQIA)

Mycosphaerella musicola R. Leach ex J.L. Mulder

yellow Sigatoka Expert opinion (T Gunua)


24

Table 2.2 continued - Pathogens, arthropods, nematodes and weeds reported associated

with banana in Papua New Guinea


Phyllachorales Phyllachoraceae

Colletotrichum musae (Berk. & Curtis) anthracnose Expert opinion (T Gunua)

Phyllachora musicola Booth & Shaw black-cross PNG Pest List Database (NAQIA)

Sordariomycetes incertae sedis

Magnaporthaceae

Magnaporthe grisea Barr Johnson spot Expert opinion (T Gunua)

Virus VI: RNA Reverse Transcribing Viruses, Caulimoviridae (Fam), Badnavirus (Genus)

banana streak virus (BSV)

(Davis et al., 2000)

Arthropods Aracnida Protstigmata

Tetranychidae Tetranychus spp. spider mites (Schuhbeck, 1996; ACNARS, 2003)

Tetranychus lambi Pritchard & Baker banana spider mite

(Waterhouse, 1997)

Coleoptera

Chrysomelidae Lema papuana Jac. (Szent-Ivany & Catley, 1960) (on Musa sapientum & M. textilis)

Curculionidae Apirocalus cornutus Pasc horned polyphagous weevil

(Szent-Ivany & Barrett, 1956)

Cosmopolites sordidus (Germar) banana weevil borer

(Froggatt, 1941; Szent-Ivany & Barrett, 1956; Greve & Ismay, 1983; Thistleton & Masamdu, 1985; Issacson & King, 1987)

Odoiporus longicollis Oliver banana stem borer

Expert opinion (D Tenakanai)

Oribius sp (Bourke et al., 1973; Thistleton & Masamdu, 1985; French, 1986)

Oribius cruciatus Marshall (French, 1986)

Oribius inimicus Marshall (Greve & Ismay, 1983)

Trochorhopalus strangulatus Gyllenhal (Ismay & Dori, 1985)

Geometridae Ectropris sabulosa Walker (Lamb & Johnston, 1976)

Scarabaeidae Dermolepida nigrum Nonfrid (Szent-Ivany & Barrett, 1956; Lamb & Johnston, 1976; French, 1986)

Lepidiota spp Expert opinion (D Tenakanai)

Oryctes centaurus Sternberg Rhinoceros beetle (Smee, 1965)

Oryctes rhinoceros(Linnaeus) Asiatic Rhinoceros beetle

(Smee, 1965; Lamb & Johnston, 1976)

Papuana spp taro beetle Expert opinion (J Bokosou)

Papuana woodlarkiana laevipennis Arrow taro beetle (Froggatt, 1941; Szent-Ivany & Barrett, 1956)

Papuana woodlarkiana Montrouzier taro beetle (Lamb & Johnston, 1976)

Rhyparida sobrina Bryant Rhyparid beetle (Waterhouse, 1997)

Scapanes australis australis (Boisduval) Melanesian rhinoceros beetle

(Szent-Ivany & Barrett, 1956; Lamb & Johnston, 1976)

Scapanes australis grossepunctatus Sternberg

coconut rhinoceros beetle

(Szent-Ivany & Barrett, 1956; Bourke et al., 1973; Lamb & Johnston, 1976)

Trichogomphus semilinki Ritz (Smee, 1965)

Xyloptrupes spp. (Smee, 1965)

Diptera


25




Muscidae Myospila argentata Walker (Greve & Ismay, 1983)

Tephritidae Bactrocera bryoniae (Tryon) Byron’s fly (Drew, 1989), PNG Pest List

Database (NAQIA)

Bactrocera dorsalis complex (CABI, 1998)

Bactrocera frauenfeldi (Schiner) mango fruit fly (Drew, 1989; Dori et al., 1993)

Bactrocera musae (Tryon) banana fruit fly (Szent-Ivany & Barrett, 1956)

Bactrocera papayae Drew & Hancock Asian papaya fruit fly

Expert opinion (S Balagawi, A Kawi, D Tenakanai)

Enoplopteron hieroglyphicum Meijere (Szent-Ivany & Barrett, 1956; Greve & Ismay, 1983)

Dermaptera

Chelisochidae Chelisoches morio (Fabricius) black earwig (Greve & Ismay, 1983; Ismay & Dori, 1985)

Hemiptera

Aleyrodidae Aleurodicus disperses Russel spiralling whitefly

Expert opinion (F Dori, R Kambuou)

Coreidae Amblypelta lutescens (Distant) banana-spotting bug

(CABI, 1998)

Miridae Prodromus spp. (Ismay & Dori, 1985)

Pentatomidae Acanthotyla Stål spp. (Greve & Ismay, 1983)

Tingidae Stephanitis typical (Distant) (Szent-Ivany & Catley, 1960) (on Musa sapientum)

Homoptera

Aphididae Pentolonia nigronervosa Coquerel banana aphid (Schuhbeck, 1996; CABI, 1998)

Rhopalosiphum maidis (Fitch) maize aphid (Waterhouse, 1997)

Coccidae Ferrisia virgata (Cockerell) (CABI, 1998)

Parasaissetia nigra (Nietner) nigra scale (CABI, 1998)

Saissetia coffea (Walker) hemispherical scale

(CABI, 1998)

Diaspididae Aonidiella aurantii (Maskell) California red scale

(CABI, 1998)

Aspidiotus destructor Sign (CABI, 1998)

Pseudaulcapsis pentagona (Targioni-Tozzetti)

(CABI, 1998)

Pseudococcidae Dysmococcus neobrevipes (Cockerell) grey pineapple mealybug

(CABI, 1998)

Lepidoptera

Amanthusiidae Taenaris dimona Hewitson Myops owl butterfly

(Greve & Ismay, 1983)

Arctidae Diacrisia papuana Rothschild (Greve & Ismay, 1983)

Geometridae Hyposidra talaca (Walker) coffee ring borer (Lamb & Johnston, 1976)

Hesperiidae Erionota thrax (Linnaeus) banana leaf roller (Issacson & King, 1987; Waterhouse & Norris, 1989; Sands et al., 1991; Sands et al., 1993)

Limocodidae Limacodidae gen.et.sp. indet slug moths, cup moths

(Ismay & Dori, 1985)

Scopelodes dinawa Bethune-Baker (Szent-Ivany, 1955; Szent-Ivany & Catley, 1960) (on Musa textilis)

Scopelodes nitens Bethune-Baker (Szent-Ivany & Catley, 1960) (on Musa sapientum)

Noctuidae Agrotis ipsilon (Huf) (CABI, 1998)

Helicoverpa armigera (Hübner) (Greve & Ismay, 1983)


26




Tirocola plagiata Walker (Catley, 1962; Smee, 1964)

Psychidae Psychidae species Boisduval bagworm Expert opinion (J Bokosou)

Pyralidae Nacoleia sp? (Walker) (Bourke et al., 1973)

Nacoleia octasema (Meyrick) banana scab moth

(O'Connor, 1949; Szent-Ivany & Barrett, 1956)

Tirathaba rufivena Walker (Smee, 1965)

Tineidae Opogona spp. (Greve & Ismay, 1983)

Zygaenidae Artona spp. (Ismay & Dori, 1985; Thistleton & Masamdu, 1985)

Homophylotis sp. nr albicilia Hampson (Greve & Ismay, 1983)

Orthoptera

Acrididae Locusta migratoria Linnaeus locusts, migratory locust

(Anonymous, 1969)

Tettigonidae Eumossula gracilis Willemse (Bourke et al., 1973)

Segestidea defoliaria defoliaria Uvarov (Greve & Ismay, 1983)

Segestidea montana Willemse (Greve & Ismay, 1983)

Segestidea novaguineae (Brancsik) (Greve & Ismay, 1983)

Sexava spp. (Smee, 1965)

Thysanoptera

Thripidae Chaetanaphothrips signipennis (Bangall) banana rust thrips

(CABI, 1998)

Thrips hawaiiensis (Morgan) (CABI, 1998)

Nematodes Aphelenchoides besseyi Christie (Bridge & Page, 1982)

Aphelenchoides spp. (Bridge & Page, 1982)

Aphelenchus avenae Bastian (Bridge & Page, 1982)

Criconematid n.g., n. sp. (Bridge & Page, 1982)

Gracilacus spp. (Bridge & Page, 1982)

Helicotylenchus dihystera Sher (Bridge & Page, 1982)

Helicotylenchus microcephalus Sher causes root/corm necrosis

(Bridge & Page, 1982)

Helicotylenchus mucronatus Siddiqi causes root/corm necrosis


Helicotylenchus multicinctus Golden banana spiral nematode


Hoplolaimus seinhorsti Luc (Bridge & Page, 1982)

Meloidogyne incognita Chitwood root-knot nematode


Meloidogyne javanica Chitwood root-knot

nematode (Bridge & Page, 1982)

Paratrichodorus minor Siddiqi (Bridge & Page, 1982)

Pratylenchus coffeae Goodey lesion nematode (Bridge & Page, 1982)

Radopholus similis Thorne burrowing nematode


Rotylenchulus reniformis Linford & Oliveira Reniform nematode


Scutellonema cf. minutum Sher (Bridge & Page, 1982)

Trichodorus cylindricus Hooper (Bridge & Page, 1982)

Tylenchus spp. sensu lato (Bridge & Page, 1982)

Xiphinema elongatum Schuurmans Stekhoven & Teunissen


Xiphinema ensiculiferum Thorne (Bridge & Page, 1982)

Xiphinema guirani apud Lamberti & Bleue-Sacheo (Bridge & Page, 1982)

Xiphinema insigne Loos (Bridge & Page, 1982)

Xiphinema orthotenum Cohn & Sher (Bridge & Page, 1982)


27




Weeds

Cyperales Rottboellia cochinchinensis W.D Clayton itchgrass Expert opinion (T Gunua)

Fabales Mimosa diplotricha C. Wright or Mimosa invisa Mart giant sensitive grass

Expert opinion (T Gunua)

Piperales Piper aduncum Linnaeus false kava, false Matico tree


Poales Imperata cylindrical Beau cogongrass, blady grass


Polygonales Persicaria perfoliata H. Gross mile-a-minute weed

Expert opinion (D Tenakanai)

Miscellaneous

Birds Cockatoos,

parrots, starlings Expert opinion (F Dori, E Guaf, L Kurika, G Ling, S Sar)

Flying foxes or Bats Expert opinion (F Dori, L

Kurika, G Ling, S Sar)

Achatina achatina (Linné) giant African

snail Expert opinion (L Kurika)

Rats long tailed rat Expert opinion (E Guaf)

2.3.2 Pest Summaries

Of the 112 species in Table 2.2, the following pest summaries cover fourteen of the

most commonly observed and managed species. Nine have been consistently reported

in formal and informal literature as being important species on PNG banana: Erwinia

chrysanthemi Burkholder et al (causes rhizome rot), Mycosphaerella fijiensis Morelet

(black Sigatoka), Ramichloridium musae (de Hoog) (tropical speckle), Cosmopolites

sordidus (Germar) (banana weevil borer), Bactrocera musae (Tryon) (banana fly),

Erionota thrax (Linnaeus) (banana leaf roller), Nacoleia octasema (Meyrick) (banana

scab moth), Pratylenchus coffeae Goodey (lesion nematode) and Radopholus similis

Thorne (burrowing nematode). An additional five taxa, in addition to being reported in

the literature, were also selected as being of importance by a majority of local experts

interviewed: Cordana musae (Zimmermann) (Cordana), Phyllachora musicola Booth

& Shaw (black-cross), Papuana spp. (taro beetles), Rhyparida sobrina (Bryant)

(Rhyparid beetle), and Scapanes australis grossepunctatus Sternberg (coconut

rhinoceros beetle). Please note that some figures may not have a measuring scale but

have instead been provided to show what the pest/pathogen looks like.

28

2.3.3 Pathogens - Bacteria

2.3.3.1 Erwinia chrysanthemi Burkholder et al.

A B Figure 2.2 (A) Fallen banana, cause may be due to rotting of basal pseudostem

(sometimes termed ‘tip-over’ by field officers in PNG) (Source: CTAHR

Hawaii); and (B) Rotting xylem vessels referred to as internal pseudostem

necrosis (Source: CTAHR Hawaii www.ctahr.hawaii.edu/nelsons/banana)

Taxonomic information: Order: Enterobacteriales; Family: Enterobacteriaceae;

Genus: Erwinia. (Note: information on phylum and class have been provided in Table

2.2 and therefore not provided here)

Common name(s): Erwinia rot. Symptoms of damage caused by E. chrysanthemi are

also referred to as rhizome rot, bacteria head rot, or tip-over (Figure 2.2A)

Part of banana plant affected: Roots and pseudostem

Distribution: Erwinia rot is a serious disease causing root and stem rot, it is mostly

recorded in lowland plantain crops (interviewed officer comments from T. Gunua).

The pathogen was isolated from banana samples in Laloki (Central Province)

(Tomlinson, 1984; Pone, 1994). Although present in the country the local distribution

of this pathogen is largely unknown (EPPO/CABI, 1997).

Symptoms: Erwinia chrysanthemi is a soft rot pathogen that degrades succulent and

fleshy plant organs such as roots, tubers, stem cuttings and thick leaves. It is also a

vascular wilt pathogen, colonizing the xylem vessels (Figure 2.2B) and becoming

systemic within the plant (EPPO/CABI, 1997). Rhizome rot describes the damage

caused by nematode infestation of the roots that cause the rhizomes to rot (Tomlinson,

29

1984). Symptoms also include wilting and death of leaves before fruit has ripened. The

centre of the pseudostem rots and there is some discolouration of the vascular tissues

of the outer leaf sheaths which can extend into the stalk of the fruit (Kohler et al.,

1997).

Literature from PNG on pest: Erwinia chrysanthemi was not previously recorded on

banana until an investigatory trial was done in 1983 (Tomlinson et al., 1988). Banana

test plants failed to mature due to failure of newly planted corms establishing and the

falling over of older plants. These symptoms were not previously recorded on banana.

The bacterium E. chrysanthemi was consistently isolated from diseased stem tissue of

suckers and artificial inoculation was shown to produce rotting in 12 weeks

(Tomlinson et al., 1988). There were ten banana cultivars tested and these represented

3 genomes (AA, AAA, and ABB). The AA genome cultivars were more susceptible

than the AAA and ABB genome cultivars. The disease is often not recognised due to

the many causes of poor growth of cultivated banana plants. The damage it causes such

as ‘tip-over’ is often attributed to the effects of strong windy conditions or beetle

damage on bananas (Philemon, 1986). High range in banana genetic diversity and

cultivation of more than one variety in subsistence and semi-commercial farming

systems may provide resistance between varieties lessening the damage caused

(Tomlinson et al., 1988).

Economic impact: Unknown.

2.3.4 Pathogens - Fungi

2.3.4.1 Cordana musae (Zimm.)

Figure 2.3 Cordana leaf spot on banana leaves (Source: CTAHR Hawaii web site:

www.ctahr.hawaii.edu/nelsons/banana)

30

Taxonomy information: Order: Incertae sedis; Family: Incertae sedis; Genus:

Cordana

Common name: Cordana leaf spot

Part of banana plant affected: Leaves

Distribution: Local distribution is not known. The leaf spot disease has been observed

in the lowlands (mainland or island provinces or both uncertain) attacking both

plantain and dessert varieties (interviewed officer comments from T. Gunua). Present

on the Gazelle Peninsula, East New Britain Province (ENB) (interviewed officer

comments from M. Lolo) and observed on Buka Island (Bougainville) (interviewed

officer comments from L. Kurika). Surveys are being carried out in PNG to determine

local distribution of pathogens (interviewed officer comments from R. Kambuou, E.

Guaf).

Symptoms: Large leaf spots, up to 100mm, pale brown or yellow, oval or diamond-

shaped, usually surrounded by a yellow halo (Figure 2.3). Note: Figure 2.3 does not

have a scale but is provided to show what the pathogen looks like on banana leaf. The

spots occur on and between the veins. Often entire edge of leaf may be infected with an

uneven, zigzag, yellow band separating diseased from green tissues. Infections often

occur on leaf spots caused by the black cross fungus (Phyllachora musicola), or leaf

blotches associated with Deightoniella torulosa (Kohler et al., 1997).

Literature from PNG on pest: Cordana is reported observed as being a minor

pathogen pest (ACNARS, 2003; Kambuou, 2003).


31

2.3.4.2 Mycosphaerella fijiensis Morelet

A B Figure 2.4 (A) Black Sigatoka on banana leaves (Source: DAFF Australia – AQIS);

and (B) Leaf infested with black Sigatoka has yellow transition zones between

infected and green uninfected leaf area (Source: CTAHR Hawaii

www.ctahr.hawaii.edu/nelsons/banana/)

Taxonomic information: Order: Mycosphaerellales; Genus: Mycosphaerella

Common name(s): Black Sigatoka, black leaf streak disease


Distribution: Detailed distribution in PNG is uncertain, informal observation has

noted its presence in various parts of the country but formal verification is yet to be

done. Observed in the central Province (interviewed officer comments from R.

Kambuou, T. Knox, P. Sale) and also observed in Madang (King et al., 1988) but

Schuhbeck (1996) does not mention it when reporting on banana pests in Island

provinces (Manus, New Ireland, New Britain and Bougainville) (Schuhbeck, 1996).

However, symptoms have been observed on the Gazelle Peninsula (interviewed officer

comments from L. Kurika, M. Lolo) and seen in Manus (Manus Province) and

Kavieng (New Ireland Province) (interviewed officer comments from M. Lolo). Not

much seen on atolls in the Island provinces (interviewed officer comments from M.

Lolo). It has also been observed in Morobe and Madang on Kalapua banana variety

(interviewed officer comments from S. Sar). Observations however need verification

through methodological sampling and expert identification.

32

Symptoms: The first symptoms of black Sigatoka are small, chlorotic flecks that

appear on the under surface of the third and fourth fully expanded leaves. The flecks

develop into narrow rusty brown streaks (up to 2 mm wide and 20 mm long) and often

have truncated ends and sides that are sharply limited by the leaf veins. During early

stages, streaks are only visible from the lower surface. The colour of streaks intensifies

to red, brown or black, sometimes with a purple tinge. The streaks enlarge, becoming

fusiform and elliptical, and darken to give the characteristic black streaking of the

leaves (Figure 2.4A). Note: Figure 2.4 does not have a scale but is provided to show

what the pathogen looks like on banana leaf. Adjacent tissues are often water-soaked,

especially under humid conditions. Central tissues of the lesions eventually collapse.

Lesions dry to a light grey with dark brown or black borders and often have narrow,

yellow transition zones between the borders and the green leaf tissue (Figure 2.4B).

Streaks on juvenile leaves are often oval and surrounded by a yellow margin. Fruit

losses occur due to a lack of functional leaf surface area (Stansbury et al., 2000).

Literature from PNG on pest: The worst fungal cases are when black Sigatoka is

present in combination with black cross and Cordana (interviewed officer comments

from R. Kambuou). Comments from local expertise suggest that wide varietal diversity

in PNG bananas may be playing a role in neutralising the spread and thus reducing the

intensity of the disease (interviewed officer comments from R. Kambuou). Of all

common fungal diseases M. fijiensis is however the most commonly observed

(interviewed officer comments from R. Kambuou) particularly on dessert cultivars

(interviewed officer comments from T. Gunua). At the Pacific Adventist University

(PAU) Farm outside Port Moresby, Sigatoka is the main problem on Cavendish banana

variety (interviewed farm managers’ comments from T. Knox & P. Sale).

Currently collaborative efforts with NARI have enabled the planting of black Sigatoka

resistant varieties developed at NARI (Kambuou, 2001; NARI, 2005, 2007b) at the

PAU farm (interviewed farm managers’ comments from T. Knox & P. Sale).


33

2.3.4.3 Phyllachora musicola Booth & Shaw

Figure 2.5 Black-cross on underside of banana leaf of local cultivar. Photo taken at

Chanel College, Kokopo, ENB (Source: A. Mararuai)

Taxonomy information: Order: Phyllachorales; Family: Phyllachoraceae; Genus:

Phyllachora

Common name: Black-cross


Distribution: Not known. Observed causing damage in Madang province (King et al.,

1988). Observed in banana plantation at Chanel College in Kokopo (ENB)

(interviewed officer comments from J. Bokosou, K Kurika) and observed on Buka

Island (interviewed officer comments from L. Kurika).

Symptoms: Black four-pointed stars, up to 60 mm long, most prominent on the lower

surface of older leaves, with long axis of the star parallel to the leaf veins (Figure 2.5).

Note: Figure 2.5 does not have a scale but is provided to show what the pathogen looks

like on banana leaf. The spots are scattered or sometimes occur in large groups. Spores

develop on the dark lines. Sometimes C. musae leaf spots are centred on the black-

cross lesions (Kohler et al., 1997).

Literature from PNG on pest: Reported observed as a minor pathogen pest

(ACNARS, 2003).


34

2.3.4.4 Ramichloridium musae de Hoog

Taxonomy information: Order: Incertae sedis; Family: Incertae sedis; Genus;

Ramichloridium

Common name: Tropical speckle

Synonyms: Periconiella musae, Veronaea musae


Distribution: Local distribution not known

Symptoms: The fungus penetrates leaf stomata and, since spread in leaf is restricted to

an air chamber and the palisade cells immediately surrounding it, only a small pin

point, brown or black lesion results. These speckles are more prominent on the upper

surface; they are very numerous and become aggregated into large (up to 4 cm

diameter) circular blotches which are chlorotic amongst the necrotic speckles.

Literature from PNG on pest: Pathogen has been reported as a minor pest

(ACNARS, 2003).

Economic impact: Unknown

2.3.5 Insects & Mites - Coleoptera

2.3.5.1 Cosmopolites sordidus (Germar)

A B Figure 2.6 (A) Lifecycle and damage caused by banana weevil borer (Source: Cook

Islands Biodiversity Database); and (B) Adult banana weevil borer (Source: G

McCormack. Cook Islands Biodiversity Database-

http://entnem.ufl.edu/creatures/fruit/borers/banana_root_borer.htm)

35

Taxonomic information: Order: Coleoptera; Family: Curculionidae

Common name(s): Banana root borer, banana weevil borer

Part of banana plant affected: Roots, corm

Distribution: Detailed local distribution in PNG is not known but it has been reported

to be present in the country (Szent-Ivany & Barrett, 1956; Waterhouse, 1997).

Symptoms: Damage done by extensive tunnelling of larvae in the corm weakening the

plant (Figure 2.6A) and causing plants to fall over light winds. Complete life cycle is

about 30-40 days (Woodruff, 1969; CSIRO, 2004). Eggs are white, about 1 mm in

diameter and are laid at the leaf base. Within 5-8 days larvae hatch out. After 3-6

weeks they pupate within the stems they bore into and after a period of one week

emerge as adults (French, 2006) (Figure 2.6B). Note: Figure 2.6B does not have a scale

but is provided to show what the insect looks like.

Literature from PNG on pest: The report by Waterhouse (1997) rated C. sordidus as

one of six major invertebrate pests of agriculture in the Southern and Western Pacific

but the relative importance of the beetle in PNG was very low. Cosmopolites sordidus

has been reported as an insect pest on banana in the Highlands provinces (Gunther et

al., 2003) when it co-occurs with Papuana spp. (taro beetle). Damage is often wrongly

attributed to wind damage or Papuana species (ACNARS, 2003). No quantitative work

has been carried out to determine the level of damage carried out by C. sordidus

(ACNARS, 2003).


