tox068

Journal of Economic Entomology, 110(3), 2017, 954–960
doi: 10.1093/jee/tox068
Advance Access Publication Date: 21 April 2017
Research article
Commodity Treatment and Quarantine Entomology
Cold Disinfestation of “Hass” Avocado (Persia americana)
of Three Species of Fruit Fly (Diptera: Tephritidae)—
Ceratitis capitata, Ceratitis rosa, and Ceratitis cosyra
A. B. Ware1,2,3 and C.L.N. du Toit1,2
Subject Editor: Lisa Neven
Received 7 October 2016; Editorial decision 3 February 2017
Abstract
The avocado industry is important in South Africa, but access to certain markets is impeded by the presence of
phytosanitary pests. One of the ways of securing entry to these markets is to demonstrate that a mitigating
treatment will result in there being a negligible chance of accidental importation. In cold treatment comparative
studies at 0 C and 2 C of immature stages of Ceratitis capitata (Wiedemann), Ceratitis rosa Karsch, and
Ceratitis cosyra (Walker) in “Hass” avocado, the third instar of C. cosyra was shown to be the most cold tolerant. This larval life stage was used in a large-scale trial to test treatment efficacy at 2 C, a temperature known to
be the better for fruit quality. There were no survivors from the 49,795 individual fruit fly larvae subjected to the
cold treatment at 2 C for 20 d. It is argued that, although this level of assessment falls short of the Probit 9 level
normally required for fruit fly, they are rarely found in avocado fruit and that the level of disinfestation obtained
is more than sufficient to achieve quarantine security.
Key words: Mediterranean fruit fly, Ceratitis rosa, Ceratitis cosyra, disinfestation
The South African avocado industry is located in Mpumalanga,
Limpopo, and KwaZulu-Natal Provinces in the east of the country,
with a small number of growers in the Eastern Cape. There are some
340 commercial growers on 15,500 ha producing 115,000 tons per
annum and employing a labor force of 1,500 (information provided
by the South African Avocado Growers’ Association).
Approximately 45% of the crop is exported to Europe, but entry to
many other markets is prohibited due to phytosanitary issues.
International trade in plant products increases the risk of introduction of new pests and diseases. Consequently, government policies are developed to manage this risk. These policies normally
dictate specific conditions for import of plant material that could
harbor pests and diseases, which could become established in specific "pest-free" areas. The conditions imposed on product entry
may range from the out-right ban to the imposition of pre- and
postharvest mitigating measures. Examples of preharvest actions
may include crop spraying, field monitoring, and inspections while
postharvest activities may include one or more of the following:
postharvest inspections, fumigation, irradiation, heat treatments,
and cold treatments. These are all designed to negate the probability
of accidental introduction (Heather and Hallman 2008).
Not all pre- or postharvest mitigation treatments are suitable for
all commodities. In the case of avocados (Persia americana Miller:
Lauraceae) irradiation of 20 Kilorad often leaves brown lesions
(Kamali et al. 1972) and the application of cold temperatures above
10 C may affect shelf life (Zauberman et al. 1977). However, a temperature of 2.0 C appears to be the treatment of choice in sterilizing
the fruit of insect pests without undue damage to fruit quality or reducing the period it can be stored (Kok et al. 2010). In the United
States, a 14-d treatment at 1.1 C or an 18-d treatment at 2.2 C of
avocado is an acceptable mitigation intervention for the
Mediterranean fruit fly [Ceratitis capitata (Wiedemann)] and
Ceratitis rosa Karsch (U.S. Department of Agriculture–Animal and
Plant Health Inspection Service [USDA-APHIS] treatment manual
2016). Unfortunately there are two other fruit fly species—Ceratitis
cosyra (Walker) and oriental fruit fly [Bactrocera dorsalis
(Hendel) ¼ Bactrocera invadens Drew, Tsuruta and White (Schutze
et al. 2015)]—that could potentially oviposit in avocado fruit in
South Africa (Brink et al 1997, Grové 2001, International Plant
Protection Convention [IPPC] 2013) that are not included in the
USDA-APHIS treatment manual. Research done in Kenya indicates
that a cold treatment of 20 d at 2.0 C is an effective postharvest
mitigation treatment for B. dorsalis (Ware et al. 2012). This article
describes a cold tolerance comparative study of the three agriculturally important fruit fly species (C. capitata, C. rosa, and C. cosyra)
indigenous to South Africa.
