Summary of Australian Research on Cold Disinfestation



DISCUSSION PAPER Cold treatment tolerance of fruit flies

Dated: 03 July 2013

Compiled by

Andrew Jessup, NSWDPI, Australia

Guy Hallman, USDA/ARS, USA

Patrick Gomes, USDA-APHIS-PPQ, USA

Eduardo Willink, EEAOC, Argentina

BACKGROUND

Currently there exists a large and seemingly inconsistent list of approved and submitted cold storage phytosanitary schedules that are required for domestic and international market access of fresh fruits and vegetables. Different quarantine schedules may vary for similar fruit types and identical pest fruit fly species depending on from which country they are exported. Members of the IPPC and its panels, the Technical Panel of Phytosanitary Treatments and the Technical Panel on Fruit Flies, have seen the need to harmonise methods used by member states in obtaining and reporting efficacy data for use in export submissions.

Not only are there apparent inconsistencies with treatments but published literature is also divided on the simple question of which immature pest life stage that is likely to be found infesting imported fruit is the most treatment-tolerant. In many experimental protocols for the development of quarantine treatments a determination of the most treatment-tolerant infesting life stage is used to facilitate testing the efficacy of the treatment to required levels of quarantine security. It is most likely that these variations are caused by variable laboratory conditions and experimental protocols between research agencies. If this is the case then harmonisation of experimental procedures and their reporting would be very useful in facilitating market access.

A meeting of cold treatment experts has been called by the IPPC in late 2013 to discuss cold treatment issues. It is envisaged that the outputs from this meeting will include delineating the variables that impact on treatment efficacy, and how to account for them or quantify them, agreement on a common approach to the development of cold treatment schedules and plans for future collaboration of experts and member states. Another function of this meeting will be to review as many current cold storage based quarantine treatments as possible that are currently approved and under review by the IPPC and national quarantine authorities.

ABSTRACT

The following is a draft position paper on the current status of

- Determination of the most treatment-tolerant pest life stage and

- Approved cold storage quarantine treatments

It is apparent that there are some inconsistencies between laboratories reports on the most cold-tolerant life stages and between countries who approve cold storage quarantine treatments. There is justification in an attempt to harmonise research and development on these treatments, globally.

More information, as it comes to hand, will be added to this position paper and the authors welcome any additions, corrections, suggestions and constructive criticism.

A brief discussion on past assessments of the most cold-tolerant Tephritid life stage

Extracted from: Guy J. Hallman, Scott W. Myers, Mokhtar F. El-Wakkad, Meshil D. Tadrous, and Andrew J. Jessup (in J. Econ. Entomol. review), Development of Phytosanitary Cold Treatments for Oranges Infested with Bactrocera invadens and B. zonata (Diptera: Tephritidae) by Comparison with Existing Cold Treatment Schedules for Ceratitis capitata (Diptera: Tephritidae).

The 3rd instar was found to be the most cold-tolerant stage for Bactrocera invadens and B. zonata (Grout et al. 2011a, Mohamed and El-Wakkad 2009).

The literature is not consistent concerning the most cold-tolerant stage of Ceratitis capitata. Grout et al. (2011b) concluded that the most cold-tolerant stage was the 2nd instar based on a commodity group research report from South Africa (Ware et al. 2006). Hallman et al. (2011) cited Powell’s (2003) analysis of historical cold treatment data for C. capitata as supporting the 3rd instar to be the most cold-tolerant stage. A summary of studies of most cold-tolerant stage of C. capitata follows.

Back and Pemberton (1916) studied cold tolerance among eggs and all three instars of C. capitata in apples from 0-4.4°C in Hawaii and found that the 3rd instar was more tolerant than the 2nd in all seven tests done. Most of Powell’s (2003) analysis indicating the 3rd instar to be the most tolerant was based on Back and Pemberton (1916). Hashem et al. (2004) in Egypt found that the 3rd instar was the most cold-tolerant stage at 1.7 and 4°C when C. capitata was reared in guava, mango, and orange (‘Navel’ and ‘Valencia’). Ware et al. (2006) did not test distinct instars but evaluated eggs and six and eight day-old larvae (reared at 26°C) at 1°C in grapefruit, orange, and lemon. They concluded that there was no statistical difference in mortality although in orange (but not grapefruit or lemon) survival was nominally higher for six than eight day-old larvae. The data for orange are curious in that survival of eight day-old larvae was higher up to 5 d at 1°C (25.3%) than in the non-treated control (17.6%).

