Host Suitability Index for Polyphagous Tephritid Fruit Flies
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Journal of Economic Entomology, XX(XX), 2021, 1–14
doi: 10.1093/jee/toab035
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Host Suitability Index for Polyphagous Tephritid Fruit Flies
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Peter A. Follett,1,3, Fay E. M. Haynes,2 and Bernard C. Dominiak2,
1
USDA ARS, Daniel K. Inouye U.S. Pacific Basin Agricultural Research Center, 64 Nowelo Street, Hilo, HI 96785, USA, 2NSW
Department of Primary Industries, The Ian Armstrong Building, 105 Prince Street, Orange, NSW 2800, Australia, and 3Corresponding
author, e-mail: peter.follett@usda.gov
Subject Editor: Lisa Neven
Received 12 December 2020; Editorial decision 1 February 2021
Abstract
Tephritid fruit flies are major economic pests for fruit production and are an impediment to international trade.
Different host fruits are known to vary in their suitability for fruit flies to complete their life cycle. Currently,
international regulatory standards that define the likely legal host status for tephritid fruit flies categorize fruits
as a natural host, a conditional host, or a nonhost. For those fruits that are natural or conditional hosts, infest-
ation rate can vary as a spectrum ranging from highly attractive fruits supporting large numbers of fruit flies
to very poor hosts supporting low numbers. Here, we propose a Host Suitability Index (HSI), which divides
the host status of natural and conditional hosts into five categories based on the log infestation rate (number
of flies per kilogram of fruit) ranging from very poor (100). Infestation rates may be determined by field sampling or cage infestation
studies. We illustrate the concept of this index using 21 papers that examine the host status of fruits in five
species of polyphagous fruit flies in the Pacific region: Bactrocera tryoni Froggatt, Bactrocera dorsalis (Hendel),
Bactrocera latifrons (Hendel), Zeugodacus cucurbitae (Coquillett), and Ceratitis capitata (Wiedemann) (Diptera:
Tephritidae). This general-purpose index may be useful in developing systems approaches that rely on poor
host status, for determining surveillance and detection protocols for potential incursions, and to guide the ap-
propriate regulatory response during fruit fly outbreaks.
Key words: host status, Tephritidae, quarantine, phytosanitary, nonhost
Increased international trade and expanded travel have led to more Hennessey 2007, Aluja and Mangan 2008). However, in some cases,
frequent incursions of invasive plant pests. Fruit flies in the family the host status of the fruit for a particular fruit fly may be unknown
Tephritidae are among the most important invasive crop pests world- or poorly studied (Follett et al. 2019a).
wide because of their potential for direct economic damage and the Hosts for fruit flies are plants (fruits or vegetables) on which flies are
stringent quarantine restrictions imposed by many countries to pre- able to lay eggs and complete their whole life cycle through to emer-
vent their entry. When incursions of tephritid fruit flies are detected, gence of adults of the next generation (Armstrong 1994). Any plants
they typically trigger regulatory efforts to prevent establishment or that do not allow flies to produce viable adult offspring are, therefore,
eradicate incipient populations. Detections of an invasive fruit fly in by definition, a nonhost. Plants that are unsuitable for a species’ re-
a new country or region can disrupt both domestic and international production typically have some traits that either prevent oviposition or
trade in fresh commodities that are classified by quarantine author- suppress growth of the immature stages (Painter 1951). For most fruit
ities as potential hosts of the invasive species (Follett and Neven flies, however, the exact mechanisms or traits that prevent host use are
2006). The actual risk, however, that is posed by a particular fruit unknown or poorly understood (Aluja and Mangan 2008). Fruits or
fly will be affected by the suitability of the commodity as a host for vegetables that are nonhosts pose no threat of supporting invasion of
the fruit fly and the fly’s level of polyphagy. If a commodity is well a fruit fly unable to reproduce in such a nonhost, and those fruits can
known as a field host of a particular fruit fly, quarantine restrictions be safely imported without any special quarantine measures. A com-
on potentially infested commodities (e.g., fruit and vegetables, here- mercial fruit may be unsuitable for a fruit fly in some of its growth
after ‘fruit’) are well justified during a fruit fly incursion (Follett and stages, but suitable in others, and within a fruit or vegetable species,
Published by Oxford University Press on behalf of Entomological Society of America 2021. 1
This work is written by (a) US Government employee(s) and is in the public domain in the US.