C The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America.
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1
Department of Agriculture, University of Mpumalanga, Private Bag X 11283, Mbombela, South Africa ([email protected];
[email protected]), 2Agri-Biotech Research Consultancies (ABRC), P.O. Box 7512, Mbombela, South Africa, and
3
Corresponding author, e-mail: [email protected]
Journal of Economic Entomology, 2017, Vol. 110, No. 3
955
Materials and Methods
Test Insects and Test Fruit
Fruit fly eggs were obtained from colonies kept at Citrus Research
International (Pty) Ltd in Mbombela, Mpumalanga Province,
South Africa. The flies were maintained in gauze cages. Ceratitis
capitata and C. cosyra were kept in a constant temperature room
(26.0 C) while C. rosa, because it is corpuscular insect, was kept
in natural light at ambient temperature under a cover that had
gauze sides.
Ceratitis capitata oviposited through the gauze cages and the
eggs were collected from a basin of water positioned under the cage.
Ceratitis cosyra laid their eggs through the perforated lids of honey
jars and the eggs were washed out using tap water. Ceratitis rosa
oviposited into Granny Smith apples and that collection of the eggs
required cutting the fruit and the washing out of the eggs with water. The collected eggs were placed onto agar-based larval food media where they developed through the larval stages. Immediately
before pupation the larvae “jumped” from the media onto sand
where they pupated. The colonies were supplemented annually with
“wild” flies to maintain genetic variability.
Hass avocados were sourced from H.L. Hall and Sons (Pty)
Ltd near Mbombela and stored at 4.0 C until required. The day
before infestation the required number of fruit was removed from
cold storage and dipped in a quaternary ammonium compound
fungicide (didecyl dimethyl ammonium chloride; Sporekill–
Hygrotec (Pty) Ltd South Africa, Pretoria, South Africa) for 5 min
and then allowed to air dry at ambient temperature. Previous research (Ware et al. 2012) has shown that maturity of the fruit is a
factor in supporting the development of eggs and larvae. The softness (density) of the fruit was tested with a densimeter (Bareiss
Analog Fruit Tester Type Shore A: Bareiss, Oberdischingen,
Germany) and the fruit were infested once a Shore (unit of measurement equal to 0.0025 mm penetration) value of 70 or less was
obtained.
Cold Rooms
The cold rooms, with dimensions 3.0 by 2.2 by 2.5 m (l by b by h),
were constructed out of polystyrene sandwiched between aluminum
sheets placed on a concrete floor. The chiller or heating coil units
were placed near the ceiling. Defrosting (fans off) was done every
six hours for 10 min. The temperature was controlled using Danfoss
control units (Danfoss (Pty) Ltd, Rivonia, South Africa). A Squirrel
meter and logger (Grant model 4F126-2040, Monitoring and control Laboratories (Pty) Ltd, Johannesburg, South Africa) connected
to 16 two-wired type T thermocouples (Temperature Controls Pty
Ltd, Randburg, South Africa) were used to measure fruit-core temperature. Before each treatment, the thermoprobes were calibrated
by placing them on melting ice and on their reaching equilibrium recording the temperature. This was repeated 10 times, and the average calculated was used to adjust for individual thermoprobe
variation. Cold room temperatures were recorded hourly. Two temperatures (0 C and 2 C) were investigated.
General Procedure
The inoculation procedure involved using an electric drill to make
a single 6-mm-diameter hole to a depth through the skin and flesh
to the pip of each avocado. Fruit fly eggs, collected within 12 h of
oviposition, were placed in distilled water and diluted until there
were 30–40 eggs per aliquot. This was then delivered into the hole
which was then sealed with a plug of absorbent cotton wool. The
fruit was then randomly placed into plastic boxes (0.48 by 0.28
by 0.30 m) together with an uninoculated fruit containing a
thermoprobe.