Three relevant studies with C. capitata were done in Australia. Hill et al. (1988) compared tolerance of eggs, a mixture of 1st and 2nd instars, and mostly 3rd instars to 1.5 ± 0.5°C in oranges and found both larval groups to be very similar, with the younger instars showing a very slight advantage in survival. Jessup et al. (1993) found that the 2nd instar was the most tolerant to 1 ± 0.2°C in two cultivars of lemons. De Lima et al. (2007) in Australia found that the 2nd instar was more tolerant than the 3rd in five types of citrus fruit at 2 and 3°C.

It is possible that different populations of C. capitata vary in relative tolerance of the different stages to cold. Diamantidis et al. (2011) found that geographically isolated populations of C. capitata vary in a number of traits (e.g., reproductive patterns, survival, developmental rate, intrinsic rate of increase). From the literature it seems that the most cold-tolerant stage for most populations of C. capitata is the 3rd instar with the only well-documented exception being Australia. Ware et al. (2012) write that Sproul (1976) working in Australia determined that 3rd instar C. capitata was the most cold tolerant in ‘Granny Smith’ apples when in actuality Sproul (1976) does address the issue of most cold tolerant stage nor do his data shed light on the subject.

References

Back, E. A., and C. E. Pemberton. 1916. Effect of cold-storage temperatures upon the Mediterranean fruit fly. J. Agric. Res. 5: 657-666.

De Lima, C. P. F., A. J. Jessup, L. Cruickshank, C. J. Walsh, and E. R. Mansfield. 2007. Cold disinfestation of citrus (Citrus spp.) for Mediterranean fruit fly (Ceratitis capitata) and Queensland fruit fly (Bactrocera tryoni) (Diptera: Tephritidae). New Zealand J. Crop Hortic. Sci. 35: 39-50.

Diamantidis, A. D., J. R. Carey, C. T. Nakas, and N. T. Papadopoulos. 2011. Population-specific demography and invasion potential in medfly. Ecol Evol. 1: 479–488.

Grout, T. G., J. H. Daneel, S. A. Mohamed, S. Ekesi, P. W. Nderitu, P. R. Stephen, and V. Hattingh. 2011a. Cold susceptibility and disinfestation of Bactrocera invadens (Diptera: Tephritidae) in oranges. J. Econ. Entomol. 104: 1180-1188.

Grout, T. G., P. R., Stephen J. H. Daneel, and V. Hattingh. 2011b. Cold treatments of Ceratitis capitata (Diptera: Tephritidae) in oranges using a larval endpoint. J. Econ. Entomol. 104: 1174-1179.

Hallman, G. J., S. W. Myers, A. J. Jessup, and A. Islam. 2011. Comparison of in vitro heat and cold tolerances of the new invasive species, Bactrocera invadens (Diptera: Tephritidae), with three known tephritids. J. Econ. Entomol. 104: 21-25.

Hashem, A. G., N. A. Soliman, and A. M. Soliman. 2004. Effect of low temperatures on eggs and larvae of Mediterranean fruit fly and peach fruit fly inside fruits as a quarantine procedure. Ann. Agric. Sci. Moshtohor 42: 345-356.

Hill, A. R., C. J. Rigney, and A. N. Sproul. 1988. Cold storage of oranges as a disinfestation treatment against the fruit flies Dacus tryoni (Froggatt) and Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). J. Econ. Entomol. 81: 257-260.

Jessup, A. J., C. P. F. De Lima, C. W. Hood, R. F. Sloggett, A. M. Harris, and M. Beckingham. 1993. Quarantine disinfestation of lemons against Bactrocera tryoni and Ceratitis capitata (Diptera: Tephritidae) using cold storage. J. Econ. Entomol. 86: 798-802.

Mohamed, S. M. A., and M. F. El-Wakkad. 2009. Cold storage as disinfestation treatment against the peach fruit fly, Bactrocera zonata (Saunders), (Diptera: Tephritidae) on Valencia orange. Egypt. J. Appl. Sci. 24: 290-301.

Powell, M. R. 2003. Modeling the response of the Mediterranean fruit fly (Diptera: Tephritidae) to cold treatment. J. Econ. Entomol. 96: 300-310.

Sproul, A. N. 1976. Disinfestation of Western Australian Granny Smith apples by cold treatment against the egg and larval stages of the Mediterranean fruit fly, (Ceratitis capitata (Wied.)). Aust. J. Exp. Agric. Anim. Husb. 16: 280-285.

Ware, A. B., C. L. N. Du Toit, S. A. Mohamed, P. W. Nderitu, and S. Ekasi. 2012. Cold tolerance and disinfestation of Bactrocera invadens (Diptera: Tephritidae) in ‘Hass’ avocado. J. Econ. Entomol. 105: 1963-1970.

Ware, T., B. Tate, J.-H. Daneel, P. Stephen, and R. Beck. 2006. Sensitivity of Mediterranean fruit fly eggs and larvae in lemons, grapefruit and oranges to cold treatment of 1°C. pp. 100-106 in: Citrus Res. Internat. Group Ann. Res. Rpt. 2005.