2.3.5.2 Papuana species

A B C

36

Figure 2.7 (A) Taro beetle burrows in damaged corm of banana sword sucker (Source:

A Mararuai); (B) Adult Papuana woodlarkiana Montrouzier (Source: A

Carmichael, PaDIL); and (C) Larvae, pupae and adult taro beetle collected at

LAES Keravat, 2005 (Source: A. Mararuai)

Taxonomy information: Order: Coleoptera; Family: Scarabaeoidae

Common name: Taro beetle

Part of banana plant affected: Corm

Distribution: Taro beetle is found in PNG. There are nine Papuana species found in

PNG but local distribution is dependent on species. While some species may overlap in

distribution not all do (Masamdu & Simbiken, 2001).

Symptoms: Adult beetles burrow tunnels into the taro corm (Figure 2.7A).

Literature from PNG on pest: Adult taro beetle are about 25 mm long and 12 mm

wide (Figure 2.7B). Note: Figure 2.7B does not have a scale but is provided to show

what the insect looks like. Males have a horn on their head. Females sometimes have a

small horn. Newly emerged beetles are brown in colour but turn black as they get older

(Carmichael et al., 2007) (Figure 2.7C). Field based surveys and trials show that

physical corm damage of 15% and above renders taro corms unmarketable in most

areas in PNG (Masamdu & Simbiken, 2001).

Banana is a primary host of adult taro beetles (Masamdu & Simbiken, 2001). Studies

however into the damage caused by taro beetles on banana requires more study

(ACNARS, 2003). Extensive research on taro beetles has been done in PNG through

national (DAL, DPI, NAQIA, NARI) and international (ACIAR, FAO, PRAP, SPC)

collaboration. Research on control and management which spans over 20 years

covering: taxonomy (MacFarlane, 1987; Masamdu & Simbiken, 2001), biology (Perry,

1977; Onwueme, 1999), damage assessments (Arura & Akus, 1988), and biological

control (Aloalii et al., 1993; Theunis & Aloali'i, 1999; Schuhbeck & Bokosou, 2006;

Simbiken, 2006); to produce field guides (Carmichael et al., 2007).


37

2.3.5.3 Rhyparida sobrina Bryant

Figure 2.8 Sketch of Rhyparidella sobrina (Bryant) (Source: Gressit (1974))

Taxonomy information: Order: Coleoptera; Family: Chrysomelidae

Common name: Rhyparid beetle


Distribution: Detailed national distribution not known.

Symptoms: Adult beetles feed on young unrolled leaves and scar newly opened

fingers. Sketch diagram shows adult beetle (Figure 2.8) (Gressit, 1974). Note: Figure

2.8 does not have a scale but is provided to show what the insect looks like.

Literature from PNG on pest: Known to be present in the Markham valley (Morobe

Province) where sporadic outbreaks have occurred (Masamdu et al., 1988, 1989). In

the Markham valley it is a damaging but seasonal pest (interviewed officer comments

from J. Bokosou, E. Guaf). Pest management trials in the valley during the 1988

outbreak found practical non-chemical solutions of control through bagging bunches

using hessian and banana leaves. It also found that there was variation in varietal

susceptibility. Banana cultivars; Wamu and Garab II were severely attacked by beetles.

Kalapua I, Gampu and Amoa experienced medium to high levels of attack; Bansim,

Araduran and Mangas varieties experienced medium levels of attack; Grukrang I and

Yawa experienced slight to medium; Stifang, Rupis and Tsitsutsitsu slight; and

Yabimu suffered no damage (Masamdu et al., 1988, 1989).


38

2.3.5.4 Scapanes australis grossepunctatus Sternberg

A A B C Figure 2.9 (A) Pseudostem bore-hole caused by Scapanes australis grossepunctatus

(Source: A. Mararuai); (B) S grossepunctatus boring into banana pseudostem

(Source: A. Mararuai); and (C) Banana bunch emerging through a hole made

by S. grossepunctatus in banana pseudostem (Source: A Mararuai)

Taxonomy information: Order: Coleoptera; Family: Scarabaeoidae

Common name: Coconut rhinoceros beetle

Part of banana plant affected: Pseudostem

Distribution: Scapanes australis grossepunctatus is found on New Britain and New

Ireland islands (Bedford, 1980; Gende et al., 2006).

Symptoms: Scapanes grossepunctatus bores through the pseudostem of banana

varieties (Figure 2.9A) and beetles can often be found boring in the pseudostem

(Figure 2.9B) Note: Figure 2.9B does not have a scale but is provided to show what the

insect looks like. This causes the growing meristem to grow out through the puncture

(Figure 2.9C). The boring position may occur from any where between ground level

and the base of the leaf stems at the top of the banana plant (interviewed officer

comments from J. Bokosou, F. Dori, K. Kurika, L. Kurika).

Literature from PNG on pest: On New Britain Island, particularly on the Gazelle

Peninsula, S. grossepunctatus is a major pest of coconut (Moxon, 1988) and also

attacks banana varieties (interviewed officer comments from G. Ling). The planting of

banana gardens near existing or within coconut plantations or near breeding sites

(glyricidia and coconut groves) may be drawing Scapanes into the gardens ((Gende et

al., 2006) and interviewed officer comments from K Kurika). Considerable research

39

has been done on the biology (Bedford, 1976; Beaudoin-Olliviera et al., 2000) and

ecology (Beaudoin-Ollivier et al., 2001) of Scapanes and its control on coconut but not

on banana (Bedford, 1986; Kakul et al., 2000; Rochat et al., 2002; Rowland et al.,

2005).


2.3.6 Insects & Mites - Diptera

2.3.6.1 Bactrocera musae (Tryon)

A B C Figure 2.10 (A) Adult Bactrocera musae (Source SPC PaciFly); (B) Fruit fly larvae

feeding tracks in ripe Cavendish banana variety (Bundun, Morobe Province)

(Source: A. Mararuai); and (C) Fruit fly larvae feeding tracks in mature green

Cavendish (Kaiapit, Morobe Province) (Source: A. Mararuai)

Taxonomic information: Order: Diptera, Family: Tephritidae

Common name(s): Banana fruit fly, banana fly

Synonyms: Strumeta musae Tryon, Dacus musae (Tryon)

Part of banana plant affected: bunch fingers, fruit pulp

Distribution: Widespread and very common on mainland Papua New Guinea, where it

is as common in the Highlands as at low elevations (Leblanc et al., 2001). In early

1999, it was trapped and bred from bananas on the Gazelle (Mararuai et al., 2001). It

may have been introduced with infested bananas brought from mainland PNG as food

relief after the devastating 1994 volcanic eruption but this has not been confirmed.

Breeding populations also occur on Lihir Island (New Ireland Province). A few

specimens have been occasionally trapped on Manus, but it is not confirmed whether

40

breeding populations occur there (Drew & Romig, 1996; Leblanc et al., 2001).

Bactrocera musae is an exotic species to the Gazelle and spatial distribution is

expanding further inland and along the coastline from initial detection sites in Kokopo

(Mararuai et al., 2001).

Symptoms: Adult (Figure 2.10A) female fruit flies lay their eggs in the fruit and the

maggots develop as the fruit matures, destroying the flesh. Note: Figure 2.10A does

not have a scale but is provided to show what the insect looks like. They oviposit into

ripe banana (Figure 2.10B) and can oviposit in mature green bananas (Figure 2.10C).

Oviposition sites can provide entry for rot producing organisms. The maggots destroy

the flesh, and secondary rots, which enter through the oviposition puncture, cause pulp

breakdown. The damage is usually concentrated on bunches suffering from physical

damage or where mixed ripening of bunches is occurring because of poor plantation

management (Pinese & Piper, 1994). Oviposition stings caused by egg laying female

flies are often invisible to the untrained eye. Feeding of larval stages occurs in the fruit

pulp beneath the peel and damage is only seen when the peel is removed.

Literature from PNG on pest: Very little research has been done on the biology and

ecology of banana fly in PNG. Research on damage levels of banana fly on banana

varieties was done in Northern province including work on biology and control options

against infestation in the same area (Smith, 1977b). Smith (1977b) observed different

levels of infestation between three banana varieties: Giant Cavendish, Dwarf

Cavendish and Tui. Peel toughness and plant height were considered as the factors

influencing the variation. On the Gazelle, fruit fly larvae damage has been noticed by

banana farmers particularly in the Vudal and Vunapalding area (interviewed officer

comments from J. Bokosou, K. Kurika). Infestation in fruit on banana varieties such as

Tukuru at Vudal is higher than that observed in other areas on the Gazelle (interviewed

officer comments from J. Bokosou).

Economical impact: Unknown.

41

2.3.7 Insects & Mites - Lepidoptera

2.3.7.1 Erionata thrax (L.)

A B

C D Figure 2.11 (A) Adult Erionota thrax butterfly (Source: K Walker, PaDIL); (B)

Caterpillar feeding on leaf (Gazelle Peninsula, ENB) (Source: A Mararuai); (C)

Leaves of banana rolled up by banana skipper (Bubia, Morobe province)

(Source: A Mararuai); and (D) Pupae in leaf roll (Gazelle, ENB) (Source: A

Mararuai)

Taxonomic information: Order: Lepidoptera; Family: Hesperiidae

Common name(s): Banana leaf roller, banana skipper


Distribution: Erionata thrax is a hesperiid butterfly native to SE Asia (Waterhouse &

Norris, 1989) (Figure 2.11A). Note: Figure 2.11A does not have a scale but is provided

to show what the insect looks like. It is an exotic to PNG. The butterfly was first

observed in Vanimo (Sandaun Province) on the PNG mainland in 1983 (Dori, 1988)

and spread rapidly, recently observed in ENB (Schuhbeck, 1996; Waterhouse, 1997). It

has been observed in the Sepik since 1986; Madang, Eastern Highlands and Morobe

since 1987 and Port Moresby since September 1988 (Arura et al., 1988, 1989;

Waterhouse & Norris, 1989; Sands et al., 1991). A detailed description of the

establishment and spread of E. thrax in PNG is given by Waterhouse & Norris (1989).

42

It has spread eastward to invade New Britain, Duke of York and New Ireland islands,

and possibly Bougainville (Dori, 1988; PaDIL, 2008).

Symptoms: Caterpillars roll the banana leaves (Figure 2.11B) as they feed reducing

leaf surface area (Figure 2.11C) and eventually pupate in them (Figure 2.11D).

Literature from PNG on pest: The life cycle length of E. thrax from egg to adult is

about 5-6 weeks long (French, 2006). Banana skipper is reported as a minor pest on

banana. It has been observed to be a seasonal pest in the Markham valley (Morobe

province) (interviewed officer comments from E. Guaf), in Central (interviewed officer

comments from R. Kambuou) and also on the Gazelle Peninsula (interviewed officer

comments from J. Bokosou, K. Kurika).

Research on the management of E. thrax in PNG has found that of eight studied

banana varieties; Dwarf Cavendish, Tall Cavendish, Babi Yadefana, Kuriva, Small

Kalapua, Wudupataten, and Brown River, the dwarf and tall Cavendish varieties were

the least of the eight varieties infested (Dori, 1988). Immature stages of E. thrax were

found on cultivated and wild banana species but none were found on closely related

species (e.g. E. glaucum or palms (coconuts, betel nut, oil palm or other palms) (Arura

et al., 1988). In the Markham valley (Mutzing) banana skipper damage observed on

Yawa and Tukuru banana varieties was very bad (interviewed officer comments from

F. Dori).

Management of E thrax through biological control agents has been successful (Arura et

al., 1988; Dori, 1988; Sands et al., 1988; Lubulwa & McMeniman, 1998; Bauer et al.,

2003). There were three eggs parasites (Ooencyrtus erionotae, Ooencryrtus sp. and

Anastatus sp.) and two pupal parasites (a Tachinid and a Chalcidid) studied (Arura et

al., 1988, Dori, 1988). The release of egg parasite O. erionotae (Dori, 1988) and the

larval parasite Cotesia erionotae achieved reasonable control (Sands et al., 1993;

ACNARS, 2003). Cotesia erionotae was released in the Island provinces, Highlands,

Central and Oro with F Dori from 1990-1993 (interviewed officer comments from K.

Kurika). In the Highlands parasitoids were released in Kainantu (Eastern Highlands

Province) and Mt Hagen (Western Highlands Province) (interviewed officer comments

from F. Dori).

43

Assessment of the impact of projects, particularly by ACIAR, carried out for the

control of E. thrax indicate that proper management can lead to better production

levels and subsequently the income generated from the sale of more produce (Lubulwa

& McMeniman, 1998; Waterhouse et al., 1998; Bauer et al., 2003).


2.3.7.2 Nacoleia octasema (Meyrick)

A B Figure 2.12 (A) Adult Nacoleia octasema (NAIC Kilakila, Port Moresby) (Source: A

Mararuai); and (B) N. octasema damage on banana fingers (Source: A

Mararuai)

Taxonomic information: Order: Lepidoptera, Family: Pyralidae

Common name: Banana scab moth

Part of banana plant affected: Bunch fingers, fruit peel

Distribution: The moth is found throughout PNG (O'Connor, 1949; Schuhbeck, 1996)

(Figure 2.12A). Note: Figure 2.12A does not have a scale but is provided to show what

the insect looks like. Banana scab moth (BSM) was not observed in Manus on the

islands of Lou, Ahus and Andra during surveys in early 2007 (interviewed officer

comments from K. Kurika, M. Lolo). On Buka Island some BSM damage was seen at

Nova but none at Selau and Chaba villages (Buka Island, Bougainville) (interviewed

officer comments from K. Kurika, L. Kurika). Not much BSM damage was seen in

Kavieng (interviewed officer comments from M. Lolo).

Symptoms: On the islands of New Britain, New Ireland and Bougainville the moth

causes fruit damage by scarring the peel (Wilkie et al., 1993; Schuhbeck, 1996).

Damage inhibits full maturity of the fingers (Figure 2.12B)

44

Literature from PNG on pest: Only moths on the island provinces of New Britain

and New Ireland cause cosmetic damage to banana fingers (Schuhbeck, 1996). The

moths on the island provinces have morphological features identical to populations on

the mainland but these do not cause damage on banana fingers in the same way,

particularly those on the Gazelle Peninsula (Schuhbeck, 1996; ACNARS, 2003). On

the Gazelle Peninsula, BSM damage is extensive and widespread throughout the

peninsula and common on Cavendish banana variety. Abandoned banana gardens are

breeding grounds for BSM (interviewed officer comments from J. Bokosou, F. Dori,

K. Kurika, L. Kurika, G. Ling, M. Lolo). On the Gazelle scab moth damage is seen on

diploid varieties of banana (although some are noted to be less infested) and Cavendish

but few on triploid varieties (interviewed officer comments from G. Ling). At the PAU

Farm outside Port Moresby, some BSM damage is observed but not as severe as that

seen on the Gazelle and is managed with chemical sprays (interviewed farm managers’

comments from T. Knox & P. Sale). Studies on chemical control have shown to control

damage levels and the application method has been innovatively re-designed to allow

local farmer usage (NARI, 2007b). An imitation of the proper application apparatus, a

bell-injector commonly used in Queensland banana farms was built using old umbrella

parts, rubber tubing, a small sprayer and a wooden pole (NARI, 2007b).

The scarring stops growth and maturity in the fingers resulting in a loss of crop (Wilkie

et al., 1993; Schuhbeck, 1996). The brown scarring and consequential cracks reduce

surface quality and market value. Formal economic evaluation has not been done but is

observed to have a major impact.


2.3.8 Nematodes

2.3.8.1 Pratylenchus coffeae (Zimmermann)

A B

45

Figure 2.13 (A) Female nematode (Source: http://nematode.unl.edu): and (B)

Symptoms of Pratylenchus coffeae feeding on banana root (Source: CAB Crop

Protection Compendium Module 1)

Taxonomic information: Order: Tylenchida; Family: Pratylenchidae: Genus:

Pratylenchus

Common name(s): Banana root nematode, lesion nematode

Synonyms: Pratylenchus musicola, Tylenchus coffeae Zimmermann, 1898, Tylenchus

mahogani Cobb, 1920, Anguillulina mahogani (Cobb, 1920) Goodey, 1932,

Pratylenchus mahogani (Cobb, 1920) Filipjev, 1936, Tylenchus musicola Cobb, 1919

Part of banana plant affected: Roots

Distribution: A survey by Bridge et al (1982) indicated that P. coffea was present in

surveyed locations in the PNG provinces of Southern Highlands Western Highlands,

East Sepik, Morobe and East New Britain (Bridge & Page, 1982); but current

distribution is not known.

Symptoms: The lesion nematode causes severe damage to roots

Literature from PNG on pest: Results from the survey show that the most important

of nematodes is the lesion nematode, Pratylenchus coffeae (Zimmermann) (Bridge &

Page, 1982) (Figure 2.13A). Note: Figure 2.13A does not have a scale but is provided

to show what the nematode looks like. It was found causing severe root damage

(Figure 2.13B) at most sample sites in the five surveyed provinces. Current

observations in the field indicate that nematode damage has an impact on plants

particularly when there is a build up of nematode population particularly in long-term

banana gardens or if an infested stand of bananas remains for a while ((Fooks, 1989,

2002) comments from R Kambuou, and farm managers T. Knox & P. Sale).

Economic impact: Unknown

46

2.3.8.2 Radopholus similis Thorne

A B C Figure 2.14 (A) Illustration of burrowing nematode (Source:

http://plpnemweb.ucdavis.edu/Nemaplex); (B) Damage to banana roots caused by the

burrowing nematode (Source: http://www.ctahr.hawaii.edu); and (C) Toppled banana

(black head) (Source: http://www.ctahr.hawaii.edu/nelsons/banana)

Taxonomy: Order: Tylenchida, Family: Pratylenchidae, Genus: Radopholus

Common name(s): Burrowing nematode, root rot nematode (Figure 2.14A). Note:

Figure 2.14A does not have a scale but is provided to show what the nematode looks

like.

Part of banana plant affected: Roots, corm

Distribution: Survey by Bridge et al (1982) indicate that Radopholus similis Thorne

was present in the five provinces they surveyed (Southern Highlands, Western

Highlands, East Sepik, Morobe and East New Britain) (Bridge & Page, 1982;

Philemon, 1986). Current distribution however is not known.

Symptoms: Radopholus similis causes Radopholus root rot. Symptoms: reddish-brown

or black rots (Figure 2.14B), often several cm long, on the root, sometimes with cracks.

The areas of rot are at first outside the vascular tissues; later, they spread throughout

the root, causing total decay. As the nematode burrows into the corm, black spots with

red margins develop. These rots, known as ‘blackheads’, may extend up to 20 mm into

the corms. Plants are weakened by the root attack and are readily blown over during

storms (Kohler et al., 1997) (Figure 2.14C).

47

Literature from PNG on pest: The damage caused by R. similis in PNG was reported

to be not as damaging as P. coffea (Bridge & Page, 1982). It is not as widespread or

serious a pest in survey locations as P. coffeae (Bridge & Page, 1982; Philemon, 1986).


2.4 Discussion

Formal publications on banana pests in PNG are few. Possibly the first formal

publication was on the basic biology, distribution and management of banana scab

moth (O'Connor, 1949). Szent-Ivany & Barrett (1956) shortly after produced the first

list on banana pests recording 14 insect pests from banana, subsequently adding to that

four years later (Szent-Ivany & Catley, 1960). These 14 are not the 14 ‘taxa’ identified

in this thesis. Subsequent pest lists have been provided by Pone (1994), Schuhbeck

(1996), Waterhouse (1997), ACNARS (2003) and Kambuou (2003). The quality of

these lists vary, some being based on local surveys (e.g. Schuhbeck, Kambuou), while

others have been external reviews (e.g. Waterhouse 1997). None are comprehensive;

each dealing with different taxa groups (e.g. insects or pathogens) while others are

spatially restricted to a certain part of the country. The list of 112 organisms provided

in this chapter (Table 2.2) is thus the first and most comprehensive list to date of all

organisms associated with banana in PNG.

While searching through publications I have noted that publications may list species as

being minor or major pests on banana but most lack the assessment methodologies

which were used to classify those organisms as pests. The nematodes are a group

example. The commonly cited Bridge & Page (1982) survey report lists 14 nematode

species as being important on PNG banana but when Pone (1994) refers to that report

he lists 24 species. Another more improved and recent example is the ACNARS (2003)

report that mentions four nematode genera of importance present in the country but

specifies that damage assessment studies are needed to determine if they cause

significant problems to banana. The reason why the species are included as pests or

non-pests in PNG is also not stated. The economic impacts of many of the organisms

listed in Table 2.2 are not documented and I conclude that formal verification of pest

status is required for most species. Crop impact studies for even major crop pests in

48

PNG is generally lacking, but can be achieved (Wesis et al., in press). Thus,

economical impact is largely unknown for all groups of pathogens and pests discussed.

There is also the issue on pest status of a recently introduced or non-endemic pest of

banana. When non-endemic banana pests are confirmed as occurring in PNG, their pest

status based on known importance in other countries cannot be used as a measure of

their current impact in PNG. Two severe pathogen diseases on banana, Fusarium

oxysporum f. sp. cubense Schltdl (Fusarium wilt) and banana streak virus (BSV),

illustrate this point. Fusarium oxysporum f. sp. cubense was detected in PNG in the

mid-1990s at three locations along the PNG/Indonesian border (Shivas & Philemon,

1996; Davis, 2004; Kokoa, 2006) and surveys are currently being done to find out its

local distribution. However, despite now being on the national pest list, its limited

distribution means it is not a current production problem for most local growers. BSV

has been detected in Alotau (in 1997, Milne Bay Province), while streak symptoms

were found on many banana cultivars (AAB, Mysore subgroup) on the coast of

Western Province in June 1999. In May 2000, BSV-Mys was confirmed from a

Mysore cultivar at Green River (Sandaun Province), BSV-Onne from a Mysore

suspected cultivar at Telefomin (Sandaun Province) and BSV-GF from Pisang Raja

(AAB) at Niokamban (Western Province) (Davis et al., 2000). Davis et al (2000)

suggest that BSV may be widespread in PNG, but observations of field officers suggest

it is not causing a concern in production systems for growers. For the PRA process,

however, all potential pests need to be identified.

Kambuou (2003) reported that the main pests of banana in PNG were: B. musae, E.

thrax, N. octasema, and the banana leaf spot complex [C. musae, M. fijiensis, P.

musicola and R. musae] (Kambuou, 2003). This list, prior to that produced in this

chapter, was the most current for PNG banana pests. The author of that paper, Rosa

Kambuou, is an internationally respected banana specialist and one of PNG’s most

senior agricultural researchers. Her list might thus be considered as having some

authority. If so, then it is these species which are most likely to impact on commodity

production and of greatest importance in managing if PNG bananas are to be exported.

Of the seven, the biology, ecology and control of E. thrax and N. octasema have been

documented. Sporadic outbreaks of E. thrax caterpillars may occur due to seasonal

weather conditions reducing foliage cover, but this occurs only occasionally and the

species is regarded and known as a seasonal pest (interviewed officer comments from

49

J. Bokosou, E. Guaf, R. Kambuou, K. Kurika, D. Tenakanai). Nacoleia octasema is

found throughout the country, but only the moths found on the Gazelle Peninsula

(ENB) cause economic levels of cosmetic damage to banana fingers. Control options

have been studied and applied practically, and the application method adapted for local

use (NARI, 2007b). With the pathogens, M. fijiensis in combination with other

pathogens can be quite damaging (interviewed officer comments from R. Kambuou),

but research is currently multiplying resistant banana varieties for cultivation and this

approach is showing success (NARI, 2005, 2007a). Surveys are also being done to

determine the local distribution of the pathogens.