Most Cold Tolerant Life Stage
Each of the three species investigated was processed simultaneously
as shown in Fig. 1. The experiment was replicated three times at
2 C for 20 d for each species.
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Fig. 1. Schematic representation of procedure followed to establish most tolerant life stage of fruit fly.
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Journal of Economic Entomology, 2017, Vol. 110, No. 3
Table 1. Survival and mortality of three replicates of eggs, 3-d-old larvae, and 6-d-old larvae of C. capitata in “Hass” avocado when subjected to various periods of cold treatment of 0.0 C and 2.0 C
C
Exposure (d)
0
Three-day-old larvae
(first and second instar)
No. of
fruit
No.
surviving
Mortalitya
(%)
No. of
fruit
No.
surviving
179
155
164
164
165
165
165
173
151
165
162
165
165
165
500.3
233.3
197.3
24.7
0.3
0
0
495.7
223.0
127.3
38.3
4.7
0
0
–
53.4
60.6
95.1
99.9
100
100
–
55.0
74.3
92.3
99.1
100
100
182
164
164
165
164
164
165
175
149
165
164
160
165
163
162
756.3
369.7
65.3
6.3
0.3
0
0
648.0
406.3
176.0
51.7
4.0
0.3
0
0
Mortalitya
(%)
–
51.3
91.4
99.2
99.7
100
100
–
37.3
72.4
92.0
99.4
99.6
100
100
Six-day-old larvae
(third instar)
No. of
fruit
No.
surviving
180
165
165
164
165
164
165
174
161
165
161
164
165
165
165
165
392.0
364.3
180.7
12.7
0.7
0
0
361.7
330.3
174.0
34.3
10.3
3.0
0.3
0
0
Mortalitya
(%)
–
7.1
53.9
96.8
99.8
100
100
–
8.9
51.9
90.5
97.2
99.2
99.9
100
100
Average number of eggs inoculated (6 SD): Eggs 0.0 C—31.8 6 3.22; 2.0 C—35.1 6 3.7; 3-d-old larvae 0.0 C—36.8 6 4.4; 2.0 C—37.2 6 4.0; 6-d-old larvae 0.0 C—37.8 6 4.1; 2.0 C—38.4 6 4.0.
a
Corrected for natural mortality using Abbott’s formula (1925).
Large-Scale Disinfestation Trials
Based on the results of the above research that was designed to determine which life stage of the three species tested was the most cold
tolerant, eggs were inoculated as described above into 2,500 fruit
and allowed to develop into 6-d-old C. cosyra larvae.
Approximately 80% of the fruit were placed into 2.0 C cold and
the balance was used as the control. The cold chamber temperature
was lowered over three days (an attempt to mimic commercial situation). Once 50% or more of the thermoprobes registered the target
temperature the treatment was deemed to have begun. The first replicate was undertaken over 18 d and another three replicates were
treated over 20 d.
Statistical Analysis
Statistical analysis was undertaken using regression analysis (Probit;
Statgraphics Plus Version 5.1, Statpoint Technologies Inc.,
Warrington, VA) after Abbott’s (1925) transformation of the data
to correct for natural mortality.
Results
Most Cold Tolerant Life Stage
Data, after corrected for natural mortality using Abbott’s formula
(1925), from the three life stages of the three fruit fly species tested
at two different temperatures (Tables 1–3) were subjected to regression analysis (Table 4). Based on the lethal time taken for 99.9%
(95% CL) of the insects to perish, it was determined that 6-d-old
(third instar) C. cosyra larvae were the most cold tolerant at both
the temperatures tested (10.6 d at 0.0 C and 13.6 d at 2.0 C).
Large-Scale Disinfestation Trials
There were two larvae that survived the 18-d treatment at 2.0 C in
an estimated 35,490 individuals tested (Table 5). There were no survivors from an estimated 95,864 treated individuals for 20 d at the
same temperature (Table 5; estimations based on the number of live
insects per fruit in the control). The hourly cold room temperatures
are shown in Fig. 2.