2 Journal of Economic Entomology, 2021, Vol. XX, No. XX
some varieties may be suitable hosts while others may be nonhosts detect infested fruits in the field or laboratory or field trials in which
(Armstrong 1994, Greany 1994). Host plant resistance, regardless of fruits are directly exposed to the target fruit fly.
what plant stage it occurs in, may affect one of the fruit fly’s life stages Cowley et al. (1992) proposed determining host status based on
or several of them. To complete its whole life cycle on a fruit or vege- a three-tiered testing protocol and decision tree: 1) laboratory cage
table, a fruit fly must first find the plant and accept it for egg laying. tests with punctured fruit, 2) laboratory cage tests with unpunctured
The eggs must hatch, and the resultant larvae survive and develop on fruit, and 3) field cage tests with unpunctured fruit attached to the
the tissues of the fruit or vegetable, reach maturity, and give rise to tree. The most crucial test is a no-choice laboratory cage trial where
healthy, sexually competent adults (Prokopy and Owens 1983, Aluja the fruit is exposed to gravid female flies and subsequently held to
and Mangan 2008). allow any eggs to develop through to the adult stage. The recom-
The International Plant Protection Convention (IPPC) has pub- mended design is to expose a single ripe fruit for 24 h to 50 gravid
lished a standard with guidelines for the determination of the host flies in 30- × 30- × 30-cm cages, replicated five times. If no adults
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status of a particular fruit to a given fruit fly in its International are produced from this replicated laboratory cage test, it is con-
Standards for Phytosanitary Treatments (ISPM) 37 entitled cluded that the fruit is a nonhost. (Preferred host fruit are typic-
‘Determination of host status of fruit to fruit flies’. This standard ally tested separately as controls to demonstrate that the gravid flies
describes three categories for fruits as potential hosts for fruit flies: are physiologically and behaviorally ready to lay eggs.) If adults are
natural host, conditional host, and nonhost. The standard also de- produced from the target fruit, further testing in the field, such as
scribes experimental procedures for placing a fruit into one of these the use of surveillance trapping or field cage exposures, is recom-
categories for a given fruit fly (Food and Agriculture Organization mended (Cowley et al. 1992). Many studies on host status have been
[FAO] 2006). A natural host is defined as a plant species or cultivar conducted using this laboratory cage approach as per Cowley et al.
that has been scientifically found to be infested by the target fruit (1992). For example, Lloyd et al. (2013) conducted no-choice la-
fly species under natural conditions and is able to sustain the fly’s boratory cage tests with 22 citrus and non-citrus fruit hosts with
development through to the emergence of viable adult flies. A con- Bactrocera tryoni (Froggatt) (Queensland fruit fly) and ranked the
ditional host is one not known to occur in nature, but which has susceptibility of hosts using a host susceptibility index, defined as the
been found by scientific tests to support infestation by the fruit fly number of adult flies produced per gram of fruit infested at the rate
of interest (with development to the adult stage) under semi-natural of one egg per gram of fruit.