For only a few species in my list of 14 is there sufficient information available to meet

all the requirements of a PNG banana PRA. It is not possible within the course of one

PhD to gather all this information, so a focus upon just one pest, as a case study, was

considered an appropriate way forward. Bactrocera musae, the banana fly, was

consistently regarded in the literature and by interview participants as the major insect

pest of bananas in PNG, yet there is very little available information on this pest. For

this reason banana fly was chosen as the focus for the remainder of the thesis. It would

also be the major pest of concern for a PNG banana PRA because B. musae affects the

fruit of banana, the commodity to be traded. Banana fly is considered a common fruit

fly species on the mainland of PNG (Tenakanai, 1996; Clarke et al., 2004). However

there is little knowledge and research done on the biology and ecology of this fly in

PNG. There is no documentation on local levels of abundance which will be important

because there are different cropping systems in PNG (Bourke et al., 1998; Bourke,

2001). In the 1970s, Stuart Smith published three papers on banana fly in Northern

(now Oro) Province detailing results of a trapping programme which show seasonal

changes in abundance in that area (Smith, 1977a). He also carried out research on the

fly’s biology and methods on how to control infestation on its host (Smith, 1977b).

While these provide a stepping stone from which to continue research, they are

insufficient for developing a national management perspective appropriate for

international commodity trade for the pest.

2.5 Thesis Progress

The aim of this thesis is to provide information for the development of a pest risk

analysis (PRA) for PNG bananas. There are three steps in the PRA (Figure 2.16) and

50

this chapter has carried out an essential part of the first step in identifying pests

associated with the commodity. I have identified 112 organisms associated with

banana in PNG and in doing so I have also identified a smaller group of 14 organisms

that are commonly identified as needing management. Of these 14, Bactrocera musae

is recorded and regarded as the major pest of banana in PNG but there is limited

knowledge available on the species to further progress through the PRA process. In

subsequent chapters I focus on this fly so as to provide information required by the

PRA. Specifically, in the next chapter, I provide detailed analysis of the local

distribution of banana fly in PNG. Outcomes of that research are pertinent for both the

“Risk Assessment” and “Risk Management” steps of the PRA.







3

2

1

Review of banana (Musa spp.)

pests in Papua New Guinea [Chapter 2]







3

2

1









3

2

1







3

2

1



Figure 2.15 Pest Risk Analysis process; with arrow indicating which step in process

information generated in this thesis has been collected for

51

Chapter 3. Distribution and abundance of five economically important fruit fly species in Papua New Guinea

3.1 Introduction

Accurate information on the distribution and seasonal abundance of fruit flies, and

knowing and understanding the factors which influence distribution and abundance, is

a key element in the strategies employed in fruit fly management and market access

(Allwood, 1996a; Leweniqila et al., 1996; Sutherst et al., 2000; Yonow et al., 2004;

Dhillon et al., 2005; Khan et al., 2005). Growers producing commodities in areas free

of fruit flies, or with very low fruit fly abundance, receive favourable treatment with

respect to market access (Maelzer et al., 2004; Follett & Neven, 2006). Even in areas

where flies are endemic and normally abundant, seasonal periods of low fruit fly

numbers can be used as part of a systems approach management strategy for market

access (IPPC, 2002c). For example, both citrus and strawberries are exported from

Queensland during winter with access to interstate markets based, in part, on a winter

window of low pest pressure (H. Gu, Queensland Primary Industries & Fisheries, pers.

comm.).

Fruit fly distribution is influenced by abiotic and biotic environmental factors such as

temperature, rainfall and the availability of hosts (Christenson & Foote, 1960;

Bateman, 1972; Fletcher, 1987). A suite of biological and environmental factors also

influence fruit fly abundance, including daily nutritional requirements (Aluja et al.,

2001; Carey et al., 2002), light intensity and day length (Brieze-Stegeman et al., 1978;

Brevault & Quilici, 2000), natural enemies (Duan & Messing, 1997; Bautista et al.,

2004), and fly movement (Kovaleski et al., 1999; Bonizzoni et al., 2004). The relative

importance of these factors may, however, vary in different regions of the world, for

example between tropical and temperate regions (Muthuthantri, 2008).

In the Pacific, research indicates that the major factor influencing fruit fly distribution

and abundance is the spatial and seasonal availability of susceptible hosts (Leweniqila

et al., 1996; Vueti et al., 1996). Most Pacific Island Countries and Territories (PICTs)

are, however, small to medium sized islands, islets and atolls which have little

variation in climatic attributes (e.g. temperature, rainfall) because altitude variation is

52

minimal and climate is largely dominated by maritime influence. In contrast, with

regions which vary significantly in climate Papua New Guinea (PNG) in the Western

Pacific has a much larger land mass than neighbouring PICTs with a significantly

greater altitudinal and tropical climate range. How these factors influence fruit fly

distribution in this particular environmental setting is largely unknown.

The geography of PNG is highly diverse and influences the tropical weather patterns

experienced in the country. Annual rainfall levels in PNG range from 1000 to >5000

mm, with variation due primarily to topographical variation (McGregor, 1989;

Bellamy & McAlpine, 1995; Macfarlane, 2000). Temperature ranges in the country are

largely affected by altitude. In general, lowland coastal areas have warm temperatures

that range from 23->35 °C, in comparison to cooler temperatures of 0-28 °C

experienced at altitudes above 1200 m.a.s.l in the Highland provinces (Macfarlane,

2000). The combined influence of geography, the southeast trade winds and the

northwest monsoon, produces seasonal patterns which are variable in their timing and

intensity in different parts of the country. For example, the wet season occurs at two

different times based on locality. Most of the country experiences maximum monthly

rainfall from January to April, but mainland areas in Milne Bay, much of Gulf

Province, the coastal region and Finschhafen area of Morobe Province, the southern

coast of New Britain, and the southern most tip of the main island of Bougainville

experience their major rainfall from May to August (Macfarlane, 2000).

Geographic diversity also contributes toward the diversity in local cropping systems

influencing the cultivation and availability of susceptible hosts. The influence of this

type of tropical cropping system on population dynamics is also largely unknown.

There are 287 discrete agricultural systems identified in PNG, each practicing a

particular cultivation system and growing a certain range of crops (Bourke et al.,

1998). A PNG specific geographical dataset known as the Papua New Guinea

Resource Information System (PNGRIS) (Bellamy & McAlpine, 1995) provides GIS

surface layer maps of these cropping systems, as well as other site specific information

such as elevation and annual rainfall which, if combined with fruit fly abundance data,

allows questions to be asked about the impact of these variables on fly distribution.

PNG’s geography has an influence the regional biodiversity of the country’s fruit fly

fauna (Michaux & White, 1999; Clarke et al., 2004; Kitching et al., 2004), but whether

climatic factors and/or cultivation practices influence the local distribution and

53

abundance of fruit fly species is largely unknown. Presence/absence distribution

records at the provincial (i.e. local government) level for all PNG Dacinae have been

published (Clarke et al., 2004), but nothing is known of the fine scale spatial

distribution and temporal abundance of fruit flies within each PNG province.

The general lack or absence of formal scientific documentation on pest fruit fly species

and their susceptible hosts in PNG is a factor which will contribute to reducing the

likelihood of market access acquirement for susceptible commodities (Allwood,

1996a). Many of the potential fresh fruit and vegetables commodities which could be

exported from PNG, including banana, are hosts of the fruit flies dealt with in this

chapter. In the management of economically important species for which detailed

ecological information is lacking readily available weather or geographic data on

factors such as rainfall and temperature, help contribute to providing an initial and

general perspective of pest distribution and abundance (Carey, 1996; Yonow et al.,

2004). Given the diverse geographical environment, the different agricultural systems,

and the large fruit fly fauna, PNG is also an ideal area to investigate the influence and

impact that tropical environmental factors may have on the distribution and abundance

of pest fruit fly species. The objectives of this study are thus twofold. Firstly, as an aid

to local pest management and market access, to detail the fine-scale distribution and

abundance of Bactrocera musae (Tryon) (banana fly) as well as four other pest fruit fly

species in major cropping regions of PNG. Secondly, so as to further our general

knowledge of fruit flies, to determine factors influencing the distributions of those

flies. In the context of the overall thesis, this chapter includes information on the main

target species: banana fly. The inclusion of the other fly species, while not directly

related to banana market access, provides an understanding on how these

environmental factors influence the population dynamics of other economically

important fruit fly species. Information of which is limited in tropical fruit fly ecology

and management.

3.2 Materials and methods

3.2.1 Trapping

The fruit flies used in this study were collected as part of fruit fly trapping surveys

carried out in PNG between June 1998 and September 2001. While not enrolled as a

student at the time, I was personally involved in that trapping program as a scientist,

54

with responsibility for the component of the trapping network covering the PNG island

provinces. In total, 167 pairs of cue-lure (4(para-acetophenyl)-2-butanone) and methyl

eugenol (4-allyl-1,2-dimethoxybenzene) baited modified Steiner traps were used.

Traps were hung, wherever possible, in trees at approximately 1.8m above the ground

and were cleared of flies every 2-3 weeks. Samples were subsequently forwarded to

Griffith University, Brisbane, where they were identified to species level using the

taxonomic keys in Drew (1989). Further details of the traps and trapping program are

presented in Leblanc et al. (2001) and Clarke et al. (2004), which are supplied as

Appendices 1 and 2. I am a co-author of both of these publications.

For this chapter, detailed analysis is undertaken for five economically important fruit

fly species: Bactrocera bryoniae (Tryon), B. cucurbitae (Coquillett), B. frauenfeldi

(Schiner), B. musae and B. umbrosa (Fabricius). Only a subset of the total trapping

data-base is used for this chapter. Trap sites providing data were chosen based on the

duration that traps were serviced. Only traps serviced for a minimum time of eight to

nine months were included to determine population fluctuations over a period of time.

These traps occurred in districts which were consistently serviced by more than one

trap so as to allow comparative analysis within an area. This reduced the study to 69

trap sites in four selected areas of PNG (Table 3.1 & Figure 3.1): (i) seventeen traps in

the Highlands Provinces (six in Eastern Highlands [EHP], three in Chimbu, four in

Western Highlands [WHP], two in Enga and two in Southern Highlands [SHP]); (ii)

sixteen traps in Morobe Province; (iii) twenty-one in Central Province; and (iv) fifteen

traps on the Gazelle Peninsula in East New Britain (ENB). Even with reduced use of

the total available data set, the tallied recordings of 891,970 trapped fruit fly specimens

are analysed here. The trap site locations cover a broad range of agricultural systems

and environment types (Bellamy & McAlpine, 1995; Bourke et al., 1998; NARI,

2008). Excluded data provided little more additional information than already provided

in Clarke et al. (2004).

55

Table 3.1 Location and number of fruit fly trap sites in four study areas in Papua New

Guinea in relation to altitude (m.a.s.l) and annual rainfall (mm) levels used in

the Papua New Guinea Resource Information System (PNGRIS)

Altitude (m)

0-600 600-1200 1200-1800 >1800

Central 20 1 Morobe 12 3 1 Highlands 13 4 Gazelle 11 3 1 Rainfall (mm)

1000-1500

1500-2000

2000-2500

2500-3000

3000-3500

3500-4000

4000-5000

Central 13 3 3 2 Morobe 1 7 3 5 Highlands 3 6 7 1 Gazelle 1 6 8

Figure 3.1 Fruit fly trapping sites used to study the influence of site variables on the

distribution and abundance of five economically important fruit fly species in

Papua New Guinea

56

3.2.2 Databases and analysis

The geographical dataset PNGRIS (Bellamy & McAlpine, 1995) was used to supply

GIS surface layers for rainfall, altitude and land use to create respective maps in

ArcGIS 9.0. Categorisation of altitude ranges and annual rainfall used in PNGRIS were

used to map and analyse the trapped fly abundance for the five studied fruit fly species

collected from traps at different levels.

Note. Altitude ranges in map legend are presented as categorised in the PNGRIS

dataset. Majority of trap sites were located from 0-1800m and therefore ranges above

1800m were grouped and similarly shaded for easier presentation. The annual rainfall

is similarly done but this time distinct shading has been given for ranges 1000-

2500mm. Rainfall ranges above 2500mm are shaded in various shades of blue.

The landuse surface layers had information on cropping systems such as the type of

agricultural crops cultivated in an area, how often they were planted, and how

commonly they were consumed, etc. Banana is one of four major food crops cultivated

in PNG and therefore there was substantial information on the crop to be able to query

PNGRIS to providing information on banana grown as a dominant (crop consumed on

a weekly basis) or subdominant (crop consumed at a lesser rate than weekly) crop. It

was therefore feasible to create a map of the spatial distribution of banana in ArcGIS

and this was labelled and referred to as a map indicating the importance of banana (the

cultivated and staple food crop) in an area. This map was used to determine the

relationship between fly abundance and host distribution. I was not able to get detailed

data on the importance and distribution of susceptible hosts for the other fly species

studied in PNGRIS. Consequently it was not possible to investigate the effect of host

distribution on the distribution of those species. For example, chillie is a host for B.

bryoniae but a spice crop not cultivated extensively and not as a staple crop like

banana. The PNGRIS surveys collected information basically on staple crops and

grouped other cultivated plants under a collective label and therefore I was not able to

query PNGRIS to extract information specifically on chillie to be able to map the crops

distribution across PNG in ArcGIS.

The fruit fly trapping data set was summarised into mean monthly trap catches and was

similarly spatially mapped within ArcGIS. The trap catch per month for each trap in an

area were totalled and monthly averages calculated for each study fruit fly species for

57

that area. These mean abundance data were also plotted over time to generate fruit fly

seasonal phenology curves for all five study species. Linear and multiple regression,

and descriptive statistics were done in SPSS Vs 15.0 to study the relationships between

fruit fly distribution and abundance and altitude and rainfall. Linear regression was

also done for B. musae abundance versus the relative importance of banana at trapping

sites.

3.2.3 Fly species

Bactrocera bryoniae (Bryon’s fruit fly) (Figure 3.2A) is a pest of capsicums and

chillies and is widely distributed across PNG except for Bougainville and Manus

(Clarke et al., 2004). Leblanc et al. (2001) regard it as one of the few economic species

common in the Highlands (along with B. musae and Bactrocera papayae Drew and

Hancock). Bactrocera bryoniae is widely distributed down the east coast of Australia,

but is not regarded as a pest (Raghu & Clarke, 2001).

Bactrocera cucurbitae (melon fly) (Figure 3.2B) is native to tropical Asia and is an

introduced fruit fly species in PNG. The fly may have been introduced into the country

during the Second World War and has now spread and is reported to be present in

virtually all provinces, but it is absent from Manus and it was collected from Western

Highlands Province only once. It is less common in the Highlands than at lower

altitude (Leblanc et al., 2001). The fly is a major pest of cucurbits and has been

extensively researched in Hawaii, where it is also a long established invader (Stark,

1995; Vargas et al., 1997; Vargas et al., 2000a).

Bactrocera frauenfeldi (mango fly) (Figure 3.2C) is a widespread, polyphagous pest

species throughout PNG and very common throughout lowland areas. It has been

recorded in all provinces, but only a few specimens have been collected in the

Highlands where it is not considered economically important (Leblanc et al., 2001).

Bactrocera frauenfeldi is a species of major importance to PNG and other Pacific

nations (Allwood & Leblanc, 1996). The fly is invasive in Australia after having been

introduced via Cape York in the mid 1970s (Drew & Romig, 1996).

Bactrocera musae (banana fly) (Figure 3.2D) is reported to be widespread and

common on mainland PNG, where it is as common in the Highlands as at low

elevations. It is a primary insect pest of bananas in PNG, causing up to 20% fruit

58

infestation (Leblanc et al., 2001). In early 1999 it was trapped and bred from bananas

on the Gazelle Peninsula, ENB (Mararuai et al., 2001). Breeding populations also

occur on Lihir Island (New Ireland Province). A few specimens have been occasionally

trapped on Manus, but it is not confirmed whether breeding populations occur there

(Leblanc et al., 2001). Bactrocera musae’s endemic range also includes far-north

Queensland (Drew, 1989).

Bactrocera umbrosa (breadfruit fly) (Figure 3.2E) is reported to be widespread and

very common in PNG, but much less abundant in the Highlands (Clarke et al., 2004). It

has been collected in all provinces except Gulf, Enga and Southern Highlands (Leblanc

et al., 2001); it undoubtedly occurs in these provinces as well. Bactrocera umbrosa

breeds in Artocarpus species (Allwood et al., 1999) and is one the few flies whose

native range, like that of its host (Walter & Sam, 2002), extends west from the Pacific

across Wallace’s line into south-east Asia.

A B

C D

59

Figure 3.2 Fruit fly study species: (A) Bactrocera bryoniae (Tryon) (approximate

magnification x5), (B) Bactrocera cucurbitae (Coquillett) (x6), (C) Bactrocera

frauenfeldi (Schiner) (x6), (D) Bactrocera musae (Tryon) (x6), and (E)

Bactrocera umbrosa (Fabricius) (x5).

3.3 Results

3.3.1 General Patterns

Species specific patterns (developed below) in fruit fly abundance were apparent but

(with the exception of B. musae) in general numbers declined above 1200m (Table

3.2). Trapping results show that most B. bryoniae were trapped in Morobe (45% of

trapped flies) and Central (32%) provinces, B. cucurbitae was most abundant in

Central Province (64%), B. frauenfeldi (65%) and B. musae (75%) were both most

common in Morobe Province, while B. umbrosa was equally abundant on the Gazelle

(45%) and in Morobe (42%). In many cases these figures do not support the general

distribution and abundance statements supplied in Leblanc et al. (2001).

The spatial population distributions and seasonal abundances of four of the five fruit

fly species were significantly influenced by altitude and annual rainfall at the “whole

country” or national level. The influence was however variable (Table 3.3); detailed

results for each fly are reported in Sections 3.3.2 to 3.3.6. The spatial distribution and

seasonal abundance of B. musae was not significantly influenced by either altitude or

rainfall (Table 3.3). Multiple regression analysis of the effect of altitude and rainfall on

distribution and abundance also show a weak relationship (Table 3.4). Seasonal

abundance of B. bryoniae, B. cucurbitae, B. frauenfeldi and B. umbrosa at the national

level suggest that fluctuations in abundance were related to the onset and duration of

E

60

the wet and/or dry season in PNG (detailed results for each fly are in Sections 3.3.2 to

3.3.6).

Agricultural cropping systems are diverse in the country but in comparing the spatial

distribution of B. musae and B. umbrosa against the cultivated spatial distribution of

their major host, results show a close relationship between the two (see details Section

3.3.5 (Figure 3.15) and 3.3.6 (Figure 3.19) respectively). For both species abundance

was high in areas where their respective hosts are an important food source (see details

Section 3.3.5 and 3.3.6 respectively). Information on the spatial distribution of

susceptible hosts for B. bryoniae and B. cucurbitae was very restricted in PNGRIS and

so not amenable to plotting. Similarly, B. frauenfeldi is a polyphagous fly with many

potential hosts and not suitable for studying if cropping system and fly abundance

visually correlate; it was also therefore not done.

Table 3.2 The monthly trap catch (June 1998 – September 2001) of five economically

important fruit fly Bactrocera species in four study areas in Papua New Guinea

Mean monthly trap catch (± SE)

Fly species Highlands Morobe Central Gazelle All regions

B. bryoniae 14.3 ± 4.6 118.9 ± 34.3 86.0 ± 15.7 49.5 ± 13.5 68.0 ± 10.6

B. cucurbitae 3.9 ± 2.0 9.2 ± 8.4 119.5 ± 43.8 67.7 ± 25.0 54.2 ± 15.5

B. frauenfeldi 0.1 ± 0.1 714.5 ± 236.9 139.2 ± 44.6 326.8 ± 78.8 279.1 ± 66.0

B. musae 123.6 ± 42.0 505.8 ± 177.8 44.0 ± 20.3 12.6 ± 11.8 163.9 ± 48.0

B. umbrosa 0.3 ± 0.1 83.9 ± 37.5 17.8 ± 11.1 131.3 ± 28.2 53.5 ± 12.5

61

Table 3.3 Linear regression analysis of the influence of: (i) altitude or (ii) rainfall on

the abundance of five Bactrocera species within and across four study areas in

Papua New Guinea, or (iii) banana in local cropping systems for B. musae only.

Results are R2 values (and probability values in brackets). Note: Analysis not

applicable (NA) for altitude in Central because 20 of 21 traps are located at one

altitude level, nor for B.musae on the Gazelle due to inconsistent and sporadic

sampling (* = P≤0.05).

Table 3.4 Multiple regression analysis of the influence of both altitude and rainfall on

fly distribution and abundance (P≤0.05) (* = P≤0.05).

Fly species Central Gazelle Highlands Morobe Papua New Guinea

Altitude (m.a.s.l)

B. bryoniae NA +0.10 (0.24) -0.11 (0.20) +0.01 (0.77) -0.08 (0.02)*

B. cucurbitae NA -0.16 (0.13) +0.04 (0.44) -0.02 (0.61) -0.08 (0.02)*

B. frauenfeldi NA -0.34 (0.02)* +0.20 (0.07) -0.14 (0.16) -0.12 (0.003)*

B. musae NA NA -0.16 (0.11) -0.13 (0.18) -0.02 (0.28)

B. umbrosa NA -0.28 (0.05)* -0.13 (0.16) -0.08 (0.28) -0.16 (0.004)*

Annual Rainfall (mm)

B. bryoniae -0.00 (0.79) +0.19 (0.11) -0.21 (0.06) -0.19 (0.095) -0.06 (0.04)*

B. cucurbitae -0.01 (0.62) -0.16 (0.14) -0.08 (0.28) -0.13 (0.17) -0.08 (0.02)*

B. frauenfeldi -0.01 (0.76) -0.02 (0.60) +0.04 (0.46) +0.25 (0.05) +0.13 (0.002)*

B. musae -0.02 (0.53) NA -0.11 (0.20) -0.16 (0.12) -0.01 (0.35)

B. umbrosa -0.01 (0.71) -0.33 (0.02)* +0.001 (0.89) +0.31 (0.03)* +0.10 (0.01)*

Banana importance in local cropping system

B. musae +0.10 (0.16) +0.06 (0.39) +0.06 (0.34) +0.19 (0.09) +0.08 (0.02)*

Fly species Central Gazelle Highlands Morobe Papua New Guinea

Altitude (m.a.s.l) and Annual rainfall (mm)

B. bryoniae 0.05 (0.63) 0.20 (0.26) 0.21 (0.18) 0.19 (0.25) 0.11 (0.02)*

B. cucurbitae 0.02 (0.80) 0.22 (0.23) 0.28 (0.10) 0.15 (0.35) 0.13 (0.01)*

B. frauenfeldi 0.02 (0.81) 0.36 (0.07) 0.21 (0.19) 0.39 (0.04)* 0.36 (0.00)*

B. musae 0.02 (0.80) NA 0.18 (0.26) 0.28 (0.11) 0.02 (0.45)

B. umbrosa 0.01 (0.92) 0.41 (0.04)* 0.23 (0.17) 0.40 (0.04)* 0.32 (0.00*)

62

3.3.2 Bactrocera bryoniae (Tryon)

Bactrocera bryoniae was most abundant in Morobe Province (45% of total sample)

and least common in the Highlands (4% of sample) (Table 3.2). (Note: percentage

figures shown here refer mean monthly trap abundance results presented in Table 3.2

were calculated). At four of the 69 trap sites no B. bryoniae were caught (Figure 3.4),

but the fly was present in the Highlands provinces, Morobe, Central and on the Gazelle

Peninsula. As previously reported (Clarke et al. 2004) the species is present in the

Highlands, but contrary to the report of Leblanc et al. (2001) it is not a common fly in

that area. The mean monthly abundance of B. bryoniae in trap catches show numbers

are low in the Highlands (above 1200m) and along the coastline (below 600m)

suggesting B. bryoniae is a mid-altitude (600-1200m), rather than low or high altitude,

species (Figure 3.4). Rainfall, at the national level, has a significant influence on B.

bryoniae abundance (Table 3.3). This effect of rainfall on B. bryoniae is particularly

clear in Morobe where numbers from trap sites along the coastline where annual

rainfall levels are above 2000mm are low in comparison to numbers from traps situated

inland (Figure 3.5). Seasonal abundance patterns of B. bryoniae were dependent on

locality. However, in general abundance in Morobe, Central and Gazelle is lower

between January-April than it is between August and December (Figure 3.3). In the

Highlands numbers are fairly static but there is an evident decline in abundance in

June/July (Figure 3.3). The occurance of the wet season between January-April may

explain the decline in seasonal abundance in Central and Gazelle. During the wet

season in Morobe this trend is not observed (Figure 3.3). The cause may be due to the

high trap catchs from traps situated inland from Lae where less rainfall occurs (Figure

3.5).