Discussion
Persea americana (cv. Hass) has a number of attributes that makes it
resistant to colonization by fruit fly. The fruit is climacteric (does
not ripen on the tree; De Villiers 2001). Preharvest fruit is hard and
fruit flies find it an unsuitable host, but once harvested, it will soften
and ripen after a few days. However, with the commercial export of
“Hass” avocados from South Africa, the fruit is cooled to around
5 C and is shipped under controlled atmosphere and exported in a
hard state. On removal from cold storage, the fruit physiology
changes and it becomes soft and a suitable host (Ware et al. 2012).
Part of the physiological change is that the hard green exocarp turns
a black color on ripening (Newett et al. 2002). Colonization is dependent on the fruit flies ability to pierce the thick exocarp (Oi and
Mau 1989, De Graaf 2009). Even once overcoming this physical
barrier, tissue regeneration and the formation of calluses restricts
survival (Kay and Schroeder 1963, Smith 1973, Ware et al. 2016) as
does antibiosis (Mwatawala et al 2006).
Avocado is not considered to be a host for C. capitata in field
and laboratory studies (Du Toit and Tuffin 1980, De Lima 1995,
Brink et al. 1997, Willink and Villagran 2007, De Graaf 2009).
They are seldom trapped in avocado orchards (Grové et al. 1998),
indicating a low pest pressure. It is suggested that C. capitata short
aculei (Jones 1989) is unable to penetrate the exocarp (De Graaf
2009).
De Graaf (2009) concluded that C. rosa and C. cosyra are able
to develop in avocado, but development was restricted by fruit defenses. The latter species was shown to be the more cold tolerant, so
the findings of previous research on the effect of cold treatment on
C. rosa could not be used to determine its phytosanitary security.
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2
0
3
5
7
9
11
13
0
3
5
7
9
11
13
15
17
Eggs
Journal of Economic Entomology, 2017, Vol. 110, No. 3
957
Table 2. Survival and mortality of three replicates of eggs, 3-day-old larvae, and 6-d-old larvae of C. rosa in “Hass” avocado when subjected
to various periods of cold treatment of 0.0 C and 2.0 C
C
0
2
Exposure (d)
Three-day-old larvae (first and second instar)
Six-day-old larvae (third instar)
No. of
fruit
No.
surviving
Mortalitya
(%)
No. of
fruit
No.
surviving
Mortalitya
(%)
No. of
fruit
No.
surviving
Mortalitya
(%)
176
163
166
163
164
713.7
66.3
10.7
0
0
–
90.7
98.5
100
100
183
163
162
164
164
525.0
187.3
6.0
0
0
–
64.3
98.9
100
100
170
158
164
168
164
165
617.3
65.0
16.3
0.3
0
0
–
89.5
97.4
99.9
100
100
177
158
165
167
165
165
458.0
94.3
9.3
1.0
0
0
–
79.4
98.0
99.8
100
100
182
160
163
161
165
165
173
158
173
163
164
165
395.3
151.3
24.3
2.7
0
0
318.0
99.0
27.0
1.3
0
0
–
61.7
93.6
99.3
100
100
–
68.9
91.5
99.6
100
100
Average number of eggs inoculated (6 SD): Eggs 0.0 C—28.5 6 3.4; 2.0 C—29.7 6 3.5; 3-d-old larvae 0.0 C—27.8 6 4.2; 2.0 C—24.7 6 3.8; 6-d-old larvae
0.0 C—30.4 6 4.5; 2.0 C—24.7 6 3.8.
a
Corrected for natural mortality using Abbott’s formula (1925).
Table 3. Survival and mortality of three replicates of eggs, 3-d-old larvae, and 6-d-old larvae of C. cosyra in “Hass” avocado when subjected
to various periods of cold treatment of 0.0 C and 2.0 C
C
0
2
Exposure (d)
0
3
5
7
9
11
13
15
0
3
5
7
9
11
13
15
17
Eggs
Three-day-old larvae (first and second instar)
a
No. of
fruit
No.
surviving
Mortality (%)
No. of fruit
No.