Preliminary Summary of Research on Cold Disinfestation against Mediterranean Fruit Fly (Ceratitis capitata) and Queensland Fruit Fly (Bactrocera tryoni)

The following tables gives a resume of reported data (published as a paper, a report to a funding agency or as an export submission).

In Table 1 items marked with a question mark (?) are unknown at present but will be added when I get the information from the researchers. With the exception of the authors mentioned in the table below all research described here was carried out by De Lima (Ceratitis capitata) and Jessup (Bactrocera tryoni).

The information in Table 1 shows that the pest life stage that is most tolerant of cold storage varies with pest, fruit species, temperature and researcher. It is known that researchers from other countries carrying out similar research have also found some variability in which immature life stages were most cold-tolerant.

The numbers of insects treated which are used to determine the most cold-tolerant immature life stage are generally quite large so statistical analyses are, on the whole, accurate, within the limitations of the statistical package used. Is it feasible that the observed variability is due to laboratory/ handing factors or intrinsic host fruit factors or, more likely, a combination? Are these differences real or are they due to human-induced artefacts?

Table 1. Summary of Australian research on cold disinfestation of a number of fruits and their cultivars against Ceratitis capitata and Bactrocera tryoni.

|Fruit |Cultivar |Ceratitis capitata |Bactrocera tryoni |

| | |MTS |Treatment |MTS |Treatment |

|Table grape |Flame Seedless |2nd |1°C 16d |1st |1°C 12d, |

| | | | | |2°C 14d, |

| | | | | |3°C 14d |

| |Ruby Seedless |2nd |1°C 16d |1st |1°C 12d, |

| | | | | |2°C 14d, |

| | | | | |3°C 14d |

| |Thompson’s Seedless |2nd |1°C 16d, |1st |1°C 12d, |

| | | |2°C 18d, | |2°C 14d, |

| | | |3°C 20d | |3°C 14d |

| |Red Globe |2nd |1°C 16d, |1st |1°C 12d, |

| | | |2°C 18d, | |2°C 14d, |

| | | |3°C 20d | |3°C 14d |

| |Crimson Seedless |2nd |1°C 16d, |1st |1°C 12d, |

| | | |2°C 18d, | |2°C 14d, |

| | | |3°C 20d | |3°C 14d |

|Grapefruit |Flame |? |2°C 18d, |1st |2°C 14d, |

| | | |3°C 20d | |3°C 14d |

| |Rio |? |2°C 18d, |1st |2°C 14d, |

| | | |3°C 20d | |3°C 14d |

|Orange |Navel |2nd |2°C 18d, |1st |1°C 16d, |

| | | |3°C 20d | |2°C 16d, |

| | | | | |3°C 16d |

| | |Egg |1°C 16d |Egg |1°C 16d |

| | | |(Hill et al. 1988) | |(Hill et al. 1988) |

| |Valencia |2nd |2°C 18d, |1st |1°C 16d, |

| | | |3°C 20d | |2°C 16d, |

| | | | | |3°C 16d |

| | |Egg |1°C 16d |Egg |1°C 16d |

| | | |(Hill et al. 1988) | |(Hill et al. 1988) |

|Tangerine |Ellendale |2nd |2°C 18d, |1st |1°C 16d, |

| | | |3°C 20d | |2°C 16d, |

| | | | | |3°C 16d |

|Tangor |Murcott |2nd |2°C 18d, |1st |1°C 16d, |

| | | |3°C 20d | |2°C 16d, |

| | | | | |3°C 16d |

|Tangelo |Minneola |2nd |1°C 16d |1st |1°C 16d |

|Mandarin |Imperial |2nd |1°C 16d |1st |1°C 16d |

|Lemon |Lisbon |2nd |1°C 14d |1st |1°C 14d, |

| | | | | |2°C 14d, |

| | | | | |3°C 14d |

| |Eureka |2nd |1°C 14d |1st |1°C 14d, |

| | | | | |2°C 14d, |

| | | | | |3°C 14d |

|Plum |Angelino |2nd |1°C 16d, |3rd |1°C 14d, |

| | | |3°C 20d | |3°C 14d |

| |Tegan Blue |2nd |1°C 16d, |Not done |

| | | |3°C 20d | |

|Cherry |Sweetheart |2nd |1°C 16d, |1st |1°C 14d, |

| | | |3°C 20d | |3°C 14d |

| |Lapin |2nd |1°C 16d, |Not done |

| | | |3°C 20d | |

|Peach |Snow King |2nd |1°C 16d, | |

| | | |3°C 20d | |

| |Zee Lady |2nd |1°C 16d, | |

| | | |3°C 20d | |

|Nectarine |Arctic Snow |2nd |1°C 16d, |2nd |1°C 14d |

| | | |3°C 20d | | |

| | | | |1st |3°C 14d |

| |August Red |2nd |1°C 16d, |Not done |

| | | |3°C 20d | |

|Avocado |Hass |Not done |3rd |1°C 16d |