63

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

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HighlandsMorobeCentralGazelle

Figure 3.3 Seasonal abundance of Bactrocera bryoniae (Tryon) in four areas in Papua

New Guinea between June 1998 and September 2001

64

Figure 3.4 Mean monthly abundance of Bactrocera bryoniae at different altitude levels in Papua New Guinea between June 1998 and September

2001.

65

Figure 3.5 Mean monthly abundance of Bactrocera bryoniae against annual rainfall levels in Papua New Guinea between June 1998 and

September 2001

67

3.3.3 Bactrocera cucurbitae (Coquillett)

Contrary to existing assumptions, abundance of B. cucurbitae was not uniformly

distributed across lowland PNG (Table 3.2). The highest trap catches were caught in

Central (64% of sample) while the lowest were in the Highlands (1% of sample) (Table

3.2). At the national level temperature and rainfall had a significant influence on B.

cucurbitae distribution and abundance. Eighty-six percent of flies were trapped

between 0-600m; indicated by large green circles on map (Figure 3.7) and abundance

was found to decrease significantly as altitude increased. Between the Highlands and

Morobe only one trap site stands out with the highest mean monthly abundance catch

in both areas (Figure 3.7). Rainfall also has a significant influence at that level (Table

3.3). Seventy-four percent of flies were collected in areas that had 1000-2000 mm

annual rainfall. A single trap between Kainantu and Lae in the 1000-1500 mm rainfall

area had the largest abundance compared to others in the same area and this area

experiences <1500mm of annual rainfall. An effect indicating that B. cucurbitae spatial

distribution is limited to elevations below 600m (Figure 3.7) and to areas that

experience less than 1500mm annual rainfall (Figure 3.8). Seasonal abundance of B.

cucurbitae in each study area is different (Figure 3.6). While the patterns are different,

in general abundance in Central and on the Gazelle fall between January-June and

increase between July-December. In Morobe and the Highalnds seasonal abundance is

higher during January-June than between June-December (Figure 3.6).

68


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50

100

150

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Figure 3.6 Seasonal abundance of Bactrocera cucurbitae (Coquillett) in four areas in

Papua New Guinea between June 1998 and September 2001

69

Figure 3.7 Mean monthly abundance of Bactrocera cucurbitae at different altitude levels in Papua New Guinea between June 1998 and

September 2001

70

Figure 3.8 Mean monthly abundance of Bactrocera cucurbitae against annual rainfall levels in Papua New Guinea between June 1998 and

September 2001

71

3.3.4 Bactrocera frauenfeldi (Schiner)

The distribution and abundance of B. frauenfeldi in PNG is significantly influenced by

altitude and rainfall (Table 3.3). Results show that this species is largely limited in

distribution to areas below 1200m because it is particularly common in lowland areas

(0-600m) (Figure 3.10). Within this altitude range abundance is related to local rainfall

levels for numbers increase in areas that receive more than 1500 mm of annual rainfall

(Figure 3.11). The high numbers caught in traps in and around Port Moresby are

indicative of this, more so to the availability of water; similar to a trap located further

south of the city (Figure 3.11). The highest numbers of B. frauenfeldi were collected in

Morobe (65%), Gazelle (24%), and Central and virtually none in the Highlands (12%)

(Table 3.2). Rainfall appears to be the major influential factor of both population

distribution and abundance for this species, with the common feature of the lowland

areas where the fly is abundant being above average (> 2000mm) annual rainfall. In

this context it is important to note that there are many dry lowland sites (esp. in

Central) where the fly is rare or absent. In multiple regression analysis, the

combination of rainfall and altitude explained 36% of the variation in the trapping data

(Table 3.3). The seasonal abundance of B. frauenfeldi is notably dependent on rainfall

levels. During the wet season from January-April numbers are high in dry rain-shadow

areas like Central and also high in Morobe (it is the dry season there) (Figure 3.9). In

relatively wet areas like the Gazelle numbers are consistent throughout the year

increasing slightly between July to December.

72


Ave

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0

500

1000

1500

2000

2500


Figure 3.9 Seasonal abundance of Bactrocera frauenfeldi (Schiner) in four areas in

Papua New Guinea between June 1998 and September 2001

73

Figure 3.10 Mean monthly abundance of Bactrocera frauenfeldi at different altitude levels in Papua New Guinea between June 1998 and

September 2001

74

Figure 3.11 Mean monthly abundance of Bactrocera frauenfeldi plotted against annual rainfall levels in Papua New Guinea between June 1998

and September 2001

75

3.3.5 Bactrocera musae (Tryon)

All 54 traps located on the mainland of PNG had samples of B. musae, but the fly was

not uniformly abundant. The greatest abundance of B. musae was in Morobe (75%),

followed by the Highlands (17%), and then Central (7%) (Table 3.2). Unlike the other

four fly species, spatial abundance was not significantly related to altitude or rainfall

(Table 3.3). The fly was sampled from sea level to above 1800m (Figure 3.13) and in

areas that experienced between 1000-3500 mm of annual rainfall (Figure 3.14).

Seasonal abundance appeared very much dependent on locality. In Morobe populations

increased January-April and again May-July. In the Highlands population peaks

occurred between January-March and a degree longer July-October. In comparison

there was no real difference in Central (Figure 3.12). Distribution of banana fly was

not correlated with the relative importance of banana in local cropping systems within

Morobe, the Highlands, Central or Gazelle. However, when abundance was correlated

against the relative importance of banana across all four areas, abundance did rise as

the importance of banana as a food crop increased in an area (r= 0.285, p = 0.02)

(Table 3.3, Figure 3.15). On the Gazelle B. musae is known to be invasive and, at the

time data was collected, the fly was still spatially and temporally sporadic. Seven of 15

traps on the Gazelle Peninsula did not trap banana fly and due to this inconsistency and

low numbers seasonal phenology patterns could not be generated (but see data

presented in Chapter 6: Bactrocera musae (Tryon) in a novel environment: banana fly

as an invasive organism on the Gazelle Peninsula, Papua New Guinea). Observations

made during field work for this thesis indicate that the fly is still expanding its range

on the Gazelle.

76


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600

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1000

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1400

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HighlandsMorobeCentral

Figure 3.12 Seasonal abundance of Bactrocera musae in three areas in PNG between

June 1998 and September 2001

77

Figure 3.13 Mean monthly abundance of Bactrocera musae at different altitude levels in Papua New Guinea between June 1998 and September

2001

78

Figure 3.14 Mean monthly abundance of Bactrocera musae plotted against annual rainfall levels in Papua New Guinea between June 1998 and

September 2001

79

Figure 3.15 Mean monthly abundance between June 1998 and September 2001 of Bactrocera musae plotted against the relative importance of

banana as a food crop in cropping systems in Papua New Guinea

80

3.3.6 Bactrocera umbrosa (Fabricius)

Bactrocera umbrosa is most abundant on the Gazelle (49% of total sample) and in

Morobe (42%) but much less common elsewhere (Table 3.2, Figure 3.17). Abundance

is significantly negatively correlated with altitude (Table 3.3) and this is reflected in

the very low numbers trapped in the Highlands (Figure 3.17). Rainfall has a significant

influence on trap catch (Table 3.3). Traps situated in areas with >1500mm of annual

rainfall have high numbers (Figure 3.18). In Morobe trap catch in Lae is higher than

those situated away from the city and on the Gazelle most traps catch high numbers

(Figure 3.18). Seasonal abundance of B. umbrosa in the two main areas where it was

trapped (i.e. Morobe and Gazelle) were similar, with peaks coinciding with the wet

season (Figure 3.16). In these localities wet seasons are, coincidently, when breadfruit

(B. umbrosa’s major host) comes into season. It is thus unclear if rainfall pattern, host

fruiting cycle, or a combination of both, is driving annual cycles. The seasonal

abundance of B. umbrosa seen here mirrors the seasonality for breadfruit in the Pacific

(Nix, 1986; Houlder et al., 2001). The host of B. umbrosa is breadfruit a predominantly

low altitude plant (<1800m). The insignificance of breadfruit as an important food in

the Highlands region may influence the lack of breadfruit trees and fruit which may

explain the low abundance of flies at higher altitudes (Bourke et al., 1998) (Figure

3.19). Low abundance levels represented by orange circles are found in areas where

breadfruit is not important while green and blue circles showing higher abundance are

found in areas where breadfruit is part of the local diet (Figure 3.19). Where breadfruit

is part of the local diet it was recorded (in PNGRIS) as a nut in combination with other

‘nuts’. The combinations vary considerably across PNG and breadfruit was also not

categorised as was banana; as a dominant, subdominant or a minor ‘nut’. A visual

comparison was therefore done and presented (Figure 3.19). Map shows area where

breadfruit is grown. Statistical analysis was not done to verify the visual results

because of the difficulties of extracting detailed breadfruit data (as was done for

banana; dominant and subdominant food crop) from PNGRIS. Thus while rainfall and

altitude explained over 30% of the variation in the B. umbrosa trapping data it may be

that both of these variables are indirectly acting on the fly through host plant

abundance and fruiting season.

81


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Figure 3.16 Seasonal abundance of Bactrocera umbrosa in four areas in PNG between

June 1998 and September 2001

82

Figure 3.17 Mean monthly abundance of Bactrocera umbrosa at different altitude levels in Papua New Guinea between June 1998 and

September 2001

83

Figure 3.18 Mean monthly abundance of Bactrocera umbrosa plotted against annual rainfall levels in Papua New Guinea between June 1998

and September 2001

84

Figure 3.19 Mean monthly abundance between June 1998 and September 2001 of Bactrocera umbrosa in Papua New Guinea where breadfruit

(Artocarpus spp.) is grown

85

3.4 Discussion

Current distribution records of fruit fly species in different parts of PNG either make

no comment about relative abundance (e.g. Clarke et al. 2004), or make statements

about distribution and abundance with no supporting data (e.g. Leblanc et al. 2001).

The data presented in this chapter has analysed and presented trapping data against

temperature (as related to altitude) and rainfall levels to identify the differential

influence of both on the fine scale spatial and temporal distribution of five fruit fly

species. It has also been able to show that host availability for two species (B. musae

and B. umbrosa) is an influential factor in their distributions but one which requires

further study. All species, with the exception of B. musae, are not common in the

Highlands provinces and there are studied areas like the provinces of Enga and

Southern Highlands where species are absent.

Attempts to use this spatial data to develop predictive distribution models (for example

to predict where B. musae might establish if introduced to another regional country)

were unsuccessful. Environmental matching programs such as Climex and BioClim are

predictive modelling tools which use information on climatic data to predict the

potential distribution range of a pest species (Yonow & Sutherst, 1998; Sutherst et al.,

1999; Vera et al., 2002; Paul et al., 2005; Stephens et al., 2007). This information is

vital for setting up appropriate and effective management measures (Baker, 1996;

Wright et al., 2005; Worner & Gevrey, 2006). I studied Climex and Dymex programs

to investigate the potential distribution of B. musae but found they were not applicable

for PNG. The country does not have adequate numbers of weather stations and the kind

of long-term consistently collected detail on weather variables such as temperature and

rainfall required to run the programmes. This problem was accentuated by the

topographical diversity of PNG. There are programmes available with which weather

variables between weather stations can be fitted but such programs still require either a

relatively even terrain between stations or a higher density of stations. The terrain of

PNG is not relatively even and the number of stations is low. Given the large number

of plant pests and diseases which are native to PNG and could invade neighbouring

countries, or conversely the number of offshore pests which might enter PNG and

spread, the inability to use ecological distribution models is a potentially serious

problem for both PNG and its neighbours.

86

With respect to B. musae, while temperature and rainfall were not found to have a

significant influence on the fly’s spatial and temporal distribution, both may play a role

on distribution and abundance at the ‘within province’ level. In low rainfall areas, such

as Central province, abundance of B. musae in dry areas outside of Port Moresby are

quite low for an area where banana is an important food and commodity crop (Hanson

et al., 2001). These abundance levels are also much lower than those in the Morobe

and Highlands study areas. The positive correlation between the relative importance of

banana in an area and the abundance of B. musae seen at the national level shows that

host availability is an important factor for further study. Specifically, there is need for

more targeted research to determine if host availability does indeed drive and sustain

banana fly population dynamics. Here host availability information is related to the

importance of the crop in an area but availability and importance may not be the same

because a host may be widely cultivated in an area but its importance as a staple food

may be low. It is therefore necessary to clarify whether trapping data can relate

abundance to host distribution and relate this measurement to the impact caused by a

study species population on susceptible hosts.

The low population abundance of four fruit fly species at higher altitudes provides

some resolution to the debate that the pest status of different fruit fly species may not

be the same at all localities within PNG, specifically when comparing between lowland

and highland production areas. These areas of low fruit fly population densities can be

monitored and managed to be classified as low-risk areas for commodity production.

Pre- and post-harvest management levels of pest species at higher altitude levels may

therefore not need to be as stringent as those required of production areas below

1200m where fly abundance is higher. Due to the different effects that temperature and

rainfall has on the five studied fruit fly species, control strategies will have to be

designed for individual species and the use of generic management models would be

inappropriate. The management of economically important fruit fly species in PNG

must incorporate long-term strategies that monitor infestation levels to help ensure that

the marketability of potential susceptible commodities is not hindered by the lack of or

inadequate number of required pest fruit fly control measures. This also highlights the

necessity to improve local quarantine measures to monitor and maintain the current

distribution of pest species and areas with low-pest-risk status.

87

3.5 Thesis Progress

The study of the distribution and abundance of B. musae and four other economically

important fruit fly species in PNG provides essential information toward the

development of the PNG banana PRA. Knowing how altitude (which can be a

surrogate for temperature), rainfall and host availability influences fly distribution can

be used to model and predict the likely risk of establishment of the fly in a novel

environment (a component of Step 2 of the PRA process), while determining possible

sites of low pest pressure for production is of relevance in developing risk management

options (Step 3 of the PRA). The following chapter specifically studies the impact of

natural B. musae populations on banana in PNG. The results pursue the question of

identifying if local abundance of the fly is linked to banana infestation rates. This

information is needed to identify the levels of risk associated with banana fly should it

establish in a novel area and for identifying potential low risk productions areas, again

relevant to Steps 2 and 3 of the PRA process.







3

2

1

Distribution and abundance of five economically important fruit fly species in Papua New Guinea [Chapter 3]







3

2

1







3

2

1

Distribution and abundance of five economically important fruit fly species in Papua New Guinea [Chapter 3]

Figure 3.20 Pest Risk Analysis process; with arrow indicating which step in process

information generated in this chapter has been collected for

88

Chapter 4. Infestation of bananas by Bactrocera musae (Tryon) in Papua New Guinea

4.1 Introduction

Banana (Musa spp.) is the fourth most important food crop in the world and in

developing countries it is the fourth most important commodity (Gold et al., 2002;

Ploetz, 2004). The cultivars most commonly produced for regional and international

trade are dessert eating Cavendish varieties (Stover, 1986). In Papua New Guinea

(PNG), there is a large range of banana varieties farmed at the subsistence and semi-

commercial farming level. The cultivars grown include both cooking varieties and

dessert types, including Cavendish (Bourke et al., 1998; Hartemink & Bourke, 2001;

Gunther et al., 2003). Bananas are cultivated from sea level up to 2200 meters above

sea level (Bourke et al., 1998). There are 235 banana accessions in PNG and over 100

varieties are farmed (Arnaud & Horry, 1997). With one exception, however, most

banana varieties have localised areas of production; only Cavendish is commonly

cultivated throughout the country (Gunther et al., 2003; Kambuou, 2005).

Banana production levels in PNG are often constrained by pest problems (Smith, 1976,

1977b; Tomlinson, 1984; King et al., 1988; Masamdu et al., 1989). One-hundred and

twelve organisms have been associated with banana in PNG (Chapter 2: Review of

banana (Musa spp.) pests in Papua New Guinea) and, of these, fourteen are reported to

be commonly observed and managed. Bactrocera musae (Tryon) (banana fly) is one of

these and is reported to be the major pest (Pone, 1994; Leblanc et al., 2001), or one of

several major pests (Kambuou, 2004), on banana in PNG. The actual infestation rate of

B. musae on PNG bananas is poorly documented, despite its apparent importance.

Leblanc et al. (2001) report 0-75% B. musae infestation on banana in PNG, but provide

no information on sample size or banana variety. Sar et al. (2001) report 25%

infestation on Kalapua variety in East New Britain Province (ENB) and 30% on

Cavendish in Central Province, but again show no assessment methodology or

information on sample size.

Leblanc et al. (2001), if read uncritically, could be used as evidence that all banana

varieties cultivated in PNG have high infestation levels and that infestation is common

89

across all parts of PNG. This would be unfortunate as Leblanc et al. (2001) give no

measure of banana varietal susceptibility to B. musae (a critical issue given how many

varieties there are) and restricted data on locality differences (again important given

known information on the distribution of the fly [Chapter 3: Distribution and

abundance of five economically important fruit fly species in PNG]). Formal

documentation on B. musae infestation levels on different banana varieties in PNG is

rare. Smith (1977, 1976) described higher infestation levels caused by B. musae on

short varieties of banana compared to a taller variety. He described Giant Cavendish as

the tall variety and the shorter varieties to be Tui/Robusta and Dwarf Cavendish.

Reports done for the commercial production of Giant Cavendish in PNG state that B.

musae infestation is a problem, particularly when the fruit is harvested ripe (Fooks,

1989, 2002).

The small amount of documentation available on B. musae infestation rates on PNG

banana is not of a standard which complies with international trade and phytosanitary

requirements. No detailed impact assessment has been carried out on Cavendish,

geographically the most widely planted banana in PNG and a variety likely to be

considered for international trade. Nor is there, with the exception of Smith (1977), any

quantified field information on susceptibility of different banana varieties. The main

objectives of this chapter were therefore twofold. The first was to carry out a national

level damage assessment survey of B. musae on Cavendish, so as to assess infestation

levels in different regions of PNG. I wanted particularly to determine if differences in

abundance of B. musae (as determined in Chapter 3) translated to lower or higher

levels of fruit infestation. If so, then cropping district could potentially be used as a

component of a banana market access tool (i.e. by picking production regions with low

infestation rates). Because it is so widely planted, Cavendish was the only variety for

which a uniform national survey could be done. The second objective investigated

differences in varietal susceptibility to banana fly infestation when bananas were

grown in a common-garden trial. Should evidence for varietal difference be confirmed,

then future market access work could concentrate on searching for commercial

varieties of low susceptibility, a recognized risk management tool (Armstrong, 2001;

Rattanapun et al., 2009).

90

The chapter falls into four parts. All investigate levels of infestation caused by B.

musae on banana varieties. The initial three parts assess damage impact on more than

one variety while the last carries out the extensive damage assessment survey on a

single variety. The initial component shows results from general host surveys of

banana carried out in different parts of PNG showing infestation levels of B. musae on

a number of cultivated banana varieties. The second part is a methodology trial, the

results of which were used to design an appropriate sampling strategy for the

Cavendish survey. The third section reports on a common-garden experiment which

looked at infestation levels on four different banana varieties, while the fourth section

reports on a national damage assessment survey of banana fly infestation in Cavendish.

4.2 Materials and methods

4.2.1 Differences in varietal susceptibility

General banana host surveys. Numerous host surveys of banana were carried out in

different parts of PNG. These samples were not collected in any methodological

manner and therefore were not analysed but are presented here to show the varieties of

banana sampled and having fruit fly infestation in different provinces. Recorded

banana varieties are labelled using common names or for varieties in Central and ENB

using germplasm identification. Banana germplasm collections in Central are kept at

the NARI’s dry-lowlands agriculture station at Laloki and in ENB at the lowlands

agriculture experiment station at Kerevat in ENB where germplasm collections are

kept. These samples of cultivated banana varieties were collected at different maturity

stages and were incubated as single finger samples or in multiple finger samples.

Records were made of the number of pupae developing and the number of adult flies

emerging from each sample.

Methodology trial. The trial was run on the Gazelle Peninsula, East New Britain

province (ENB) from November to December 20021. Three varieties of cooking

banana were used in the trial: Kekiau (PNG101 Musa Eumusa AA), Vudu Papua

(PNG004 Musa Eumusa AA), and Tukuru (PNG118 Musa Eumusa ABB). The

morphological and taxonomic characteristics of each variety are described in the PNG

1 The field work for this trial was undertaken prior to my PhD candidacy. However, I fully designed and implemented this trial, the data of which remained unanalysed until I started my PhD. All data analyses reported here were undertaken while I was an enrolled PhD candidate.

91

Musalogue (Arnaud & Horry, 1997). The banana bunches were collected from gardens

in the Vudal and Vunapalading areas northwest from Kokopo and Rabaul and an area

into which B. musae populations were still spreading (Mararuai et al., 2001). Whole

banana bunches were hung at three different locations on the eastern side of the

Gazelle Peninsula between Kokopo (04° 20’S, 152° 18’E) and Rabaul (04° 11’S, 152°

08’E), an area where banana fly is present (Mararuai et al., 2001 and Chapter 3). At

each location a mature, harvested banana bunch of each variety were simultaneously

hung uncovered on posts about two meters off the ground and exposed to wild flies for

a week. After this time, individual fingers were removed and setup over moist sawdust

for the recording of fly emergence (and hence infestation levels). Details on the

methods used for rearing-out fruit flies from harvested fruit (for this and subsequent

trials) are described and illustrated in Leblanc et al. (2001) (see Appendix 1). The

selection procedure for finger samples was as follows: the top two hands on the bunch

were referred to as the top part of the bunch and from these two hands five fingers

were randomly selected. Sample selection was concentrated on the top two hands

because field observation showed more flies sitting on the top half of the banana bunch

and maturity in banana fingers began at this location. The next two to three hands

below were referred to as the middle part and from here three fingers were randomly

selected. From the remaining hands below the middle part, two fingers were randomly

selected. Six bunches of each of the three banana varieties were exposed and sampled,

leading to a total sample of 180 banana fingers. A two-way ANOVA was carried out to

determine if there was any significant differences in banana fly infestation rates at

different sample locations within the bunch. The intention was that if such a difference

was found, subsequent surveys would sample hands within a banana bunch which had

the highest probability of being infested.