surviving
180
165
162
165
164
165
389.7
264.0
153.3
10.3
0
0
32.3
55.7
97.4
100
100
–
179
165
165
165
164
165
165
165
149
160
165
167
166
166
162
165
165
538.3
378.7
153.0
38.3
4.0
0.3
0
0
426.7
319.3
232.0
122.0
25.3
4.3
0.3
0
0
174
155
161
160
147
165
164
165
364.3
256.0
166.0
41.7
6.3
0.3
0
0
29.7
54.4
88.6
98.3
99.9
100
100
–
Mortality
(%)
–
29.7
71.6
92.9
99.3
99.9
100
100
–
25.2
45.6
71.4
94.1
99.0
99.9
100
100
a
Six-day-old larvae (third instar)
No. of
fruit
No.
surviving
180
165
159
164
164
164
165
165
173
161
164
166
188
165
164
166
164
363.7
222.7
113.0
32.3
6.3
0.7
0
0
342.3
268.7
175.0
95.7
45.0
6.3
1.7
0.3
0
Mortalitya
(%)
–
38.7
68.9
91.1
98.3
99.8
100
100
–
21.5
48.9
80.8
86.6
98.2
99.5
99.9
100
Average number of eggs inoculated (6 SD): Eggs 0.0 C—35.4 6 4.9; 2.0 C—37.2 6 5.8; 3-d-old larvae 0.0 C—31.0 6 4.6; 2.0 C—30.3 6 4.2; 6-d-old mature larvae 0.0 C—32.1 6 4.6; 2.0 C—31.1 6 4.6.
a
Corrected for natural mortality using Abbott’s formula (1925).
A trait of fruit fly is that multiple insects may reside in an individual fruit—described as a contagious distribution (Follett and
McQuate 2001). However, the fruit would receive a quarantine
treatment that would result in a mortality of >99.9% and the rare
survivors would have a random distribution within a shipment
(Baker et al. 1990). It is argued that for a contagious distribution the
Poisson distribution model may not be appropriate and that a negative distribution model is more applicable. However, for rare events
such as fruit fly in avocado, the predictions are similar (Follett and
McQuate 2001) and for either model the probability of finding one
or more mating pairs is given by
h
i
NFT 2
P¼ 1e 2
(Follett and McQuate 2001)
where N is the number of fruit in a shipment, F is the field infestation rate per fruit, and T is the pest survival rate after a postharvest
treatment (Liquido et al. 1995). NFT is the number of live insects after a postharvest treatment. De Graaf (2009) did not find any larvae
in his field survey of 16,883 fruit. For the purposes of this study, it is
assumed that 5 larvae were present in the 16,884 fruit surveyed.
This assumption has been made because although fruit flies have a
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0
3
5
7
9
11
0
3
5
7
9
11
Eggs
958
Journal of Economic Entomology, 2017, Vol. 110, No. 3
Table 4. Regression analysis of the survival of three life stages of C. capitata, C. rosa, and C. cosyra after various periods of cold treatment
Species
Egg
C
LT99.9 (d) (95% CL)
Regression (y ¼ mortality, x ¼ days)
P*
0.0
10.1 (9.9–10.4)
4.8 (4.7–4.9)
9.6 (9.4–9.9)
7.5 (7.3–7.7)
5.6 (5.4–5.8)
9.8 (9.6–10.0)
8.7 (8.5–8.9)
6.9 (6.7–7.1)
10.6 (10.3–10.9)
10.1 (9.9–10.3)
5.3 (5.1–5.4)
10.9 (10.7–11.3)
10.1 (9.9–10.4)
5.6 (5.4–5.8)
13.1 (12.8–13.4)
10.6 (10.4–10.9)
7.0 (6.8–7.2)
13.6 (13.3–14.0)
y ¼ 0.4842x-1.809
y ¼ 1.1079x-2.2453
y ¼ 0.5748x-2.4287
y ¼ 0.7041-2.1785
y ¼ 1.0650-2.86
y ¼ 0.5426-2.2207
y ¼ 0.8107x-3.926
y ¼ 0.7539x-2.126
y ¼ 0.4711x-1.8833
y ¼ 0.4884x-1.6416
y ¼ 0.9689x-2.0086
y ¼ 0.4782x-2.164
y ¼ 0.4989x-1.9622
y ¼ 0.9432x-2.1910
y ¼ 0.3932x-2.0571
y ¼ 0.5570x-2.8238
y ¼ 0.7188x-1.9371
y ¼ 0.3682x-1.9388
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
Three–day-old larvae (first and second instar)
Six-day-old larvae (third instar)
Egg
2.0
Three–day-old larvae (first and second instar)
Six–day-old larvae (third instar)
*P-value in the analysis of deviance <0.01 indicates there is a statistically significant relationship between the variables at a 99% confidence level.