| | | | |(>46°C 15min HW dip) |

|Blueberry |Premier | |1st |1°C 12d |

| |Climax | |1st |1°C 12d |

| |Sharpe Blue | |1st |1°C 12d |

|Apple |Red Delicious | |1st |1°C 12d, |

| | | | |3°C 12d |

| | | | |(Leach et al.) |

| |Pink Lady | |1st |1°C 12d, |

| | | | |3°C 12d |

| | | | |(Leach et al.) |

|Nashi |Nijisseiki | |3rd |1°C 12d, |

| | | | |3°C 12d |

| | | | |(Leach et al.) |

| |Hosui | |1st |1°C 12d, |

| | | | |(Leach et al.) |

| | | |3rd |3°C 12d |

| | | | |(Leach et al.) |

|Pear |Packham | |1st |1°C 12d, |

| | | | |3°C 12d |

| | | | |(Leach et al.) |

| |Williams | |1st |1°C 12d, |

| | | | |3°C 12d |

| | | | |(Leach et al.) |

|Capsicum annuum |Red or Green maturity | |1st |3°C 10d |

| | | | |(preliminary data)* |

| | | | |(Ekman) |

|Lychee |Bengal | |1st |1°C 12d |

| | | | |(preliminary data) |

* (preliminary data) – data not sufficient to demonstrate Probit 8.7 ( for export to Japan and others) or Probit 9 (for export to the USA and others)

In Table 2 a summary of some international research done on Ceratitis capitata only is shown. It can be seen that these approved quarantine treatments are not uniform even when the same pest fruit fly and host commodity are involved.

There is a desire to harmonise cold disinfestation treatment schedules into something more logical than is current. We need to know why these schedules differ so widely. It is no doubt due to changes in refrigeration technology, variations in experimental protocols, variations in statistical analyses and so on.

While accepting that different fruit fly species may well have different tolerances to cold storage it is thought unlikely that a particular insect species would vary in its tolerance to temperatures depending on its origin. However there is discussion amongst entomologists that species may adapt to different climatic regimes in their habitat and so be more tolerant of cold storage than insects of the same species in warmer climates. Additionally, discussion has been on whether insects are more able to tolerate cold storage in some fruit species, and even in some fruit varieties, than others. This certainly seems to be the case when looking at cold tolerance data for some fruit flies in oranges versus lemons.

Tables 3 and 4 are included to show how variable approved export conditions are between country origins, destinations and fruit fly species. It seems illogical to have so many different quarantine treatment schedules.

Table 2. Quarantine cold treatment references and reported treatment parameters for killing 100% of Mediterranean fruit fly eggs and/or larvae. (Adapted from “Evaluation of cold storage treatment against Mediterranean Fruit Fly Ceratitis capitata (Wiedemann) (Diptera:Tephritidae)”, USDA May 2, 2002 and other papers shaded grey in the table below.

|Reference |Temperature (°C) |Life stage |Time (days) |

|Back & Pemberton 1916a |0 |Eggsb,c |11 (no data for 10d) |

| |0–0.56 |1st instarc |12 |

| |0.56–1.11 |1st instarc |16 (15d for 3rd instar) |

| |1.11–2.22 |3rd instarc |13 |

| |2.22 |3rd instar |16 |

| |2.22–4.44 |3rd instarc |11 (no data for 10 d) |

| |3.33–4.44 |3rd instarc |25 (no data for 24 or 23d) |

| |4.44–7.22 |3rd instarc |46 |

|Baker 1939d |0 |Larvaee |12 |

| |0.56 |Larvaee |13 |

| |1.11 |Larvaee |14 |

| |2.22 |Larvaee |16 |

|Cottier 1952 |-1.11–0 |Larvaee |21f |

|De Lima 1998 |0.5–1.5 |1st instarc |16 |

|De Lima et al. 2007 |≤1 |2nd instar |16 (orange, tangor, tangerine), 14 (lemon) |

| |≤2 |2nd instar |18 (orange, tangor, tangerine), 16 (lemon) |

| |≤3 |2nd instar |20 (orange, tangor, tangerine), 18 (lemon) |

|Fallik 2012 |1.5 or 4 |Eggs and larvae |21 |

|Fares 1973a |0 |Eggsb,c,g |10 |

|Grout 2011 | ................
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