Common garden experiment. A banana garden was planted in mid-2007 at the [PNG]

National Agricultural Research Station Laloki (09°23’S, 147°17’E), in the Central

province of PNG, just outside the capital city of Port Moresby. Three fields (3

replicates) were planted using a randomised planting allocation design with ten plants

of each of four banana varieties: Kokopo 1 (PNG030); Kalapua [dwarf] (PNG171);

Daru (PNG131); and Kurisa. The characteristics of PNG030, PNG171 and PNG131

are supplied in Musalogue (Arnaud & Horry, 1997), but Kurisa is not included in that

catalogue. These four are economically important banana varieties PNG. Banana

92

bunch harvest began in February 2007 and sampling continued until March 2009.

When bunches were mature and ready for harvest, multiple fingers were setup in single

incubation containers over moist sawdust as previousy described. The entire bunch was

setup for observation as single fingers, not a subset of fingers from the bunch as in the

Methodology trial. A record was made of the number of pupae recovered and the

number of adult flies that emerged from each sample/container. The date of submission

for this thesis fell prior to the completion of the trial. In addition, complete sampling of

the all varieties was not done due to labour constraints at the garden but what data was

recorded is presented here. Low banana fly infestation levels and incomplete sampling

meant that formal analysis of data could not be undertaken, rather results are

summarized and presented graphically. The purpose of this experiment was to

investigate B. musae infestation levels on economically important banana varieties

other than Cavendish.

4.2.2 National Cavendish survey

I carried out the national survey between November 2007 and January 2008 with the

assistance of technical staff from the National Agricultural Research Institute (NARI)

and Fresh Produce Development Authority. There were three reasons why this survey

was done at this time of the year. Firstly, during the course of my PhD study this time

frame was the most logistically fesible during which I could carry out the survey.

Secondly, it is during this time of the year when the fluctuations in seasonal abundance

of the study fly, B. musae, are at their lowest in Morobe and the Highalnds but are

uniform to Central (Section 3.3.5 - Chapter 3). This is important because it can be

assumed that the natural B. musae populations in samping areas are similar and one

area will not have a higher population number which may consequently have an effect

on infestation levels and prevent comparative analysis between surveyed areas.

Thirdly, the resultant information gathered during this time period of low seasonal

abundance is certainly a factor that can be incorporated into management systems and

approaches into fruit fly management and be used as a banana market access tool.

There were 22 areas or sampling locations, evenly spread in number over the four PNG

production areas which were analysed in Chapter 3. Five locations were situated in the

Central province; seven were located in the Highlands zone (covering three locations

in Chimbu province and four in Eastern Highlands province (EHP)), six in Morobe

province, and four on the Gazelle Peninsula, ENB (Figure 4.1). At each location five

93

mature bunches of Cavendish banana were harvested. Within a location the bunches

may have all come from one site (a single farm for example), or neighbouring sites

(e.g. adjoining farms) depending on availability: in total there were 57 local collection

sites (11 in Morobe, 18 in EHP, 12 in Chimbu, nine in Central, and seven on the

Gazelle). Detailed collection information for each bunch, including site coordinates,

weight and number of fruit sampled are provided in Table 4.1. The sampling

methodology used to select bananas from a bunch was that determined from the

Methodology trial. Altogether there were 111 banana samples collected; 31 in Morobe,

20 in EHP, 15 in Chimbu, 26 in Central and 19 on the Gazelle. All subsamples were

incubated over moist sawdust and a record was made of pupal and adult emergence

numbers. Again, because of the very low banana fly infestation levels recorded, formal

analysis of data was not undertaken, rather results are summarized and presented

graphically.

Figure 4.1 Map of harvest spots for Cavendish banana during the fruit fly damage

assessment survey (November 2007-January 2008) carried out in five provinces

in Papua New Guinea

94

Table 4.1 Sampling details for the national Cavendish survey

Province Sample location

Sample site GPS reading Stage of Maturity

*

Weight (g)

No of banana fingers (B-

Bunch) Latitude (S) Longitude (E)

Morobe Kaiapit Mutzing 06° 20΄48˝ 146°13΄51˝ MG/R 4572.1 32 Nasuapum Orockangku 06°35΄18˝ 146°49΄22˝ MG 3198.7 24 Ngarefe 06°35΄36˝ 146°48΄41˝ MG 2411.4 18 Ngarefe 06°35΄36˝ 146°48΄41˝ MG 3603.6 27 Gomamos 06°35΄48˝ 146°48΄31˝ MG 1916.4 15 Gomamos 06°35΄48˝ 146°48΄31˝ MG 1950.8 15 Gabensis SDA Primary Sch 06°41΄51˝ 146°48΄00˝ MG 3865.5 29 SDA Primary Sch 06°41΄42˝ 146°48΄02˝ MG 941.4 7 SDA Primary Sch 06°41΄42˝ 146°48΄02˝ MG 1325.7 10 SDA Primary Sch 06°41΄42˝ 146°48΄02˝ MG 1960.4 15 SDA Primary Sch 06°41΄42˝ 146°48΄02˝ MG 2417.9 18 Bundun Training Centre 06°51΄16˝ 146°37΄06˝ GM 3474.2 26 Training Centre 06°51΄16˝ 146°37΄06˝ MG 1741 13 Training Centre 06°51΄16˝ 146°37΄06˝ MG 18614.9 14 Training Centre 06°51΄16˝ 146°37΄06˝ MG 3001.2 23 Training Centre 06°51΄16˝ 146°37΄06˝ MG 1176.7 9 Bukawa Poahum 06°39΄22˝ 147°02΄17˝ MG 1355 10 Poahum 06°39΄22˝ 147°02΄17˝ MG 2021.3 15 Didiman station 06°38΄59˝ 147°02΄14˝ MG/R 3814.5 29 Liklik Rot, Situm 06°39΄50˝ 147°03΄44˝ MG 1646.2 12 Liklik Rot, Situm 06°39΄50˝ 147°03΄44˝ MG 1983.9 15 Liklik Rot, Situm 06°39΄50˝ 147°03΄44˝ MG 1900.9 14 Bubia NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 2187.3 26 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 3078.3 23 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 5022.2 38 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 2347.9 18 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 3372.7 33 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 4430.1 34 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 3702 26 NARI Bubia 06°40΄04˝ 146°54΄75˝ MG 1881.7 30

Eastern Highlan

ds Watabung Top - Sharp Kona 06°04΄19˝ 145°12΄41˝ MG 3574.2 30

Top - Sharp Kona 06°04΄19˝ 145°12΄41˝ MG 4313.9 41 Fionoku 06°04΄06˝ 145°12΄24˝ MG/R 3028.9 30 Watabung station 06°04΄53˝ 145°12΄28˝ MG/R 3536.7 35 Efaka 06°04΄39˝ 145°12΄19˝ MG/R 4853.7 38 Goroka Kofa, Korepa 06°02΄08˝ 145°15΄39˝ MG/R 7199.3 43 Kerefa 06°01΄40˝ 145°23΄36˝ MG 4145.6 36 Massy, Okiufa 06°03΄05˝ 145°23΄07˝ MG 2661.4 26 Kabiufa village 05°59΄45˝ 145°22΄20˝ R 5127.7 36 Fanifa 06°05΄53˝ 145°23΄45˝ R 5819.6 32 Henganofi Kapitina primary 06°17΄28˝ 145°42΄55˝ MG 6405.9 50 Avani, Kompri 06°18΄00˝ 145°41΄00˝ MG 6433.3 32 Agafa 06°18΄17˝ 145°38΄59˝ R 6359.2 35 Seganafamo 06°14΄54˝ 145°35΄20˝ MG 3524.8 25 Manicon 06°14΄59˝ 145°33΄45˝ MG 5125.9 47 Table continued overleaf

95

Table 4.1 continued Sampling details for the national Cavendish survey



*

Weight (g)



Kainantu/Aiyura Twimpika 06°17΄25˝ 145°51΄12˝ MG 2583 44

Konofi 06°18΄16˝ 145°52΄35˝ MG 2231.5 26 Aiyura 06°19΄56˝ 145°53΄55˝ MG 2839.1 29 NARI Aiyura 06°20΄39˝ 145°54΄19˝ MG 2920.2 30 NARI Aiyura 06°20΄39˝ 145°54΄19˝ R 4341.3 29

Chimbu Kerowagi Munju 05°56΄23˝ 144°51΄20˝ MG 3161.6 29 Tauglpene 05°54΄24˝ 144°51΄14˝ MG 1717.8 26 Tauglpene 05°54΄24˝ 144°51΄14˝ MG 7580.3 45 Simgau 05°56΄42˝ 144°51΄39˝ MG 6600.2 52 Dangma Road 05°56΄45˝ 144°51΄44˝ MG 4414.2 35 Chuave Migin 06°07΄08˝ 145°06΄57˝ R 4209.9 34 Agugu 06°06΄57˝ 145°06΄47˝ MG 3399.3 38 Agugu 06°06΄48˝ 145°06΄39˝ MG 3420.5 35 Migin 06°07΄08˝ 145°06΄57˝ MG 1624.8 19 Migin 06°07΄08˝ 145°06΄57˝ MG 984.3 9 Kundiawa Guo market 05°59΄43˝ 144°56΄18˝ MG/R 5443.9 36 Guo 05°59΄51˝ 144°56΄34˝ MG/R 3438 28

Works compound 06°01΄34˝ 144°58΄12˝ MG/R 3061.8 24

Works compound 06°01΄34˝ 144°58΄12˝ MG/R 1853.2 15

DPI compound 06°01΄23˝ 144°58΄40˝ MG/R 5031.1 34 Central Tubusereia Kogo 09°32΄59˝ 147°21΄01˝ MG 1340 20

Kogo 09°32΄59˝ 147°21΄01˝ MG 2680 31 Kogo 09°32΄59˝ 147°21΄01˝ MG 1020 18 Kogo 09°32΄59˝ 147°21΄01˝ MG 600 15 Barakau 09°37΄51˝ 147°24΄38˝ MG 4300 30 Barakau 09°37΄51˝ 147°24΄38˝ MG 700 14 Doa Lolorua 08°57΄41˝ 146°57΄06˝ MG 2230 39 Noosa 08°56΄06˝ 146°57΄06˝ MG 4550 31 Noosa 08°56΄13˝ 146°57΄19˝ MG 5370 37 Noosa 08°56΄13˝ 146°57΄19˝ MG 2500 32 Noosa 08°56΄13˝ 146°57΄19˝ MG 3380 26 Vanapa Vabi village 09°10΄ 147°12΄ MG 2720 24 Vabi village 09°10΄ 147°12΄ MG 1380 25 Vabi village 09°10΄ 147°12΄ MG 1350 18 Berere village 09°09΄ 147°10΄ MG 2320 20 Berere village 09°09΄ 147°10΄ MG 1120 21 Veimauri Solien farm 09°02΄58˝ 147°04΄52˝ MG 1370 24 Solien farm 09°02΄58˝ 147°04΄52˝ MG 1820 28 Solien farm 09°02΄58˝ 147°04΄52˝ MG 1680 20 Solien farm 09°02΄58˝ 147°04΄52˝ MG 3860 47 Solien farm 09°02΄58˝ 147°04΄52˝ MG 2130 27 Kwikila Saroakeina 09°49΄40˝ 147°44΄05˝ MG 3920 26 Saroakeina 09°49΄40˝ 147°44΄05˝ MG 3520 28 Sivitatana 09°49΄39˝ 147°45΄57˝ MG 3920 32 Sivitatana 09°49΄39˝ 147°45΄57˝ MG 2910 30 Sivitatana 09°49΄39˝ 147°45΄57˝ MG 3180 33 Table continued overleaf

96

Table 4.1 continued Sampling details for the national Cavendish survey



*

Weight (g)



East New Kokopo Ulapea 04°20΄38˝ 152°18΄25˝ MG 5300 38 Britain Ulapea 04°20΄38˝ 152°18΄25˝ MG 3950 29 Ulapea 04°20΄38˝ 152°18΄25˝ MG 3430 30 Ulapea 04°20΄38˝ 152°18΄25˝ MG 3180 34 Ulapea 04°20΄38˝ 152°18΄25˝ MG 4730 39 Rabaul Pilapila 04°11΄29˝ 152°08΄20˝ MG 3180 28 Vuvu 04°12΄41˝ 152°07΄35˝ MG 2940 27 Vuvu 04°12΄41˝ 152°07΄35˝ MG 5530 34 Karakakaul 04°12΄35˝ 152°07΄12˝ MG 4130 24 Keravat NARI Keravat 04°19΄ 152°01΄ MG 2910 28 NARI Keravat 04°19΄ 152°01΄ MG 4460 29 NARI Keravat 04°19΄ 152°01΄ MG 4650 46 NARI Keravat 04°19΄ 152°01΄ MG 3600 30 NARI Keravat 04°19΄ 152°01΄ MG 5060 41 Induna Induna Plantation 04°35΄56˝ 152°22΄06˝ MG 4840 34 Induna Plantation 04°35΄56˝ 152°22΄06˝ MG 2960 30 Induna Plantation 04°35΄56˝ 152°22΄06˝ MG 2890 37 Induna Plantation 04°36΄13˝ 152°21΄48˝ MG 6800 39 Induna Plantation 04°36΄13˝ 152°21΄48˝ MG 3200 22

* Stage of maturity: MG – mature green, R – ripe

4.3 Results

4.3.1 Differences in varietal susceptibility

General banana host survey. Cultivated banana varieties were sampled in five

provinces (Central, East New Britain, Madang, Morobe, and Western Highlands)

(Table 4.2). In the Western Highlands mature green Kalapua samples did not have fruit

fly infestation (Table 4.2). In the Central province twenty-one varieties were sampled

but only five varieties were infested. Mature-green to ripe samples of Cavendish,

Kalapua, OBP21, OBY6 and Yawa were infested by B. musae (Table 4.2). In East

New Britain, twenty-one varieties were collected but four of these had infestation. Ripe

samples of KMC15, Ramarama and Tukuru had B. frauenfeldi infestations while ripe

samples of Yawa had both B. frauenfeldi and B. musae. In Madang two varieties were

sampled but only one variety, Kalapua had B. musae infestation. In Morobe three

97

varieties were sampled and mature-green to ripe samples were infested with B. musae

(Table 4.2).

Table 4.2 Damage assessment records of miscellaneous host records of banana

varieties sampled between 1998 and 2000 in Western Highlands, Central, East

New Britain, Madang, and Morobe provinces in Papua New Guinea

Province Date Banana variety Stage of

Maturity*No of

samples

No of samples infested

Bactrocera species reared

Western Highlands Oct 2000 Kalapua M/G 34 0 Central Mar 2000 Acc. 052 banana M/G 15 0 Mar 2000 Acc. 103 banana M/G 10 0 Mar 2000 Acc. 123 banana M/G 5 0 Mar 2000 Acc. 144 banana M/G 10 0 Mar 2000 Acc. 268 banana M/G 5 0 Feb 2000 Acc. 306 banana M/G 7 0 May 1999 Cavendish R 100 71 B. musae Aug 2000 Cavendish dwarf G 40 14 B. musae Aug 1999 Kalapua M/G 16 1 B. musae Sep 1999 Kurisa G 14 0 Feb 2000 NBE 16 banana M/G 5 0 Mar 2000 NBF9 banana M/G 5 0 Mar 2000 NBH 10 banana M/G 10 0 Feb 2000 NBK 11 banana M/G 8 0 Feb 2000 NBM 17 banana M/G 10 0 Mar 2000 OBA 5 banana M/G & R 19 0 Mar 2000 OBB 11 banana M/G 13 0 Mar 2000 OBP 21 banana M/G 5 1 B. musae Feb 2000 OBX8 banana M/G 4 0 Mar 2000 OBY 15 banana M/G 15 0 Feb 2000 OBY 6 banana M/G 10 1 B. musae Mar 1999 Yawa M/G 101 14 B. musae

East New Britain

Apr 2000 Buka R 23 0

Dec 1997 Chinese dwarf KMD 6 G 2 0

Dec 1997 Chinese dwarf M/G & R 9 0 Dec 1997 Chinese dwarf M/G 41 0 Jan 1998 Chinese dwarf M/G & R 20 0 Feb 1998 Chinese dwarf M/G 26 0 Mar 1998 Chinese dwarf M/G 10 0

Dec 1997 Chinese tall KMD 3 G 10 0

Aug 1998 Chinese tall KMD 3 G 4 0

Feb 2000 Chinese tall KMD 3 R 45 0

Mar 2000 Chinese tall KMD 3 R 66 0


98

Table 4.3 continued…Damage assessment records of miscellaneous host records of

banana varieties sampled between 1998 and 2000 in Western Highlands, Central, East



Maturity*No of

samples



Apr 2000 Chinese tall KMD 3 R 13 0

Dec 1997 Gunth M/G 14 0 Apr 2000 Kalapua R 16 0 Dec 1999 Katkatur R 7 0 Jan 1998 Kekiau M/G 12 0 Feb 1998 Kekiau G 6 0 Feb 2000 Kekiau R 38 0 Mar 2000 Kekiau R 57 0 Apr 2000 Kekiau M/G & R 68 0 Dec 1997 KMC 2 R 12 0 Dec 1997 KMC 11 M/G 25 0 Dec 1997 KMC 15 R 12 1 B. frauenfeldi Dec 1997 Maram R 40 0 Jan 1998 Maram M/G & R 19 0 Feb 1998 Maram R 22 0

Jan 1998 Marnaiar KMC 13 M/G & R 49 0

Dec 1997 Pitu KMC 12 G & M/G 32 0 Feb 1998 Poro KMD 7 M/G & R 51 0 Feb 2000 Ramarama R 18 0 Mar 2000 Ramarama R 19 1 B. frauenfeldi Apr 2000 Talauba R 7 7 ? Dec 1997 Touben KMC 9 M/G & R 4 0 Dec 1997 Tukuru M/G 16 0 Feb 1998 Tukuru M/G 12 0 Feb 2000 Tukuru KMC 10 R 11 4 B. frauenfeldi Mar 2000 Tukuru R 50 1 B. frauenfeldi Apr 2000 Tukuru M/G & R 34 0 May 2000 Tukuru R 17 0

Jan 1998 Vabokor (minintina) M/G & R 28 0

Dec 1997 Vudu vok KMC 16 G 47 0

Dec 1997 Vudu vok KMC 16 R 6 0

Dec 1997 Vudu vok KMC 16 M/G 17 0

Dec 1997 Yawa KMD 1 M/G 28 0 Dec 1997 Yawa KMD 1 R 54 0 Jan 1998 Yawa KMD 1 R 29 0 Feb 1998 Yawa KMD 1 R 13 0 Mar 1998 Yawa KMD 1 R 11 0 Table continued overleaf

99

Table 4.4 continued…Damage assessment records of miscellaneous host records of

banana varieties sampled between 1998 and 2000 in Western Highlands, Central, East



Maturity*No of

samples



Feb 2000 Yawa KMD 1 R 38 1 B. frauenfeldi & B. musae

Mar 2000 Yawa KMD 1 R 52 0 Madang Jun 2000 Kalapua R 17 7 B. musae Jun 2000 Cavendish M/G 121 0 Morobe Oct 1998 Kalapua R 12 0 May 1999 Kalapua G 74 1 B. musae Aug 1999 Kalapua R 68 4 B. musae Oct 1999 Kalapua M/G 311 34 B. musae Oct 1999 Kalapua R 33 0 Nov 1999 Kalapua R 22 0 Dec 1999 Kalapua M/G 20 0 Apr 2000 Kalapua R 16 15 B. musae Apr 2000 Kalapua M/G 34 16 B. musae Apr 2000 Kekiau R 22 1 B. musae Dec 1998 Wild banana M/G 287 0 May 1999 Wild banana R 15 1 B. musae Sep 1999 Wild banana R 100 0 Nov 1999 Wild banana R 105 3 B. musae Jan 2000 Wild banana R 101 0 Apr 2000 Wild banana R 291 2 B. musae Sep 1998 Yawa F 13 1 B. musae Jan 1999 Yawa R 61 0 Jan 1999 Yawa M/G 12 0 Jan 1999 Yawa G 10 0 Apr 1999 Yawa R 13 2 B. musae Apr 1999 Yawa M/G 60 7 B. musae Jun 1999 Yawa R 10 0 Jun 1999 Yawa M/G 23 0 Aug 1999 Yawa R 14 2 B. musae Aug 1999 Yawa M/G 13 1 B. musae Nov 1999 Yawa R 37 2 B. musae Nov 1999 Yawa M/G 15 0 Apr 2000 Yawa R 16 0

* Stage of maturity: G – green, MG – mature green, R – ripe, F - fallen

Methodology trial. Data from the trial, when tested for homogeneity of variance using

Levene’s test was found to be non-homogenous, even after standard transformations.

Analysis was thus done using the nonparametric Kruskall-Wallis test. Infestation rates

(and total flies yielded) of Kekiau, Vudu Papua and Tukuru varieties were found,

respectively, to be 25% (606), 20% (495) and 37% (343). The mean yield of flies was

100

not significantly different across varieties (α2 = 2.531, d.f. = 2, p = 0.282). Grouping

data across varieties, infestation rates at three locations on the banana bunch (top,

middle and bottom) indicated apparent higher levels of infestation in the top and

middle part of the bunch. Across all varieties 28% of fruit fly infestation occurred in

the top of the bunch, 33.3% in the middle and 19.4 % in the bottom hands (Figure 4.3).

The high variance in the data, however, resulted in analysis failing to detect any

significant difference in mean fly yield across sampling localities (α2 = 2.433, d.f. = 2,

p = 0.296). Although results conclude that a banana sampled from anywhere within a

banana bunch is equally likely to be infested with banana fly, for the Cavendish survey

I chose to take a conservative approach to sampling and only sampled from hands in

the upper part of the bunch.

Location on bunch

Mea

n (+

SE

) nu

mbe

r of

flie

s

0

2

4

6

8

10

12

14

Top Middle Bottom

Figure 4.2 Mean (± SE) fruit fly infestation in finger samples collected from three

locations on a banana bunch (top, middle, bottom). Finger samples were from

three banana varieties; Kekiau, Vudu Papua, and Tukuru

101

Common garden experiment. A total of 54 bunches (2404 fingers) was harvested

from the garden, but only five bunches (9.3%) had fruit fly infestation (Figure 4.3).

Only varieties Dwarf Kalapua (14%) and Babi (8%) showed infestation, but these were

also the two most sampled varieties and so it cannot be determined if infestation

differences are due to varietal differences or sample size. Infestation was caused not

only by B. musae, but also by the exotic Bactrocera papayae Drew and Hancock

(Asian papaya fruit fly). Seventy-eight B. musae were collected from four infestations,

while 129 B. papayae were collected from five infestations. For fly rearing, banana

hands from bunches were individually set up in containers. At that level, for all

varieties combined (= 248 containers, ~9.7 fingers per hand), infestation rate was

3.2%.