Table 5. The number of live 6-d-old (third instar) C. cosyra larvae in avocado that had undergone treatment at 2.0 C for 18 or 20 d
Replicate
1 (18 d)
1 (20 d)
2 (20 d)
3 (20 d)
Control
Treated
Live larvae
No. of fruit
Mean no. of flies/fruit
No. of fruit
Estimated no. of larvae treated
No. of live larvae found
7,602
7,602
1,402
2,203
460
458
440
494
16.53
16.53
3.19
4.46
2,147
2,131
2,002
1,835
35,490
35,225
6,386
8,184
2
0
0
0
contagious distribution and egg packets laid by the fruit flies may
contain 15 or more eggs, there is a large natural attrition rate due to
encapsulation (Ware et al. 2016) and possible antibiosis. The five
larvae represent a field infestation rate of one larva from 3,367 fruit.
From the results of this study, the assumption is made that the
49,796 fruit sampled contained a living larva and indicates there is
at most a 0.0000201 survival. It is estimated that there are 84,840
avocados in a container (based on 16 fruit/4-kg carton and 264 cartons per pallet with 20 pallets per 12.2-m-long container). Assuming
a shipment of one container, the probability of one mating pair is
2.5 109.
An alternative approach that measures risk is recommended and entails calculating the probability of the pest establishing after importation
(Baker et al. 1990). For this study, it is assumed that a single C. cosyra
survives in 49,796 treated individuals (see Table 5), resulting in a treatment survival rate that is 0.0000201. Assuming a natural infestation
rate of 0.0000592 (one infested fruit from 16,883 [De Graaf 2009]) and
the number of fruit per container is 84,480 (De Graaf 2009) then the
probability of one mating pair per shipment is 2.5 10 9.
There was no natural infestation in 16,883 fruit assessed by De
Graaf (2009). Assuming for this study a single fruit was infested by
five larvae then the probability of one mating pair being present in
this consignment is 84.3%. This is derived from
P¼
1 x
X
k
1 21x expðkÞ
x!
x¼2
(Landolt et al. 1984)
¼ 1 þ expðkÞ – 2 exp ðk=2Þ
(Baker et al. 1990)
where k is the number of flies recovered.
This translates to 1 larva in 3,376 fruit harvested. From the
cold treatment results above, it was determined that there were no
survivors in 49,795 individuals that were subjected to treatment.
If it is assumed that a single fruit fly survived the treatment then to
isolate this fly 168,107,920 fruit would have to be harvested. A
12.2-m shipping container accommodates 84,480 fruit (20 pallets
made up of 264 cartons each containing 16 fruit [De Graaf
2009]); therefore, 1990 shipping containers would only contain
the single fruit fly. If one assumed that a single shipment is
500,000 fruit then there would be a single fly in one of the 336
ships. As we require at least two flies if a colony is to be established, the number of ships required for that level of infestation
would be double and then there is still only a 40% probability of
there being a mating pair.
These results can be viewed in another way: traditionally Probit
9 level of security (99.9968%) has been used for phytosanitary pest
and disease threats. Baker (1939) determined this to be not more
than 32 survivors out of a million—the true survival rate is less stringent at 136 survivors in 1,000,000 individuals (CL 95%) tested
(Couey and Chew 1986). If there is only a single surviving fly from
the 168,107,920 fruit harvested, then the Probit 9 level, assuming
32 flies in a million survive, indicate that the level of safety for C.
cosyra is oversubscribed by >5,253 times.