field conditions, such as field cages, greenhouses, or in caged or The international standard ISPM 37 (FAO 2006) was developed
bagged branches bearing fruit. A nonhost is a fruit that has never after the publication of Cowley et al. (1992) and focuses on field ra-
been observed to be naturally infested and does not sustain develop- ther than laboratory testing to determine host status under natural
ment under natural or semi-natural conditions. or semi-natural conditions. The premise of this newer approach is
While the above categories seem clearly separated, in fact, host that laboratory tests with fruit exposed to fruit flies in a confined
suitability for natural and conditional hosts under natural or semi- space and high fly pressure is appropriate for demonstrating nonhost
natural conditions for most polyphagous fruit flies is better de- status but may be inappropriate for demonstrating natural or con-
scribed as a spectrum of host quality, ranging from highly attractive ditional host status. Specifically, artificial conditions in the labora-
fruit that support the development of many individuals to marginal tory such as the use of harvested fruit that continues to ripen may
hosts that support only a few. Given this range of acceptableness in lead to greater fruit susceptibility to fruit flies than occurs in nature.
nature, we feel that a more comprehensive quantitative description The most reliable confirmation of natural host status comes from
of host status categories of natural and conditional hosts would be tree sampling during the harvest period and observation of natural
useful in support of effective but not overly restrictive phytosanitary infestation and development to viable adults in fruit. If no natural
or quarantine measures, thus promoting both environmental safety infestation is observed, trials are then run based on the introduction
and trade. This more nuanced approach should be useful in the de- of flies in field cages, greenhouses, or bagged fruit-bearing branches
velopment of quarantine systems and effective treatments, and in the at the optimal maturity stage. These trials represent semi-natural
design of regulatory responses to fruit fly incursions. conditions that may adequately reflect the natural process of infest-
Here, we propose a method of host ranking called the Host ation and positive results indicate that a fruit is a conditional host.
Suitability Index (HSI) as an adjunct to ISPM 37. This index categor- ISPM 37 does not specify the number of fruit flies or duration of
izes fruits into groupings that better distinguish the degree to which fruit exposures under semi-natural conditions. ISPM 37 also does
a fruit is either more or less likely to support the tephritid life cycle, not address the case where the distribution of a fruit fly and a po-
from oviposition through development. To illustrate the use and po- tential fruit host currently do not overlap, preventing any type of
tential value of the approach, we discuss the application of the HSI field study.
to several polyphagous tephritid fruit flies from the Pacific region. Bellamy et al. (2013) reviewed the literature on host status in-
dices and developed a Host Potential Index (HPI) using Drosophila
suzukii (Matsumura) as a model insect. The HPI calculated index
values by host ranking and statistical weighting across choice and
Host Status Determination no-choice studies of host selection, oviposition, and physiological
Determining the likely host status of a fruit for a particular fruit fly development to characterize postharvest host status. The HPI was
is an important part of pest risk analysis, and such determinations elegant but quantitatively complex and data intensive, and the re-
are typically required before permitting shipment of a new fruit in sulting index values were nonintuitive. For example, the fruit host
international trade. When host status is uncertain, a combination of with the highest potential for D. suzukii, raspberry, had an HPI value
historical evidence, pest interception records, and scientific literature of 350.6 and the host with the lowest potential, grapes, had an HPI
can be used to make the determination. If historical records and pub- value of 248.3. Although the HPI value for grapes is lower than rasp-
lished reports are deemed unreliable or insufficient, additional la- berries, the relatively high number for grapes might suggest to those
boratory and field trials may be required. Various research methods not familiar with the calculation methods that this fruit still supports
have been proposed to determine host status either from surveys to development of many flies.
Journal of Economic Entomology, 2021, Vol. XX, No. XX 3
We propose a simpler, more intuitive index for ranking of host
status of natural or conditional hosts that focuses on the number of
fruit flies that infest and develop within a fruit. A HSI divides the
suitability of a host to become infested into five categories based on
the log numbers of flies that infest or emerge from fruit during host
sampling or testing, and the score attaches an adjective to each cat-
egory that reflects the relative importance of infestation at each level
(Table 1). HSI is presented on a per weight basis (number of fruit
flies per kilogram) to account for different fruit sizes and weights.