Banana variety

Daru Kurisa Kalapua Babi

Num

ber

of b

unch

es

0

5

10

15

20

25

30

35

UninfestedInfested

Figure 4.3 Bactrocera species infestation of bunches from four banana varieties (Daru,

Kurisa, Kalapua and Babi) grown in a common garden at Laloki, Papua New

Guinea

102

4.3.2 National Cavendish survey

The national survey showed that B. musae infestation levels on Cavendish banana were

generally low throughout PNG. Sample infestation was 15.4% in Central, 8.3% for the

Highlands, 7.4% for Morobe and 10.5% for the Gazelle. While at least some bananas

from all agroecological zones were infested, large areas within each zone yielded no

infested fruit (Table 4.3). For example, in the Highlands, 35 samples were collected but

the only infested samples collected were from the Watabung area in the Eastern

Highlands; between Chuave and Goroka. No flies were reared from samples collected

in Chimbu; from Kerowagi to Chuave, nor from sites between Goroka and Aiyura. In

other regions infestation was similarly patchy.

While sampled bananas were not set up as single fingers (logistics precluded this), it is

none-the-less possible to estimate infestation rate at the individual fruit level. For

example, using the data in Table 4.3 and assuming an average of 30 fingers per sample,

it can be seen that for Morobe 19 flies were reared from approximately 900 fingers, an

infestation level of only 2%. This analysis assumes one fly is emerging per banana, but

in practice, however, multiple flies will generally emerge from an infested banana as B.

musae lays in clutches (see results in preceding section and next chapter). At the level

of the individual finger, therefore, banana fly infestation of Cavendish in PNG is

probably well less than 1% during the period November 2007 to January 2008. It is a

time frame when B. musae seasonal abundance is low.

Identification of adult flies was only done for samples collected in Central Province.

Of the four infested samples from Central sample 1 (from Doa) had 1 B. musae, sample

2 (from Veimauri) has 65 B. musae and 42 B. papayae, sample 3 (from Saroakeina)

had 26 B. musae and two B. papayae, and sample 4 from Sivitatana had nine B. musae.

It is unknown if this level of co-infestation occurs in other regions where B. papayae is

established, but it does clearly show that in future work that the invasive B. papayae

has to be considered equally with B. musae as a PNG banana pest.

103

Table 4.5 Infestation of Cavendish banana samples for 22 localities in Papua New

Guinea. Each sample consisted of about 30 individual fingers collected at

mature green stage of ripeness

Region Locality Number of samples at locality

Number of infested samples at locality

Number of flies reared

Morobe Kaiapit 1 1 4 Nasuapum 5 2 15 Gabensis 5 0 0

Bundun 5 0 0 Bukawa 6 0 0 Bubia 8 0 0

Highlands Watabung 5 2 12 Goroka 5 0 0 Kainantu/Aiyura 5 0 0 Henganofi 5 0 0 Kerowagi 5 0 0 Chuave 5 0 0 Kundiawa 5 0 0

Central Tubusereia 6 0 0 Doa 5 1 1 Vanapa 5 0 0 Veimauri 5 1 107 Kwikila 5 2 37

ENB Kokopo 5 2 72 Rabaul 4 0 0 Keravat 5 0 0 Induna 5 0 0

4.4 Discussion

Levels of infestation caused by B. musae on banana varieties in PNG is seen to be

variable and patchy, but generally low. Infestation rate does not seem to be related to

local abundance of flies. The common garden experiment at Laloki, for example, was

located in the Central province an area where trapping data (Chapter 3) indicated that

B. musae abundance is high, yet only five of 54 bunches were infested, and within

those five bunches there were only nine infested samples, each probably the result of a

single oviposition event. If each infestation was the result of a single oviposition event,

then the infestation rate at the level of the individual banana was only 0.37%. The

9.3% bunch infestation rate, on four varieties in one small location at Laloki, is very

similar to the results from the national Cavendish survey which was carried out across

104

a much more diverse environmental landscape. Such data reinforces the results for B.

musae in Chapter 3, which suggests that banana fly populations are probably not

driven by local site factors, but are present wherever bananas are grown (resulting in a

standard level of fruit infestation). Such data suggests that trying to identify areas of

low pest pressure for commodity production will not be a particularly useful strategy

for B. musae.

The quality of data was consistently low due to sampling problems and consequently

there were no obvious data sets in this chapter to suggest banana varietal differences in

infestation by B. musae. Infestation level did not differ for three varieties on the

Gazelle Peninsula, and while two out of four varieties at Laloki were not infested, this

could simply have been due to the low sampling effort on those varieties. Such

findings are at odds, however, with Smith (1977) and observations of PNG banana

researchers who believe different varieties are differentially attacked (R. Kambuou per.

comm.).

Additional to variation between varieties, are still questions pertaining to general low

host usage. The Cavendish survey was carried out when seasonal abundance of B.

musae in all surveyed locations was low. Low infestation of collected banana hand

samples by B. musae during this time may be an indication of a ‘low pest population

pressure’.

4.5 Thesis progress

Banana fly is very abundant in PNG (Chapter 3), yet infestation was so infrequent in a

comprehensive survey of Cavendish that no formal analysis of data could be done

because of the excess of zero values. This seems very unusual and, from the point of

view of understanding the risk posed by banana fly as a biosecurity threat, needs to be

pursued. In the following chapter I study in detail host use by banana fly on two

commercial banana varieties, Cavendish and Ladyfinger. In the laboratory I look at

both host selection (i.e. oviposition) and utilization (larval survival) on these two

varieties at three stages of ripeness; green, colour-break and ripe. Understanding and

documenting such behaviour is critical for understanding the factors which influence

B. musae infestation rates on banana. This, in turn, is important in assessing the

potential risk involved in the transportation of the commodity and pre-harvest

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management of the fruit fly. Both are essential to the second and third part of the PRA

process; Risk Assessment and Risk Management.

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Chapter 5. Host selection and utilisation by Bactrocera musae (Tryon) on two banana varieties at different ripening stages

5.1 Introduction

Market access for certain crops can be based on non-host status (Follett & Hennessey,

2007) and for fruit flies, non-host or conditional non-host status at a particular stage of

harvest maturity is an internationally recognised phytosanitary measure (FAO, 2005).

While most market access protocols for fruit fly susceptible commodities rely on post-

harvest disinfestation treatments (e.g. heat treatments and irradiation (Jacobi et al.,

1993; Moy & Wong, 2002; Follett, 2004)), more recent research has begun to

investigate the concept of varietal susceptibility, particularly in commercial hosts for

which more than one variety are produced (Follett & Neven, 2006).

Differences in fruit fly infestation levels were found in commercial avocado varieties,

with some varieties more susceptible than others (Hennessey et al., 1995a). Similar

studies have shown that different levels of infestation, and thus susceptibility to fruit

fly attack, also occurs in commercial apple varieties (Bower, 1977), citrus varieties

(Staub et al., 2008), star fruit (Hennessey et al., 1995b), tomato (Balagawi et al., 2005)

and mango (Rattanapun et al., 2009). Subtle differences between varieties of a fruit

may influence fruit fly host utilisation as host selection behaviours are influenced by a

variety of host cues including colour (Dalby-Ball & Meats, 2000b; Brevault & Quilici,

2007), fruit shape and size (Sugayama et al., 1997), smell (Dalby-Ball & Meats,

2000b) and pericarp thickness (Eisemann & Rice, 1989; Balagawi et al., 2005).

Bananas are an international commodity for which several varieties are marketed. The

susceptibility of different varieties to fruit fly infestation is not known. In PNG,

research has indicated Bactrocera musae (Tryon) (banana fly) infestation can be high

on some varieties and low in others (Smith, 1977b). Field observations by local

agricultural officers in PNG also suggest that B. musae infestation, which is most

commonly attributed to the presence of larvae and larval feeding tracks in banana

fingers, is not the same across different cultivars. Smith (1977) suggested plant height

and peel thickness as indicative of the preferential fly behaviour he observed.

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There are direct implications of banana varietal differences for trying to understand the

biosecurity risk posed by B. musae to PNG bananas. The studies on B. musae

infestation on PNG bananas in Chapter 4 indicate that field infestation levels are much

lower than might be expected for such an abundant, unmanaged fly. One reason for

this may be that the “primary” host(s) of B. musae is not the banana varieties I sampled

or, to put it another way, banana fly may simply not “like” Cavendish and the other

varieties I sampled. While it may initially seem odd to say that banana fly doesn’t like

bananas, it needs to be kept in mind that despite the human applied label of “banana

fly”, we actually know almost nothing about host use of B. musae. The fly is

considered largely host specific to Musa species (Drew & Romig, 1996) and will

attack fruit of both cultivated and wild Musa species (Gold et al., 2002), but it is

crucial to note that available host records show Musa banksii is the major host specie

for banana fly, not Musa x paradisiaca cultivars (May, 1953; Rowe, 1981; Simmonds

& Weatherup, 1990; Hancock et al., 2000). Even the assumption that B. musae is

restricted to Musa species is a largely untested assumption, although laboratory studies

on adult oviposition preferences showed that B. musae had a strong preference for its’

“usual” host, i.e. Musa x paradisiaca over other fruits (Fitt, 1986). Whether that

preference is displayed within its native geographic range is largely unknown, although

host surveys in Australia indicate that Musa banksii is the major host for banana fly

(Hancock et al., 2000), while in PNG the fly has been collected from unidentified

Musa sp. in lowland rainforest (Novotny et al., 2005). If the primary host preference of

B. musae is for wild, non-cultivated banana species, then infestation of cultivated

varieties may only occur because they (both the flies and bananas) are so abundant in

the environment. Whatever the reason may be, the unexpected low levels of infestation

in the field prompts the need for a more detailed understanding of host selection and

utilisation by B. musae.

In addition to preferences between banana varieties or species, another factor may well

be important in influencing host choice in banana fly. Across many species of

Bactrocera, ripeness of fruit is a factor which has been shown to influence the number

of visits to fruit (Messina & Jones, 1990), the number of eggs laid and larval survival

(Rull & Prokopy, 2004), and development rates (Souza-Filho et al., 2009). Generally

all of these attributes are more favourable in ripe fruit, versus green or colour-break

fruit maturity stages (Jang & Light, 1991; Rattanapun et al., 2009). As most

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Bactrocera exhibit such preferences, harvesting fruit at mature green stage is an

accepted quarantine management strategy (Armstrong, 1983; Armstrong, 2001).

Banana fly seems to be something of an exception to this general rule, as it has been

reported that the fly will infest green bananas. The literature about this, however, is

contradictory. Vijaysegaran (1996) and Drew et al. (1982) report that banana fly will

attack green fruit, with Drew et al. 1982 specifically stating “they can sting even young

fruit as it appears on the bunch.” Other authors, however, qualify this position,

recording that while B. musae is able to oviposit into both immature and mature

bananas, eggs in immature fruit will not develop unless fruit ripens very soon after

oviposition (Smith, 1977b; Fitt, 1986; Gold et al., 2002). Smith (1977), for example,

reports that gravid females were able to oviposit into green bananas at the ‘full’ stage,

but only if the bananas began to colour within the following three days. The

description of ‘full’ that Smith uses may resemble a maturity stage close to what

current industry colour charts (Dadzie & Orchard, 1997; Banana Colour chart,

websites) refer to as the colour-break stage (in particular “Stage 2”)2. This is not the

green and hard maturity stage when bunches are harvested for international trade,

referred to as ‘three quarters full’ (Dadzie & Orchard, 1997). The studies of Smith, and

also May (1953), are applied in commercial banana production in Australia with the

harvesting of green banana bunches an accepted practise for banana fly management

(Fooks, 1989; Pinese & Piper, 1994; Fooks, 2002; Gold et al., 2002). Given this

conflict in the literature, and its impact on biosecurity/pest management practice, a

definitive study on B. musae host use at different ripeness stages is required.

Given the above discussions concerning banana fly host use, both across banana

varieties and within a variety across ripening stages, in this chapter I study both the

impact of variety and maturity stage on B. musae host use. Specifically, in choice and

no-choice arenas I study adult host selection and larval host utilisation of B. musae for

two banana varieties, Cavendish and Ladyfinger, at three ripening stages, green,

colour-break and ripe. I also carry out a trial, following internationally accepted

2 See also standard banana colour chart websites:

http://www.globalfruit.ie/index.php?option=com_content&task=view&id=14&Itemid=21, http://www.catalyticgenerators.com/service.html, http://lib.store.yahoo.net/lib/catalyticgenerators/bananacc.pdf, http://www.bananaland.com.au/info/facts/banana_details_ripening_stages.php.

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protocols, to confirm the status (either positively or negatively) of green Cavendish as

a host of B. musae.

5.2 Materials and Methods

There were three areas investigated in this study. The first was adult oviposition choice

and subsequent offspring emergence. Tests were done to investigate host selection

behaviour by female flies given choice or no-choice between different banana varieties

and ripeness stages. The second area was on larval host utilisation. The impact of

different banana hosts on juvenile development was calculated by inoculating fertile

eggs under the peel of two banana varieties at three ripeness stages. The third area

looked at was banana fly use of green banana, using standard international protocols.

The test was setup using the specified requirements for testing the host status of a fruit

or vegetable variety at a defined stage of maturity to a given fruit fly species (FAO,

2005).

Experiments were carried out in a controlled environment room (RH 70%, 26°C) at the

Queensland Primary Industries and Fisheries laboratories in Cairns, Queensland. The

banana varieties used were organically produced Cavendish (Williams) and

Ladyfinger, obtained from commercial growers in Tully and Mareeba. Three maturity

stages of banana were used, green, colour break and ripe, and these were identified

using an industry standard maturity colour chart (Dadzie & Orchard, 1997; QDPI,

2004). The B. musae colonies used were 3rd-4th generation flies from locally collected

wild populations (sourced from infested Musa x paradisiaca banana varieties). Flies

were cultured on protein, water and sugar, with oviposition into banana and artificial

egging domes, and larvae reared on fruit fly carrot medium. Flies used in the

experiments were mature, mated 20-25 day old female flies. Most flies were subjected

to a single exposure to artificial and banana egging domes prior to exposure to the test

fruit to encourage oviposition. All observation trials were carried out in 30 x 30 x 30

cm observation cages and flies had access to sugar and water during observation

periods.

5.2.1 Adult host choice and utilisation

Choice tests. Three choice experiments were done. Experiment 1 observed oviposition

choice by a single female fly in a cage when provided with a single ripe finger of

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Cavendish and Ladyfinger. Experiment 2 observed oviposition choice by a female fly

in a cage with a green, colour-break and ripe finger of Cavendish. Experiment 3

observed the same but of green, colour-break and ripe Ladyfinger. All experiments

were observed at 3 min intervals from 1000-1400 hrs (i.e. an observation was done at

1000am, the next at 1003am, the next at 1006am, etc). There were 16 replicates for all

experiments and fingers were individually incubated for subsequent adult fly

emergence (i.e. 128 containers were used to incubate the samples). Incubation period

was a minimum of two weeks and numbers of emergent adults, plus the number of

observed oviposition events, were the measures of host use analysed.

No-choice tests. In the no-choice tests, a single finger of each ripeness stage of each

variety was placed in a separate cage and left exposed to a female fly for one day

between 10.00am and 3.00pm. There were 16 replicates for each ripeness stage of each

variety. Samples were then individually incubated and adult emergence was recorded

after a minimum incubation period of two weeks. Oviposition was not recorded.

5.2.2 Larval host utilisation

Fertile eggs were collected from B. musae cultures and then artificially inserted into

each variety and ripeness stage tested (as above). Methodology used to collect the eggs

is as described in Balagawi et al. (2005). To insert the eggs under the peel, a 1 cm slit

was made about 3 cm from the flowering end of the banana finger and then pulled back

gently to deposit 60 eggs before resealing the wound with parafilm. Sixteen replicates

were done for each variety and ripeness stage. Fingers were then incubated

individually as for the preceding trials and the number of adult flies emerging from

each recorded.

5.2.3 Host use of green banana

This trial tested the status of green Cavendish fruit as a host of B. musae using

internationally accepted host status tests (FAO, 2005). The protocol prescribed 500gms

of fruit (the nearest whole fruit load was four green banana fingers, slightly more than

500gms) was placed inside a 30 x 30 x 30 cm cage for a period of 24 hours. During

that time the fruit were exposed to 25 mature, female B. musae flies randomly selected

from a culture colony. After 24 hours fingers were removed and individually

incubated. Adult emergence was recorded after two weeks. The trial was replicated

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five times, with an additional single replicate using ripe Cavendish (a formally

recognised known host) to act as a control (to ensure flies used were gravid and

fertile).

5.2.4 Host plant attributes

Measurements were taken of banana peel toughness, peel thickness, pulp thickness,

peel colour, and sugar content in pulp of Cavendish and Ladyfinger in ripe, colour-

break and mature-green ripeness stages. Procedures for the measurement of each

biological feature were obtained from procedures used in an INIBAP technical

guideline (Dadzie & Orchard, 1997). A Chatillon digital force gauge LTCM-6 and a

hand-held penetrometer using a 0.5mm needle were used to measure peel toughness. A

digital vernier calliper was used to measure peel and pulp thickness. Sugar content,

measured in Brix (%), was recorded using methodology described in the INIBAP

technical guideline (Dadzie & Orchard, 1997) using a hand-held Brix Refractometer

(model: MT-032ATC, measuring range: 0-32% Brix, accuracy: ± 0.2%). The sugar

content is described by a rank for which, in banana, a reading of 8-10 is poor, 10-12 is

average, 12-14 good and 16 excellent3. A Minolta CR-300 colour meter was used to

measure peel colour. Peel colour was measured using the CIE LCH(uv) chromatic

colour system: L stands for luminance (lightness) and is measured vertically from 0

(black) to 10 (white); C stands for chroma (colour purity or colourfulness) and is

measured radially outward from the neutral (gray) vertical axis; and measures the

lightness and “purity” or strength of a colour; lower chroma being less pure, more

washed out, as in pastels); and H is for hue and is measured in degrees around

horizontal circles and measures which colour is most complemented (Wright, 1984).

5.2.5 Analysis

Choice and no-choice trials were initially designed to be analysed using one-way and

two-way ANOVA. Large numbers of zeros, however, and non-homogeneously

distributed errors, which could not be made homogeneous following transformation,

meant that parametric data analysis was not possible. Rather, non-parametric analysis

was carried out to determine if there were significant differences in observed

3 http://crossroads.ws/brix/index-page6.html http://www.honeycreek.us/brix.php.

112

oviposition behaviour and adult emergence numbers between varieties and ripeness

stage. Depending on the test the analyses included the Kruskall-Wallis or the Mann-

Whitney U-test, with the Games-Howell test used as a post-hoc for the Kruskall-

Wallis. Where there were simply too many zeros to allow analysis, data is presented

visually (i.e. it is summarised and graphed). Differences between banana varieties in

individual plant attributes were analysed using one and two-way analysis of variance

tests.

5.3 Results

5.3.1 Adult host choice and utilization

Direct observation of oviposition behaviour under laboratory conditions showed very

few flies attempted to oviposit in either Cavendish or Ladyfinger. Observations

showed that flies did move between fingers within a cage and so were able to make a

choice, but oviposition was still rare. Of the few oviposition events made, not all

attempts (if eggs were laid) were successful in maturing into adult flies. In a choice

arena between ripe fingers of Cavendish and Ladyfinger, no oviposition was made into

Cavendish and only a very small number into Ladyfinger (Figure 5.1). When flies were

given a choice across three ripeness stages within a single variety, overall oviposition

was higher on Cavendish than Ladyfinger, and flies emerged from all ripeness stages

of Cavendish (Figure 5.2). For both these trials the large number of zero values made

statistical analysis inappropriate.

5.3.2 Adult no choice

In the adult no-choice experiment, the Kruskall-Wallis test detected no effect of banana

variety on adult emergence (2 = 0.867, df =1, P=0.360). There was, however, an

effect of fruit ripeness stage (2 = 9.811, df =2, P=0.007), with the post hoc Games-

Howell test detecting that significantly fewer flies were bred from colour-break fruit

than from ripe fruit. Green fruit was intermediate between the other two and not

significantly different from either (Figure 5.3).

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Banana variety

Num

ber

of o

vipo

sitio

n e

vent

s or

flie

s

0

1

2

3

4

5

Number of oviposition eventsNumber of emergent flies

Cavendish Ladyfinger

Figure 5.1 Number of oviposition events and subsequent number of emergent flies

from single ripe fingers of two banana varieties when offered in a choice arena

to single female Bactrocera musae (n=16 for each variety)

Banana variety and ripeness stage

Num

ber

of o

vipo

stio

n ev

ents

or

flies

0

5

10

15

20

25

GreenGreen Colour-break Colour-break RipeRipe


114

Figure 5.2 Number of oviposition events (darker shade) and subsequent number of

emergent flies (lighter shade) from single fingers of Cavendish and Ladyfinger

banana varieties at three stages of ripeness when offered in a choice arena to

single female Bactrocera musae (n=16 per variety/ ripeness combination)

Ripeness stage

Num

ber

of f

lies

0

10

20

30

40

50

CavendishLadyfinger

Green Colour break Ripe

Figure 5.3 Number of emergent flies from single fingers of two banana varieties at

three stages of ripeness when offered in a no-choice arena to single female

Bactrocera musae (n=16 banana fingers per variety/ ripeness combination)

5.3.3 Larval host utilization

Non-homogenous errors meant that data from the egg inoculation trials also had to be

analysed using nonparametric techniques. Combining data across varieties, when eggs

were inoculated into fruit of three ripeness stages, adult emergence from ripe and

colour-break fruit was significantly better than from green fruit (Kruskall-Wallis test,

2 = 13.048, df =2, P<0.001, Games-Howell post hoc test). Combining data across

ripening stages, mean adult emergence was greater from Ladyfinger than from

Cavendish (Mann-Whitney U = 677.00, Z = -3.985, P<0.001) (Figure 5.4).

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Banana variety

Num

ber

of f

lies

0

2

4

6

8

Stage of ripeness

Num

ber

of f

lies

0

2

4

6

8

Green Colour break Ripe


A

B

A

BB

Figure 5.4 Mean (± SE) number of flies reared from individual fingers of two banana

varieties at three ripeness stages when inoculated with 20 Bactrocera musae

eggs (n=16 inoculated banana fingers per variety/ ripeness combination, 60

eggs per banana)

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Ripeness stage

Nu

mbe

r of

flie

s

0

20

40

60

80

100

Green Ripe

Figure 5.5 Mean (± SE) number of Bactrocera musae emerging from green Cavendish

bananas following the exposure of 500gm of banana to 25 gravid female flies

(n = 5 replicates). Emergence of flies from ripe fruit (n = 1 replicate) is a

positive control, demonstrating that the flies used to run the trial were gravid.

It should not be used to compare yield of flies from green versus ripe fruit

5.3.4 Host use of green bananas – green Cavendish as a host of Bactrocera musae

Following international protocols for assessing fruit fly host status, green Cavendish

should be considered a host of B. musae as flies were reared from it (Figure 5.5).

5.3.5 Host plant attributes

Six attributes of Cavendish and Ladyfinger banana fingers were measured at mature-

green, colour-break and ripe stages: peel toughness, peel thickness, pulp thickness, peel

colour, and pulp sugar content. The analysis of the importance of variety, ripeness

stage and the Variety x Ripeness interaction for each attribute is presented in Table 5.1

and presented graphically in Figure 5.6.