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C. capitata
C. rosa
C. cosyra
C. capitata
C. rosa
C. cosyra
C. capitata
C. rosa
C. cosyra
C. capitata
C. rosa
C. cosyra
C. capitata
C. rosa
C. cosyra
C. capitata
C. rosa
C. cosyra
Life stage
Journal of Economic Entomology, 2017, Vol. 110, No. 3
959
These conclusions are conservative, as they do not include additional elements of a systems approach that may entail the monitoring of fruit fly and the subsequent application of bait and chemical
sprays. The sanitation of the orchard through the removal and destruction of fallen fruit as well as packhouse inspection would further decrease the risk of fruit fly. It is concluded that the quarantine
risk of any Hass avocado consignment having undergone a cold
treatment of 2 C for 20 d poses a negligible risk of containing indigenous South African fruit fly species (C. ceratitis, C. rosa, and C.
cosyra).
Acknowledgments
References
Fig. 2. Average hourly temperature during large-scale disinfestation research
of C. cosyra. Average temperature (6 sd) for replicate 1 (18 d): 2.21 C 6
0.193; replicate 1: 1.87 C 6 0.271; replicate 2: 2.04 C 6 0.280; replicate 3:
1.916 C 6 0.1 (20 d).
Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide.
J. Econ. Entomol. 18: 265–267.
Baker, A. C. 1939. The basis for treatment of products where fruit flies are involved as a condition for entry into the United States. US Department of
Agriculture Circular No. 551.
Baker, R. T., M. Cowley, D. S. Harte, and E. R. Framton. 1990. Development
of a maximum pest limit for fruit flies (Diptera: Tephritidae) in produce imported into New Zealand. J. Econ. Entomol. 83: 13–17.
Brink, T., W. P. Steyn, and M. de Beer. 1997. Artificial exposure of different
avocado cultivars to fruit fly S. Afr. Avocado Growers’ Assoc. Yearb 20:
78–79.
Couey, H. M., and V. Chew. 1986. Confidence limits and sample size in quarantine research. J. Econ. Entomol. 85: 312–317.
De Graaf, J. 2009. Host status of avocado Hass to Ceratitis capitata, Ceratitus
rosa, and Ceratitis cosyra (Diptera: Tephritidae) in South Africa. J. Econ.
Entomol. 102: 1448–1459.
De Lima, C.P.F. 1995. Determination of host status of hard avocados to
Mediterranean fruit fly. New Zealand Ministry of Agriculture and Forestry,
Wellington, New Zealand.
De Villiers, E. A. 2001. The cultivation of avocado. Agricultural Research
Council, Institute for Tropical and Subtropical Crops (ARC-ITSC),
Nelspruit, South Africa.
Du Toit, W. J., and A. Tuffin. 1980. The role of fruit flies on avocado early in
the season. S. Afr. Avocado Growers’ Assoc. Yearb 4: 86–87.
Follett, P. A., and G. T. McQuate. 2001. Accelerated development of quarantine treatments for insects on poor hosts. J. Econ. Entomol. 94: 1005–1011.
Grové, T. 2001. Fruit flies, pp 276–278. In E.A. D. V.(ed). The Cultivation of
Avocado. ARC-Institute for Tropical and Subtropical Crops, Nelspruit,
South Africa.
Grové, T., M.S., De Beer, S. Dreyer, and W. P. Steyn. 1998. Monitoring fruit
flies in avocado orchards. S. Afr. Avocado Growers’ Assoc. Y Book 21:
80–82.
Heather, N. W., and G. T. Hallman. 2008. Pest management and phytosanitary trade barriers. CAB International, Wallingford, United Kingdom.
(IPPC) International Plant Protection Convention. 2013. Status of Bactrocera
invadens in Limpopo and Mpumalanga Province, South Africa. (https://
www.ippc.int/static/media/files/pestreport/2013/07/10/1337323587_eradica
tion_of_bactrocera_invade_201304232117en.docx) (accessed 3 March 2017).
Jones, S. R. 1989. Morphology and evolution of the aculei of true fruit flies
(Diptera: Tephritidae) and their relationship with host anatomy. Ph.D. dissertation, The Pennsylvaia State University, University Park.