This index is based in the fact that host suitability is a continuum
and assumes that polyphagous tephritid fruit flies generally have a
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reproductive capacity of at least 10 eggs per female per day or more,
which seems to be the case for many economically important spe-
cies (Vargas et al. 1984, Carey et al. 1986, Foote and Carey 1987,
Prokopy and Fletcher 1987, Vargas and Carey 1989, CABI/EPPO
1997). At one end of the continuum is a host fruit that may be highly
attractive and yield large numbers of adults with minimal mortality
during development; at the other end is a marginally attractive
and rarely infested host that does not elicit strong oviposition be-
havior or causes high mortality during development. For tephritid
fruit flies that are more host specific, such as Bactrocera minax
(Enderlein) (Citrus spp.), Bactrocera oleae (Rossi) (olive, Olea spp.),
and Rhagoletis indifferens Curran (cherry), HSI may be useful in
describing the host status of fruit cultivars.
Many host-status studies have adopted the no-choice laboratory
cage methods of Cowley et al. (1992), which allows comparisons
across fruit fly species and fruit types. For the HSI, we propose using
basic methods from Cowley et al. (1992) and ISPM 37, including
laboratory cage tests (using harvested fruit; Fig. 1) or screened field
cage tests (using fruit on the tree; Fig. 2). Sleeve cage tests can be Fig. 1. No-choice cage tests with apples exposed to wild strains (F3) of
particularly useful for climacteric fruit that ripen after harvest and Bactrocera dorsalis, Ceratitis capitata, and Zeugodacus cucurbitae. Cage
in doing so become better hosts (Follett 2009). In both cases, indi- tests were conducted in an open-sided greenhouse to provide natural light
vidual fruit are exposed to 50 gravid females for 24 h. Cowley et al. and temperature conditions.
(1992) recommended placing fruit in 30- × 30- × 30-cm cages, but
similar laboratory or sleeve cages sizes would be appropriate. Tests extent that data were available, the HSI was applied to different life
with individual fruit should be replicated a minimum of five times stages for these species including adults (Table 2; 93 fruit by fruit fly
but higher replication is desirable as fruit infestation rates can be combinations), pupae (Table 3; 87 fruit by fruit fly combinations),
highly variable. Small fruit (e.g., cherries, blueberries, grapes) may and third-instar larvae (Table 4; 17 fruit by fruit fly combinations).
be exposed as multiple fruit for a minimum weight of 100 g. Wider By definition, emergence of adult flies is needed for a fruit to be a
adoption of these methods as a standard would provide a common host, but information on larval infestation and pupal emergence are
language for quantifying and discussing host status. Field surveys presented for the purpose of comparison. The studies included both
can provide supplementary information. no-choice host testing of fruit in laboratory cages and field surveys of
harvest mature fruit from the tree for fruit fly infestations. Data are
organized into columns for field versus laboratory (intact or punc-
HSI for Pacific Area Fruit Flies tured fruit) results, and all fruit infestation results are standardized
We illustrate the HSI concept using 21 papers on the host usage on individuals per kilogram of fruit weight basis. Several studies did
of five economically important, invasive, polyphagous fruit flies in not report fruit weights, so the infestation rate per kilogram of fruit
the Pacific Region: Bactrocera tryoni, Bactrocera dorsalis (Hendel), and the resulting HSI category were estimated using average fruit
Bactrocera latifrons (Hendel), Zeugodacus cucurbitae (Coquillett), weights from the literature. HSI rankings are based on infestation
and Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). To the data from the field if available or from laboratory trials with intact
fruit (no damage, punctures, or blemishes) or both. The laboratory
studies used to develop the HSI mostly used the experimental pro-
Table 1. Proposed Host Suitability Index (HSI) with categories
cedures proposed by Cowley et al. (1992), with minor variations
based on log numbers of fruit flies emerging per kilogram of fruit
such as the number of gravid flies used in trials (Follett et al. 2019a).