Peel toughness varied significantly between varieties (greater in Ladyfinger) and

ripening stages (softer in ripe banana). There was a significant interaction effect

between variety and ripening stage, most likely due to a very large drop in peel

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toughness between colour-break and ripe stage in Ladyfinger, an effect which was

present, but less marked, in Cavendish. Fruit pulp thickness does vary between

varieties or across ripeness stages. Peel thickness does not vary significantly but

changes across ripening stage, generally decreasing as fruit matures. The decline in

peel thickness in ripe fruit was more marked in Ladyfinger than Cavendish. Cavendish

is a heavier fruit than Ladyfinger, the weight of which does not change across ripening

stage. The weight of Ladyfinger, however, declined slightly as fruit ripened. Cavendish

was a sweeter variety overall than Ladyfinger, but what was most dramatic was the

change in Brix across ripening stage. Mature green and colour-break bananas of both

varieties had similar, low Brix percentages, but Brix increased dramatically when the

fruit ripened. Colour measurements (Hue, Chroma and Luminescence) clearly indicate

that each ripeness stage has a distinct colour (Figure 5.6).

Table 5.1 Summary two-way ANOVA output table for Cavendish and Ladyfinger fruit

attributes at three ripening stages

Attribute Source df F P value Peel toughness Variety 1 46.57 <0.00 Ripeness 2 353.71 <0.00 Variety x ripeness 2 160.39 <0.00 Pulp thickness Variety 1 0.96 0.331 Ripeness 2 1.06 0.350 Variety x ripeness 2 3.74 0.228 Peel thickness Variety 1 1.36 0.247 Ripeness 2 131.94 <0.00 Variety x ripeness 2 18.90 <0.00 Chroma Variety 1 12.56 0.001 Ripeness 2 307.98 <0.00 Variety x ripeness 2 79.11 <0.00 Luminance Variety 1 35.02 <0.00 Ripeness 2 426.31 <0.00 Variety x ripeness 2 3.37 0.039 Hue Variety 1 0.13 0.724 Ripeness 2 200.48 <0.00 Variety x ripeness 2 2.44 0.093 Weight Variety 1 204.33 <0.00 Ripeness 2 0.94 0.394 Variety x ripeness 2 5.91 0.004 Table continued overleaf

118

Table 5.2 continued…Summary two-way ANOVA output table for Cavendish and

Ladyfinger fruit attributes at three ripening stages

Attribute Source df F P value Brix (%) Variety 1 26.78 <0.00 Ripeness 2 1785.52 <0.00 Variety x ripeness 2 9.99 <0.00

Gra

ms

0

200

400

600

800

Green C-B Ripe Green C-B Ripe Cavendish Lady-finger

mm

26

27

28

29

30

31


Chr

oma

(C)

x

0

10

20

30

40

50

60

70


mm

2.0

2.5

3.0

3.5

4.0

4.5


Hue

h (

y)

80

90

100

110

120


Lum

inan

ce L

(Y

)

40

50

60

70

80


Peel toughness Pulp thickness

Peel thickness Chroma

Luminance Hue

aa

b

a a

b

aa

b

a

a

b

a

b

c

a

b

c

a

b

c

a

b

ca

b

c

a

b

c

119

Figure 5.6 Mean (± SE) fruit attributes for two banana varieties at three stages of

ripeness. Letters above columns denote significant difference in the fruit

attribute between ripeness stages within the one banana variety (based on 1-

way ANOVA with a Tukey’s post-hoc test at p < 0.05)

Gra

ms

0

50

100

150

200

250

Per

cent

age

0

5

10

15

20



Brix Weight

ab

c

a a

b

aab b

Figure 5.6 continued Mean (± SE) fruit attributes for two banana varieties at three

stages of ripeness. Letters above columns denote significant difference in the

fruit attribute between ripeness stages within the one banana variety (based on

1-way ANOVA with a Tukey’s post-hoc test at p < 0.05)

5.4 Discussion

In the experimental arenas, few female B. musae visited banana fingers regardless of

the variety offered or the ripeness stage. This lack of interest exhibited by gravid B.

musae females toward banana fingers suggests a very low attractiveness to these

banana varieties. Further, when eggs were inoculated into fruit, larval development did

occur through to the adult stage, but mortality rates were high (~90%+). The survival

rates observed across the immature stages (i.e. eggs, larvae and pupae) are low in both

banana varieties, across all ripeness stages. Immature development occurs in the pulp

and so the reasons why mortality is high is most probably due to unfavourable or

limiting conditions in the pulp.

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Different experiments gave inconsistent patterns with respect to the preferred banana

variety. Of the two varieties studies, adult choice oviposition trials suggest that

Cavendish was the more preferred host, but this pattern is not repeated in the no-choice

trials, while the inoculation trial suggests Ladyfinger is a better host. The simple

interpretation of this data is that under no-choice conditions the flies will lay into any

banana, when given a choice between varieties they show varietal preference for

Cavendish, but once eggs are in fruit larvae do best in Ladyfinger. A preferential

selection by fruit flies between fruit varieties in a choice arena, but which is then lost in

a no-choice arena, is known for fruit flies (Ero, 2009; Rattanapun et al., 2009) and may

be happening with banana fly. However, the generally low oviposition rates and poor

offspring survival makes any definitive interpretation of the data difficult. However,

further studies are needed to provide definite evidence to confirm this. One piece of

hard evidence which cannot be argued against, however, is that in both individual fly

arenas, and following international protocols, green Cavendish fingers harvested at

maturity are stung by B. musae and deposited eggs can develop through to adult flies.

The low oviposition rates and poor larval development rates observed in this chapter

on Cavendish appear to reflect the very low field infestation results obtained in the

PNG Cavendish survey (Chapter 4). This poses the question: Is Cavendish an

unattractive variety to B. musae? If so then this may explain the low damage

assessment levels found during the PNG Cavendish survey. Infestation was also low in

other varieties studied in Chapter 4, as it was in Ladyfinger in this chapter. Such

consistent results, from both the field and lab, suggest that very low levels of host

utilisation is the ‘normal’ behaviour exhibited by banana fly toward Musa x

paradisiaca varieties, i.e. M. x paradisiaca varieties are not major hosts for B. musae.

Infestation, where it does occur, may be because these varieties are simply so abundant

in the PNG environment that even very low levels of host use, infestation will still be

picked up.

Fruit attributes and characteristics are known to influence host selection and utilisation.

For Cavendish and Ladyfinger, fruit attributes of both show similar peel characteristics

which may explain the similar responsiveness or attractiveness received from B.

musae. Varietal characteristics are different in peel toughness, weight and Brix

measure but these differences are much greater between the three ripeness stages.

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Mature-green and colour break characteristics are more similar to each other in

comparison to the peel attributes of ripe fruit.

For potential export banana production in PNG, there is a large number of cultivated

banana varieties which might be considered. For each of these economically important

varieties, susceptibility to B. musae will be necessary in helping determine those

selected for commercial production. Even at low levels of infestation, commercial

production will still require management protocols and strategies that ensure harvested

bunches are not exposed to B. musae infestation. Nevertheless, evidence accumulating

in this thesis suggests that M. x paradisiaca varieties are not inherently highly

susceptible to banana fly, which will help make other control strategies more effective.

Harvesting bananas at mature green, however, is unlikely to be utilised as a lone

control method, because female flies are able to oviposit into mature green bananas,

but one used with two or more methods in risk reduction strategies.

5.5 Thesis progress Population distribution and abundance of B. musae is related to the availability of its

host (Chapter 3). While B. musae is documented to be attracted to Musa species, within

this genus studies on host selection and utilisation now indicate that female flies are

likely to be selective with respect to species and variety. Such behaviour may explain

the low infestation levels obtained on cultivated Musa x paradisiaca cultivars studied

in this thesis thus far. In the following chapter (Chapter 6), while host selection is not

the chapter’s aim, I do provide further information on how host utilisation impacts on

the fly’s pest status. Chapter 6 studies the impact of B. musae on banana in the field

from an invasive biology perspective. In PNG, the Gazelle Peninsula of East New

Britain province is a novel environment where B. musae is a recently introduced exotic

fruit fly species, and it is in this area that the fly’s distribution, population abundance,

phenology and impact on banana are studied.

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Chapter 6. Bactrocera musae (Tryon) in a novel environment: banana fly as an invasive organism on the Gazelle Peninsula, Papua New Guinea

Note concerning chapter contents Approximately half of this chapter reports work accomplished and published (by me) prior to my PhD candidacy. I acknowledge that this component of the chapter does not meet the requirements of a PhD, in that the work was not done whilst I was an enrolled student. The chapter, including the previously published material, is still included here, however, because it presents a case-study about an invasive potential of B. musae in a non-endemic environment. The chapter ties the thesis together by providing an example which pulls together the independent studies presented in earlier chapters. The published components of this chapter are presented as Appendix 3 and should not be considered as part of the “original contribution” of this thesis.

6.1 Introduction

Perhaps the single most important aspect of a Pest Risk Analysis (PRA) is predicting

the consequences of how a pest organism will behave in a novel environment and the

impact that it will have on local crops (IPPC, 2006a). While an organism may be

transported along a commodity pathway, simply knowing that transport may occur is

not, of itself, sufficient to then regard that organism as being of biosecurity concern.

Rather, the organism has to have the capacity to establish in the novel environment,

reproduce and spread, and then negatively impact on crops or the environment in that

new range (Vermeij, 1996; Kolar & Lodge, 2001; Maynard et al., 2004; Lockwood et

al., 2005). Knowing the likelihood of these factors allows managers to setup effective

control strategies (Carey, 1996; Simberloff, 2003a; Simberloff, 2003b; Maynard et al.,

2004; Clarke et al., 2005).

Establishment probability is dependent on whether or not ecological factors in the

novel area are suitable. Often invasive organisms are not able to reproduce successfully

and do not establish. However, if they are able to establish the impact they may have

on the novel environment becomes of concern. Much has been documented on the

continuous negative effect that invasive incursions can have on the social, economical

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and natural environment they invade (Levine, 2008). With respect to tephritids, the

effect that invasive fruit flies have had on the social and economic livelihood of

affected agricultural communities is commonly negative and with management costly

(Drew, 1996; Headrick & Goeden, 1996; Maynard et al., 2004).

Prevention or very rapid management of incursions is the primary aim of biosecurity

organisations around the world, because management of the invasive at the earliest

opportunity is the most efficient and cost effective solution (Perrings et al., 2002;

McAusland & Costello, 2004; Perrings, 2005). As part of this, studies on the behaviour

and impact of invasives in novel environments are useful (Andersen et al., 2004).

Finding out the likely chance of establishment and spread, phenology in the new

environment and the impact that an invasive may have on local production of a

susceptible commodity are all important elements for study. This chapter looks at just

such an example, where a non-endemic fruit fly species has been detected in a novel

environment and has subsequently been tracked post-establishment. Relevant to this

thesis is that the invasive organism is Bactrocera musae (Tryon) (banana fly) and the

invaded region is a locality where banana plays a significant social and economic role,

the Gazelle Peninsula, East New Britain Province (ENB), Papua New Guinea (PNG).

Bactrocera musae was traditionally considered as being absent from the Gazelle and

other PNG island provinces (Drew 1989). It was, however, detected on the Gazelle in

mid-2000 (author’s data). The pathway for entry was not confirmed, but may have

been linked to either food relief supplied after the 1994 Rabaul volcano explosion, or

simply through carriage of infested bananas by travellers (Putulan et al., 2004). I was

the locally based fruit fly entomologist on the Gazelle at that time and subsequently

carried out research on the fly up until the time I commenced my PhD studies. All data

presented in this chapter was gathered before my studies commenced but, with one

exception, had not been analysed. The exception is work on the establishment and

spread of banana fly on the Gazelle which was published prior to commencing studies

(Mararuai et al., 2001) (Appendix 3). Sections from that paper are included in this

chapter because of the insights they provide on B. musae as a biosecurity threat.

The presence of B. musae in a novel environment, such as the Gazelle, provides an

ideal opportunity to provide data on various aspects of its potential invasion biology,

including spread potential and likely impacts. The Gazelle Peninsula is an area where

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banana, the major and [presumed] preferred host of B. musae, is widely cultivated in

semi-plantation stands; an ideal setting to study the fly from an invasive species point

of view. The impact that this fruit fly species may have on banana in the Gazelle is

unknown, but a priori would be considered serious given the fly’s perceived pest status

on the crop.

In this chapter I collate information which has been gathered on banana fly in the new

environment of the Gazelle. The peninsular has a wet-tropical, lowland environment

similar to most northern coastal areas of mainland PNG (where banana fly is endemic).

Environmental and cropping information for the Gazelle is provided as part of the

analyses carried out in Chapter 3 (Distribution and abundance of five economically

important fruit fly species in Papua New Guinea). Since 2000, B. musae has moved

from being a newly arrived and still spreading incursive on the Gazelle, to being an

established part of the local environment. Information I have collated for this chapter

covers the fly’s distribution and spread, population abundance and phenology of the

established population, and then host infestation levels. All such information is a

crucial and necessary requirement in carrying out a PRA for PNG bananas.

6.2 Materials and Methods

6.2.1 Distribution and spread of Bactrocera musae (Tryon) on the Gazelle Peninsula

Two sets of delimiting surveys were carried out soon after banana fly was detected (i.e.

in 2000) to determine the distribution and population levels of banana fly. These

surveys were: (i) an initial set of three “snapshot” surveys (i.e. very short term) in the

Rabaul and Kokopo areas to identify and confirm incursion; and (ii) a second,

intensive delimiting survey six months later. All trapping was done with modified

Steiner traps (Drew et al. 1982) baited with a mixture of male fruit fly attractant

methyl-eugenol and the insecticide malathion. Trapped flies were sorted to species

level, identified at NARI’s Lowlands Agricultural Experiment Station, Keravat, and

then sent for confirmation of identity to Prof. R.A.I. Drew, Griffith University,

Brisbane. Additional material was screened in the genetics laboratory of Prof J.

Hughes, Griffith University, and confirmed to be genetically similar to known material

of B. musae from North Queensland.

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The initial set of surveys was carried out between late 1999 and mid 2000 to confirm

the incursion of B. musae. They covered areas from the coast to the hinterland of the

Gazelle Peninsula (Figure 6.1). Survey one ran from November to December 1999,

covering the Kokopo town area, and had 23 trap locations setup in both residential and

commercial areas. Survey two ran from May to June 2000 along the northern coastline

of the peninsular from Rabaul to Tavilo. Traps were set at 11 locations in village

residential areas and vegetable gardens. Survey three ran from June to July 2000, and

covered the mountain plateau areas of Malmaluan, Nangananga and Raluan about 5km

inland from the coastline between Rabaul and Kokopo towns. Traps were established

at 13 trap locations covering village residential areas with many areas under vegetable

cultivation.

The delimiting survey was an intensive survey of the Gazelle Peninsula which was run

in December 2000. The aim of the survey was to determine, as far as possible, the

distribution of banana fly at that time. Sixty-one traps were distributed covering the

major road networks on the peninsular at approximately 10km intervals. The trap

network extended along the northern coastline from Tavui to Lassul (04°13’S,

151°43’E), along the southern coastline from Kokopo to Gar in the Sum Sum Bay

(04°42’S, 151°21’E) and further inland from Kokopo toward Warangoi (04°29’S,

152°09’E) and as far as Riet (04°34’S, 152°05’E) at the base of the Baining Mountains

(Figure 6.1).

In addition to presenting the data from these two surveys, I also present the current

known distribution of banana fly on the Gazelle. This information is not based on a

single formal trapping program, but is a collation of information from different sources

including growers, research colleagues and personal observations made during survey,

experimental and farmer out-reach work.

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Figure 6.1 The Gazelle Peninsula, East New Britain Province, Papua New Guinea.

The three highlighted localities are where impact trials were carried out

6.2.2 Population abundance and phenology

Two trapping datasets were used to study the abundance and phenology of B. musae.

The first set, used here for comparative purposes, is the phenology data for B. musae in

its endemic areas on the PNG mainland, as presented in Chapter 3. The Gazelle

abundance data was collected from a trapping programme run concurrently with a

bagging trial (details described in the next section, 6.2.3) in early 2002. There were

three traps and all were located in areas where B. musae was first detected, the sub-

coastal strip between Rabaul and Kokopo. Traps were located in village residential

areas surrounded by vegetable gardens and plantation stands of cocoa, coconut and

vanilla. Trap sampling occurred from April 2002 to July 2003 and traps were emptied

weekly.

Tavui

Karavia

Malapau

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6.2.3 Impact Studies

Market Surveys (2000-2001)

To measure the level of infestation being caused by the banana fly incursion at the time

of the initial incursion, bananas were purchased from local roadside markets and

collected from the Lowlands Agricultural Experiment Station banana plots and from

gardens in the Rabaul and Kokopo areas. Fruit were set in individual containers and

kept to assess the level of fruit fly infestation as described in Leblanc et al. (2001)

(Appendix 3). Rearing occurred at intervals over a twelve-month period from June

2000 onwards. All reared flies were identified by R.A.I. Drew.

Bagging trial (2001-2003)

Host infestation levels were assessed from a banana field control trial carried out

between March 2001 and July 2003. The trial established three banana plots in separate

locations, but all in areas with high B. musae abundance. The trial was a collaborative

effort with local farmers aimed at demonstrating the procedure and benefits of bagging

against fruit fly infestation. Plots were established at Tavui, Karavia and Malapau

(Figure 6.1). The banana variety chosen for study, Tukuru (PNG118 Musa Eumusa

ABB) (Arnaud & Horry, 1997), is a commonly consumed and marketed variety on the

Gazelle and one of important cultural value.

At each plot, 20 banana bunches were bagged (i.e. physically protected from banana

fly) and 20 were not bagged (i.e. exposed to banana fly). The type of bags used were

polythene bags used in the packaging of fresh or dried cocoa beans, a widely available

and non-costly option for subsistence and semi-commercial farmers. All bagged

bunches were bagged at the mature green stage, about six weeks after the appearance

of the inflorescence bulb. Bagged and un-bagged bunches were then harvested at

maturity and banana samples were setup over moist sawdust. Incubation period was a

minimum of two weeks during which pupae and adult emergence were observed and

recorded.

Current damage

To get an estimate of current levels of damage this chapter uses information from the

Cavendish survey (Chapter 4: Infestation of bananas by Bactrocera musae (Tryon) in

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Papua New Guinea). It also presents some informal information gathered from

colleagues.

6.3 Results

6.3.1 Distribution and spread of Bactrocera musae (Tryon) on the Gazelle Peninsula

On the Gazelle, B. musae was first collected from sites just behind Kokopo (e.g. 40

flies from 15 clearances of a trap hanging at the Vunamami Farmer Training Centre

(04°21’S, 152°13’E)). At the same time isolated individuals were trapped at more

distant localities, such as Keravat, and these probably represented dispersing flies. The

absence of flies in surveys prior to its detection (Leblanc et al., 2001) and the lack of

local cultural control methods against fruit fly infestation on banana supported the

conclusion that B. musae is an invasive on the Gazelle Peninsula.

Snapshot surveys confirmed the presence of B. musae on the Gazelle. The flies

distribution when first surveyed in mid-2000 showed the population to be radiating

from Rabaul and Kokopo (Figure 6.2). The initial distribution was limited to areas

along the coastline with high abundance areas in and around Rabaul and Kokopo. By

late 2000 the distribution had spread further inland and along coastal areas (Figure

6.3). Traps were able to catch few flies in areas further along the northern coastline

toward Lassul and along the eastern coastline toward Gar. Toward the hinterland,

samples were collected in areas such as Warangoi and Reit. To my knowledge the

current distribution of banana fly on the Gazelle covers all parts of the Gazelle up to

the Baining Mountains (Figure 6.4).

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Figure 6.2 Distribution of Bactrocera musae (Tryon) on the Gazelle Peninsula, East

New Britain, Papua New Guinea in mid 2000. Source: Mararuai et al. (2001)

Figure 6.3 Distribution of Bactrocera musae (Tryon) on the Gazelle Peninsula in

December 2000. Source: Mararuai et al. (2001)

0 flies

Keravat

RABAUL Lungalunga

Tavui No. 2

KOKOPO

Karavia No. 2

Toma

Gazelle Peninsula 11-50 flies

1-10 flies

>50 flies

Tokua

0km 20km

0 flies

1-10 flies

11-50 flies

>50 flies

Toma

Lungalunga

Riet

Vunamarita

Keravat Kokopo

Watwat

Gar

Gazelle Peninsula

0km 20km

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Figure 6.4 Distribution of Bactrocera musae (Tryon) indicated by red pins on the

Gazelle Peninsula in June 2009; pins mark village residential areas surrounded

by vegetables gardens, plantations, secondary or primary rainforest

6.3.2 Population abundance and phenology

On the Gazelle, B. musae populations fell in January and remained low until July,

when the population began to rise, with a nearly continual increase through to

December (Figure 6.5). This trend is somewhat similar to that shown by banana fly in

the Highlands between January and July. However between August and December

seasonal abundance remains high while the curves in Morobe and the Highlands fall

distinctly. Analysis in Chapter 3 suggests that weather variables do not have a major

influence on the population dynamics of B. musae and so cultivation practices for

banana may be responsible for the differences observed. If this is the case for the

mainland sites, it may also be the case for the Gazelle. The mean monthly abundance

levels of B. musae on the Gazelle between April 2002 and July 2003 were quite large

and similar to levels in areas on the PNG mainland.

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0

200

400

600

800

1000

1200

1400

1600

1800

Jan

Feb

Mar

Apr

May Ju

n

Jul

Aug Sep Oct

Nov

Dec

Time (Months)

Ave

rag

e m

on

thly

tra

p c

atc

h

Highlands

Morobe

Central

Gazelle

Figure 6.5 Phenology curve of Bactrocera musae (Tryon) on the Gazelle Peninsula

(East New Britain, Papua New Guinea (PNG)) (from April 2002 to July 2003)

compared with curves in three areas on the PNG mainland (from 1999 to 2001)

6.3.3 Impact studies

6.3.3.1 Fruit rearing (2000-2001)

From fruit collected from 28 roadside markets along the north and south coasts of the

Gazelle, 6% infestation was recorded, caused equally by B. musae and Bactrocera

frauenfeldi (Schiner). Fruit collected from 18 field locations in May and June 2001

yielded fewer flies, with less than 1% infestation rate (Table 6.1). However, comments

from village farmers during this collection were pertinent; for example “Bananas have

to be harvested earlier than usual to prevent them getting damaged”. When infested

fruit was collected, infestation of individual fingers was found to be heavy. One sample

of seven ripe fingers, weighing 1.76 kg and collected from Tavui No 3 village (behind

Rabaul town) on 12 April 2000, yielded 418 B. musae pupae.

6.3.3.2 Bagging trial (2001-2002)

The infestation impact of B. musae on bagged and un-bagged Tukuru was almost the

same. There were 12 bagged and 12 un-bagged samples collected from each plot at

Tavui, Karavia, and Malapau (i.e. a total of 36 bagged and 36 un-bagged bunches).

Only one un-bagged bunch harvested from Malapau was infested (Figure 6.6). These

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infestation levels are despite the presence of a large wild population in the

environment.