Kamali, A. R., E. Maxie, and H. L. Rae. 1972. Effect of gamma irradiation on
‘Fuerte’ avocado fruits. Hort. Sci. 4: 125–126.
Kay, E., and W. Schroeder. 1963. Seasonal regeneration of avocado fruit tissue. Proc. Am. Soc. Hort. Sci. 83: 287–390.
Downloaded from https://academic.oup.com/jee/article/110/3/954/3746969 by guest on 13 June 2022
The South African Growers’ Association funded the research. Johan de Graaf
and Derik Donkin are thanked for their constructive comments.
960
complex (Diptera: Tephritidae): Taxonomic changes based on a review of
20 years on integrative morphological, molecular, behavioral and chemoecolological data. Syst. Entomol. 40: 456–471.
Smith, D. 1973. Insect pests of avocados. Qld. Agric. J. 99: 645–653.
(USDA-APHIS) U.S. Department of Agriculture – Animal and Plant Health
Inspection Service 2016. U.S. Department of Agriculture – Animal and Plant
Health Inspection Service Treatment Manual.
Ware, A. B., 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. 195: 1963–1970.
Ware, A. B., L. N. Du Toit, E. Du Toit, R. Collins, R. Clowes, S. Ekesi, and S.
A. Mohammed. 2016. Host suitability of three avocado cultivars (Persea
americana Miller: Lauraceae) to oriental fruit fly (Bactrocera (invadens)
dorsalis (Hendel) (Diptera: Tephritidae). Crop Prot. 90: 84–89.
Willink, E., and M. E. Villagran. 2007. Evaluation of quarantine risk of the introduction of Ceratitis capitata in ‘Hass’ avocado from Argentina. In:
Proceedings of the VI World Avocado Congress, 12-16 Nov. 2007, Vina
Del Mar, Chile. (http://www.avocadosource.com/WAC6/en/Extenso/2a58.pdf)
Zauberman, G., M. Schiffman-Nadel, and U. Yonko. 1977. The response of
avocado fruit to different temperatures. Hort. Sci. 12: 353–354.
Downloaded from https://academic.oup.com/jee/article/110/3/954/3746969 by guest on 13 June 2022
Kok, R. D., P. Bower, and I. Bertling. 2010. Low temperature shipping and
cold chain management of "Hass" avocados: An opportunity to reduce shipping costs. S. Afr. Avocado Growers’ Assoc. Year Book. 33: 33–37.
Landolt, P. J., L. Chambers, and V. Chew. 1984. Alternative to the use of
Probit 9 mortality as a criterion for quarantine treatments of the fruit fly
(Diptera: Tephritidae) infested fruits. J. Econ. Entomol. 77: 285–287.
Liquido, N. J., T. Chan, and G. T. McQuate. 1995. Hawaiian tephritid fruit
flies (Diptera): Integrity of the infestation-free quarantine procedure for
‘Sharwil’ avocado. J. Econ. Entomol. 88: 85–96.
Newett, S.D.E., H. Crone, and G. Delhove. 2002. Cultivars and rootstocks. In A.
W. Whiley, B. Schaffer, and B.N. Wolstenholme (eds.), The Avocado, Botany,
Production and Uses. CAB International, Wallingham, United Kingdom.
Mwatawala, M. W., M. De Meyer, R. H. Makundi, and A. P. Maerere. 2006.
Seasonality and host utilization of the invasive fruit fly, Bactrocera invadens
(Diptera: Tephritidae) in central Tanzania. J. Appl. Entomol. 130: 530–537.
Oi, D. H., and R.F.L. Mau. 1989. Relationship of fruit ripeness to infestation
in ‘Sharwil’ avocados by the Mediterranean fruit fly and the Oriental fruit
fly (Diptera: Tephrididae). J. Econ. Entomol. 22: 453–458.
Schutze, M. K., N. Aketarawong, W. Amornsak, K. F. Armstrong, A. A.
Augustinos, V. J. Barr, W. Bo, K. Borrtzis, L. M. Boycin, C. C
aceres, et al.
2015. Synonymization of key pest species with Bactrocera dorsalis species
Journal of Economic Entomology, 2017, Vol. 110, No. 3