Table 6.1 Tephritid fruit flies reared from bananas purchased from markets (March to

June 2000) or collected from gardens (May to June 2001) on the Gazelle

Peninsula, East New Britain, Papua New Guinea

Figure 6.6 Infestation of banana bunches protected (bagged) or unprotected

(unbagged) from Bactrocera musae (Tryon) on the Gazelle Peninsula, East

New Britain, Papua New Guinea

Market Surveys Garden Surveys Number of banana varieties sampled 15 11 Number of markets/gardens visited 28 18 Fruit fly species collected Bactrocera frauenfeldi

Bactrocera musae Bactrocera frauenfeldi

Bactrocera musae % infestation by both fruit fly species 6% 0.8% % infestation by Bactrocera musae 3% 0.2% Most common varieties sampled Yawa Kiakiau, Yawa,

Tukuru, Katkatur, Chinese Tall

Total weight of banana sampled 19.6 kg 36.8 kg Number of banana fingers set up Not recorded 393 Average development stage of bananas sampled mature green mature green

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6.3.3.3 Current status

The current levels of damage caused by B. musae across the whole peninsular have not

been formally documented. While on a field trip to PNG in July 2007, I learned from

local sources that areas of the Gazelle along the northern coastline around Vudal and

Vunapalading may be hot spots for B. musae. Farmers in those areas had begun to

notice fruit fly larval damage on banana and were enquiring at the Lowlands

Agriculture Experiment Station (Keravat) for staff to determine the cause and advise of

control options. Farmers were advised to bag their bananas and demonstrations were

provided in gardens and/or at the agriculture station. That farmers are now seeking

advice to control the pests implies that, for at least some districts, damage levels are of

sufficient level to concern growers. In contrast to this, however, is the Cavendish data

(Table 6.2 and Chapter 4), for which only two samples from 19 yielded any flies. This

low level of infestation much better reflects the earlier results of the bagging

experiment and market survey.

Table 6.2 Infestation of mature green Cavendish banana by Bactrocera musae (Tryon)

at four locations on the Gazelle Peninsula, East New Britain, Papua New

Guinea, in 2007

Location Sample Weight of sample (gms)

Number of fingers Number of flies

Kokopo 1 5300 38 0 2 3950 29 3 3 3430 30 0 4 3180 34 69 5 4730 39 0 Rabaul 1 3180 28 0 2 2940 27 0 3 5530 34 0 4 4130 24 0 Keravat 1 2910 28 0 2 4460 29 0 3 4650 46 0 4 3600 30 0 5 5060 41 0 Induna 1 4840 34 0 2 2960 30 0 2 2890 37 0 4 6800 39 0 5 3200 22 0 Total 19 77,740 619 72

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6.4 Discussion

This chapter, on an invasion by B. musae, identifies a species that has arrived in a

novel area, become established and spread from the original point of arrival.

Ecological factors in the environment have obviously been favourable for B. musae

establishment, while the initial population was also obviously large enough to allow

establishment. Sampling for B. musae on the Gazelle shows banana fly populations are

as large as endemic mainland sites, but the impact of those flies on local banana

production is apparently minimal. Almost ten years post incursion (at least seven since

first detection), it is only recently that I have heard of banana farmers observing

damage and enquiring for appropriate control measures; and then only in certain areas

on the peninsular. Whether impact has been low due to limitation by local cultivation

practices is uncertain, but that may have an influential role. On the Gazelle farmers

harvest at maturity and consumption is often immediate, meaning that the fruit may be

picked and consumed before they are at the stage most vulnerable to fly infestation. Or,

again reinforcing the point made in both Chapters 4 and 5 (Infestation of bananas by

Bactrocera musae (Tryon) in Papua New Guinea), commercial banana varieties may

be poor hosts of banana fly and generally little affected by it (at least in an

environment where more preferred Musa species or cultivars may be apparent). Further

studies into the biology and ecology of B. musae in this novel environment would

further improve our understanding of the invasibility of B. musae in this novel

environment. It would also provide information on the invasiveness of such a

Bactrocera species, one with a narrow host range, in a novel tropical environment.

With respect to information for developing a PRA, what does the incursion into East

New Britain tell us? Firstly, that flies can be transported along some pathway, in

numbers sufficient to lead to local establishment. What that pathway was is uncertain,

but Putulan et al. (2004) argue that simple carriage of infested bananas was a likely

pathway. Data from their work identified that one in every 100 airline passengers

landing on the Gazelle (i.e. about one person a day) would be carrying an infested

banana. That the flies must have been carried to the Gazelle, rather than dispersing

naturally, is evidenced by the fact that West New Britain Province, much closer to the

mainland, remains free of the fly (Mararuai et al., 2001), inferring that the fly has

“hopped” (via a pathway) to the Gazelle. Having established a bridgehead, the fly very

rapidly expanded its range, occupying substantially larger areas in only six months

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between the first phase and second phase delimiting surveys. This rapid spread meant

that eradication plans for the fly were abandoned (A. Allwood 2001, unpublished

report), and poses a serious biosecurity concern for regions where the fly might

potentially enter. In short, this data suggests that if the fly does enter and establish in a

new area, eradication needs to be attempted immediately if hoped to be successful. The

final issue for a PRA is to do with impact. While banana fly is a recognised pest of

banana fruit, on the Gazelle infestation levels are low in experimental trials, surveys

and gardens. Part of this may be due to banana varietal effects and management

practices, but it again reinforces the data from other chapters that banana fly is not of

major concern in PNG.

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Chapter 7. Discussion

7.1 Thesis summary

7.1.1 Introduction

Banana is an important staple food crop in PNG, as well as being an important revenue

generating crop. Improved crop production methods and the setting up of pathways for

crop marketing are recognised mechanisms by which improved socio-economic

development can be achieved for PNG’s subsistence and semi-commercial farming

population. With the PNG National Government’s intentions of promoting banana fruit

as an export commodity, international phytosanitary guidelines on market access

protocols must be adhered to if export is to occur (IPPC, 2005, 2006a, 2008). The Pest

Risk Analysis (PRA), a three step process used for identifying phytosanitary risk and

risk mitigation treatments, is a key element of those protocols (IPPC, 2006b, 2007). A

PRA evaluates scientifically generated information to determine whether an organism

is a pest of quarantine concern for a commodity importing country or region, defines

the probability of introduction, establishment and spread of the pest in that region, and

risk management options that can reduce the risk to an acceptable level (IPPC, 2007).

This thesis carried out work to help assist the PRA process for PNG banana fruit

exports. A summary of the thesis results follow, while a full description of how the

results fit within a PNG banana PRA after that is presented.

7.1.2 Summary

Evaluation of agriculture research reports, published literature and expert opinion for

pests of banana in PNG found that there are 112 organisms associated with this crop;

consisting of pathogens, insects, nematodes and weeds. Fourteen of these species are

commonly managed. Reports on the local research done on these 14 cover aspects in

biology, damage assessment, and applicable methods for their control however there is

little information in comparison available for B. musae, a fruit fly species documented

as the major pest of banana fruit. Information supplied in this thesis fills key aspects of

the previously missing information about this pest.

Analysis of trapping surveys carried out in PNG show that the detailed distribution of

B. musae in PNG is contrary to that previously reported (e.g. Drew 1989). The fly

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species is widely distributed across mainland PNG, but is absent (except as a recent

incursive) on the PNG island provinces of the Bismarck Archipelago (i.e. New Britain,

New Ireland, Manus and Bougainville Islands). On the mainland the fly is found from

sea level to above 1800 m.a.s.l. Host availability is weakly, but significantly correlated

with population abundance, while the abiotic factors of altitude and rainfall are not

significantly correlated with banana fly population abundance.

Previously reported as a major (often “the major”) pest of PNG banana fruit,

information reported in this thesis contradicts this assessment. Results gathered from

damage assessment surveys, field trials and detailed laboratory work, present a

consistent outcome that unambiguously point to the fact that cultivated banana

varieties (at least of the varieties assessed here) are not the preferred or primary host of

B. musae. This judgement is based on the uniformly low levels of field infestation, in

both endemic and introduced parts of the species’ range, and very poor host selection

outcomes in lab based studies. Laboratory trials found the fly has a preference for ripe

fruit over mature-green and colour-break fruit and, while able to oviposit and develop

in mature green fruit, probably does so only rarely in the field. Similar, but very low

rates of oviposition and adult emergence from Cavendish and Ladyfinger banana,

strongly suggests that both these varieties are poor hosts for the fly. Very high

abundances of banana fly in PNG must be generated from Musa species, or Musa x

paradisiaca varieties, not studied in this thesis.

7.2 PRA for PNG Banana

7.2.1 Definitive statement of IPPC PRA process

Organisms associated with a commodity intended for international commodity trade

are studied to determine if they may pose a social, economical or environmental threat

if transported from the site of production and establish in the region of sale (IPPC,

2004a, b). The studies must adhere to standardised requirements and be reported as

specified by international guidelines (IPPC, 2002a). The study of each organism of

interest is important because their biology will describe the method through which the

organism attacks or causes damage, while ecological information on factors

influencing survival and reproduction is essential information in their management

(Allwood, 1996a). Due to the continuous threat of invasive organisms transported via

commodity trade, such information enables the setting up of processes and approaches

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to minimise pest movement, and to predict and prevent their establishment (Cook,

2008).

Reporting of information for a PRA has standardised outlines, with specific

requirements for necessary elements (IPPC, 2002a, 2007). The framework must

include verification of the purpose of the PRA, stating the pathway of concern that may

harbour and transport potential risk organisms to the destined import market

environment (IPPC, 2007). Main elements for documentation require identification of

the target organism, or in my case the banana variety selected for trade, and the area

where production will occur. Required information on biological attributes of

organisms associated with the commodity is their ability to cause damage, their host

range, and method and mode of infestation. Information on the evidence and detailed

analysis on social, economic and environmental impact and the sources from which

such information is obtained is important. The report should also contain the

conclusion obtained from the completed PRA and the decisions and justifications

made. It should clearly state the pest risk management measures identified, evaluated

and recommended and the dates of when the PRA was done, by whom and reviewed

by which authoritative individual(s) and reviewer(s).

7.2.2 Summary on PNG banana PRA

The purpose of a PNG banana PRA would be to determine risks involved in moving

unwanted organisms via the production, storage and transportation of banana from

PNG to an international market destination. The PRA would be initiated for the

assessment of a commodity, or pathway, as referred to in the IPPC guideline not a

certain pest and thus is recognised as a ‘pathway initiated analysis’ (IPPC, 2007). The

report requires certification of the processes carried out, verification of the supervising

national quarantine authority and names of authors, contributors and reviewers

responsible and associated in producing the report.

The PNG banana PRA would require a morphological and taxonomical description of

the banana variety(s) selected for commodity production. Other necessary information

required include: areas identified for commodity production, distribution of and

cultivation practices for the variety, non-commodity varieties present in the producing

area, and use of the commodity variety in the producing area. A categorised pest list

would require the current 112 organisms identified associated with banana to be sorted

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by pest status. The fourteen commonly reported organisms may be reported as pests,

but they also require categorisation as to whether pest status is that of a quarantine

pest. This list, however, is not specific to a certain banana variety and therefore is best

utilised as a reference point when studying organisms associated with the variety(s)

selected for commodity production. Verification of areas where production would

occur is important and a detailed study in the locality would be required. Research in

PNG on those fourteen species provides information on biological, ecological and

management details, but some of the reported work is not current and an update would

be appropriate. Studies would need authentic investigation, be formally reported and

should be readily accessible to the international community. Economic impact

assessment is an area which needs more focus. Documentation and the use of

standardised methodologies and processes are important to verify the impact of

damage on produce quantity and quality even for those species that do not cause

serious problems and to allow for comparison across different banana varieties.

Assessment procedures and methodologies are important for transparency in report

writing and for trade partners and is an area which future assessment reports must

provide. It is also important to note that the collecting of information on the organisms

associated with banana is a continuous activity. Investigations carried out in this thesis

provide the following information for the PRA and shows areas that need attention

(Table 7.1).

7.2.3 Detailed PRA response for banana fly

Within the context of a full PNG banana PRA as described above, and using the three

step outline of the PRA, this thesis has found the following for banana fly:

Step 1 Risk Initiation. Banana fly is a presumed oligophagous fruit fly species on

Musa species. Reported as a major pest of commercial banana (Musa x paradisiaca

varieties), this thesis has shown that due to the consistently low infestation levels on

cultivated varieties reported pest status of banana fly is incorrect and that it should be

regarded as a minor pest of cultivated banana varieties in PNG. In the tropical

environment of PNG, the importance of banana in local cropping systems is weakly,

but significantly correlated with banana fly population abundance, while temperature

and rainfall have no significant influence. The distributional range of the species is

from sea level to above 1800 meters in elevation and endemic to the PNG mainland.

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The inference of results presented here are that bananas grown anywhere in PNG are at

equal, albeit low, risk of banana fly infestation.

Table 7.1 Checklist of information available and necessary for carrying out a pest risk

analysis of PNG bananas; a pathway initiated analysis

Requirements Information available Information needed Commodity description Banana varieties in PNG

currently documented Selected variety(s) for commodity production

Categorised Pest list 112 organism identified, 14/112 commonly managed

Categorisation list – quarantine pest, non-quarantine pest

Evidence of economic impact, which includes environmental impact

No detailed or specific information available for economic and environmental impact

Update needed for 14 commonly managed pests, Environmental impact studies

Conclusions of pest risk assessment (probabilities and consequences)

Not yet done

Decisions and justifications to stop the PRA process

Not yet done

Pest risk management: phytosanitary measures identified, evaluated and recommended

Not yet done

Step 2 Risk Assessment. Fly larvae can be transported via banana and establishment in

novel areas will be influenced by the presence of susceptible hosts. Based on the

known incursion in East New Britain province, establishment of the fly in non-endemic

areas may readily occur in the presence of hosts, with spread from the point of

establishment rapid. Ripe banana fingers are the preferred maturity stage for

oviposition, but mature-green and colour-break fingers are able to sustain banana fly

immature development through to the adult stage. Wild banana fly populations can

occur in relatively large numbers, but the impact that such populations may have on the

commodity will be dependent on the banana variety and stage of ripeness at harvest.

Further study is required to determine the impact of banana fly on a wider range of

cultivated varieties because studied varieties are not heavily infested, suggesting these

varieties may not be the primary host. Other banana varieties may be heavily infested.

This is a particular risk as export of banana from PNG may focus on less common

banana varieties which target specialist and gourmet markets.

141

Step 3 Risk Mitigation. The research done in this thesis suggests that there will only

be a few possible risk mitigation techniques. The very high abundance of flies, but

very low infestation rates, means that traditional pre-harvest control techniques (e.g.

cover-sprays, male annihilation, protein bait spraying, crop hygiene) (Allwood, 1996b)

are unlikely to substantially influence infestation rates, as flies are obviously breeding

in non-managed areas. Management of flies in the immediate crop area is thus likely to

cause little or no reduction in the total background fly populations and, hence, no

change in the already low infestation rates. Harvesting bananas at mature green, a

currently recognised protocol, should be maintained, although I show that this cannot

be regarded as a definitive, single-step treatment as flies can oviposit into, and develop

through, on mature green bananas. Bagging of banana bunches does appear an

effective management strategy, with no infestation of bagged bunches in the trial run

on the Gazelle Peninsula. Low levels of infestation in unbagged controls, however,

mean that further trials would need to be run before this approach could be used with

confidence. Nonetheless, fruit bagging is a widely used fruit fly management tool,

particularly in countries where labour is relatively inexpensive (Allwood, 1996b).

Given the field infestations are so low, single step post-harvest treatments (e.g.

insecticide dipping, heat treatments) (Armstrong, 1996; Neven & Drake, 2000; Shellie

& Mangan, 2000) are likely to be the most effective phytosanitary protocol for banana

fly, as there is little or no need for in-field, pre-harvest controls..

7.3 Implications of thesis for wider fruit fly market access issues

The abundance of an insect pest is often assumed to be directly and positively

correlated to the crop damage caused by that pest (Drew et al., 1984; Alyokhin et al.,

2001; Meats et al., 2003). The international phytosanitary protocols of “areas of low

pest pressure” (IPPC, 1995, 1997, 1998, 1999, 2002b) operate under the assumption

that low levels of pest abundance will result in low levels of crop infestation.

Alternatively, areas where a pest is well established require commodity treatment

protocols (Armstrong, 1996; Carey, 1996; Armstrong, 2001; Follett, 2004; Stice et al.,

2007), based on the assumption that commodities will be infested. However, the results

obtained in this thesis for B. musae on banana in PNG shows that levels of fly

abundance need not relate to host infestation levels. Low banana finger infestation

142

levels in areas with very large banana fly populations raises questions about the

certainty of predicting crop damage levels from population abundance (e.g. trap) data.

7.3.1 Trap abundance and host use by fruit flies

Detection and monitoring (leading to subsequent management) of pest Bactrocera

species, such as B. musae, is almost entirely done through adult trapping (Cowley,

1990; Rössler et al., 1998; Broumas et al., 2002; Hollingsworth et al., 2003; Meats et

al., 2003; Meats & Clift, 2005; Burrack et al., 2008). Fruit fly traps utilise two lures

that are recognised by adult male flies, with a particular fruit fly species responsive to

only one lure type (Metcalf et al., 1975; Brieze-Stegeman et al., 1978; Hooper, 1978).

Maturing and mature adult male flies forage for, and are positively attracted to,

naturally occurring plant chemicals and these chemicals are identical, or very similar,

to the lures used in traps (Fletcher et al., 1975; Chuah et al., 1997; Nishida et al.,

2004). Female flies do not generally respond to these lures and are rarely caught in

fruit fly traps (Metcalf et al., 1975; Hill, 1986). Traps for most Bactrocera species are

very effective and are able to attract adult male flies within a radius of 500m (Metcalf

& Metcalf, 1992; Jang & Light, 1996). Such traps allow for the collection of

information on male fruit fly distribution and abundance in different habitats and

cropping systems. It is a general tacit assumption of fruit fly trapping that measures of

male abundance are positively correlated with assumed female abundance.

Abiotic factors such as temperature, rainfall and host availability all influence the

population dynamics of tephritid species (Bateman, 1972; Allwood, 1996a). Biotic

environmental factors such as amount of canopy cover (Dalby-Ball & Meats, 2000a;

Raghu et al., 2004), natural sources of male parapheromones (Jang & Light, 1996),

olfactory chemicals (Flath et al., 1990; Meats & Osborne, 2000), and food resources

(Drew et al., 1983; Fletcher, 1987; Raghu, 1998) also influence total population

abundance, as well as the local densities of flies within a larger population. While all

such factors may influence the abundance of flies, the effect that each may have on a

local population of a particular fruit fly species may vary. This is illustrated with the

correlation analysis in Chapter 3, where the correlation of altitude and rainfall on

population levels of five fruit fly species all varied. Most importantly, of all the factors

which may influence the abundance of a local fly population, it is only one of these,

host availability, which is directly related to crop impact (i.e. flies utilising a

143

commodity for breeding will impact upon it). It is equally important to note that fruit

fly traps attract males, yet is the unstudied females which cause crop damage. Thus is it

perhaps not surprising that there need be no obvious relationship between fruit fly trap

catch and crop infestation, as in the case of banana fly.

For fruit fly susceptible commodities, host impact is the damage resulting from feeding

by fruit fly larvae. The larvae hatch from eggs oviposited by female flies. Host

selection is a complex and time-consuming process of search and investigation, before

selection and oviposition, and is influenced by olfactory, semiochemical and physical

cues present in the habitat in which the parental female forages (West & Cunningham,

2002; Bruce et al., 2005). Having said that, with respect to banana fly in PNG, why

does an abundant and widespread fly not routinely use a common and widespread

host?

Banana fly is a narrowly oligophagous fruit fly species (Fletcher, 1987) and has a

preferential host utilisation and selection behaviour (for Musa spp) characteristic of

specialist herbivores (Fitt, 1986). Specialist herbivores are more sensitive to their

environment and are more affected by host-plant resistance mechanisms and variable

host quality than are generalists (Tscharntke et al., 2001). Plant attributes which are

known to influence tephritid host use include characteristics such as colour, sugar

content, and peel hardness or toughness (Bateman, 1972; Fletcher, 1987), all of which

are highly variable across banana species and cultivars (Osuji et al., 1997; Lucas et al.,

2000). It is thus possible (likely?) that particular banana varieties may be highly

susceptible to banana fly, just not the varieties studied here.

Population dynamics of specialist herbivores are also considered to be less influenced

by abiotic conditions and more by their host’s population characteristics, such as host

population size (Scheidel et al., 2003). With respect to the PNG banana fly situation,

the germplasm diversity of banana (Musa spp.) in PNG is very large and multiple M. x

paradisiaca varieties are cultivated in banana growing areas at any one time, while

wild Musa species can be highly abundant in contiguous and remnant rainforest areas.

The low levels of banana crop utilisation observed for banana fly in PNG may simply

be the normal behaviour of a specialist herbivore which, in the presence of an abundant

food source, utilises only a small portion of potential larval food resources (Singer et

al., 1989; Debouzie et al., 2002). This behaviour may be exacerbated if the main

144

commercial varieties grown, such as Cavendish and Ladyfinger, are inherently non-

preferred or poor quality hosts, as seems to be the case based on laboratory results

(Chapter 5).

7.3.2 How does this relate to Market access?

The nature of developing international protocols (in any field) means that issues are

often highly simplified so to address as wide a range as possible of different

contingencies and stake-holder issues and sensitivities. With respect to phytosanitary

protocols, one of the most common simplifications is that given a pest (insect or

pathogen), and given a reported host crop, infestation is going to occur and needs to be

managed. While the logic for such a simplification is obvious, the science

underpinning the simplification is less obvious. Even for highly polyphagous pest

insects host preference rankings occur (Bravo et al., 2001; Clarke et al., 2005), a very

well documented trait among herbivorous insects (Fry, 1996; Carriere, 1998;

Steinbauer, 2002). Preferences are not static, but can change based on the physiological

status of the insect, the quality of the host plant(s) and a suite of other traits both

internal and external to the insect. Herbivore preferences are such that in the presence

of a preferred host, less preferred hosts are unlikely to be utilised (Fitt, 1986). In my

banana fly case, literature records that bananas are hosts for banana fly means that

export restrictions for getting banana out off PNG will be very stringent, despite

evidence from the field that banana usage by banana fly is very low. This is because

the published records make little or no acknowledgement of the fact that banana fly is

likely to infest different banana species and cultivars differently, even when in high

abundance. If international phytosanitary protocols are to be based on sound science,

as international agreements require, then greater emphasis must be placed on

understanding the biological link between herbivores and host use, so as to allow better

links to be made between pest abundance, crop infestation and phytosanitary risk.

145

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Appendices

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Appendix 2 Distribution and Biogeography of Bactrocera and Dacus species (Diptera: Tephritidae) in Papua New Guinea

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Appendix 3 Introduction and Distribution of Bactrocera musae (Tryon) (Diptera: Tephritidae) in East New Britain, Papua New Guinea

Mararuai, A., Allwood, A.J., Balagawi, S., Dori, F., Kalamen, M., Leblanc, L., Putulan,

D., Sar, S., Schuhbeck, A., Tenakanai, D., & Clarke, A.R. (2001). Introduction and

distribution of Bactrocera musae (Tryon) (Diptera: Tephritidae) in East New Britain,

Papua New Guinea. Papua New Guinea Agricultural Journal, 45, 59-65.

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