Infestation rate (number of fruit flies All the fruit fly species in the reviewed studies were classified
per kilogram of fruit) Category as polyphagous, but infestation levels differed by fruit species and
host variety (see Table 2 for fruit scientific names). For example, the
100.1 Very good and this two-log difference in numbers would result in a two-level
difference in HSI categorizations of moderately good (MG) versus4 Journal of Economic Entomology, 2021, Vol. XX, No. XX
consistent across studies. For example, field-collected guava, loquat,
and pear were good or very good hosts for B. tryoni, whereas lemon
was a moderately good host in studies by both Lloyd et al. (2013)
and Dominiak et al. (2020) (Table 2).
In about 70% of cases, puncturing fruit increased host suscepti-
bility of test fruit in laboratory cage studies, sometimes significantly
(Tables 2 and 3). For example, intact ‘Red Globe’ grapes produced
three adult B. tryoni per kilogram (MG, a moderately good host),
whereas punctured fruit produced 30 adult flies per kilogram (G, a
good host) (Jessup et al. 1998). Intact Navel orange was a nonhost
for Z. cucurbitae, but punctured fruit were a moderately good
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host (McQuate et al. 2015). Higher infestation rates in damaged
fruit compared with sound fruit is a common observation in host
status studies that examine culls (Armstrong 1983, 1991, 2001).
Puncturing is a well-known and often used method to increase la-
boratory infestation of host fruit during development of quarantine
treatments (Cowley et al. 1992, De Lima et al. 2007).
Infestation data from third-instar larvae, pupae, or adults may
provide equally good indicators of host status (Tables 2–4), although
few host status studies have reported infestation rates of all three life
stages for comparison. The general rule of thumb from laboratory
rearing of fruit flies on diet is about 10% mortality between life
stages. For B. tryoni on diet, the mortality rate was approximately
15% between pupa and adult (Fanson et al. 2014). At this level of
stage-to-stage mortality, host categorization using the HSI will not be
affected significantly by measuring third instars or pupae or adults.
However, stage-specific mortality may be inherently higher in certain
species, and mortality in fruit can be significantly higher than in diet,
particularly for poor hosts (Rengifo et al. 2011, Muthuthantri and
Fig. 2. Sleeve cage test showing a ‘Malama’ avocado on the tree with 50
Clarke 2012, Follett et al. 2019a,b). For example, in a no-choice
gravid Bactrocera dorsalis added for 24 h. study by Rengifo et al. (2011), C. capitata laid 1,723 eggs per kilo-
gram in passion fruit, but only 3.9 larvae (HSI = MG, a moder-
very good (VG), respectively (Table 1). For C. capitata, in labora- ately god host), 0.36 pupae (HSI = P, a poor host) and 0.0 adults (a
tory cage studies, intact ‘Gold’ kiwifruit produced 0 adult offspring nonhost) per kilogram of fruit developed successfully. In this case,
(nonhost) and punctured fruit produced an average of 6.9 adults off- the sheer numbers of eggs laid under cage conditions biased the HSI
spring per kilogram (HSI = a moderately good host), whereas intact rating upward, making passion fruit appear to be a moderately good
‘Green” kiwifruit produced an average of 2.9 adults per kilogram host (from larvae) or poor host (from pupae) for C. capitata when
(HSI = MG, a moderately good host) and punctured fruit produced it is indeed a nonhost (from adults). For all hosts but especially for
an average of 32 adult offspring per kilogram (HSI = G, a good host) poor hosts, adults emerging from the fruit are ultimately the best in-
(Table 2). In the same study, intact papaya produced 246–514 adult dicator of true host status.
offspring and punctured fruit produced 387–560 adult offspring per Further research is needed to validate the categories of HSI for
kilogram (both HSI = VG, a very good host) (Table 2). In the prac- more fruit fly species and their fruit hosts. The HSI evaluates a fruit’s
tical application of an HSI, a very poor or poor host may not need infestation potential only in terms of number of individuals produced
to be treated or managed in the same way as a good or very good and does not include other performance measures that may be useful
host in terms of the severity of a quarantine treatment or regulatory for evaluating host suitability and fitness (Bellamy et al. 2013). For
response to an incursion to achieve the same reduction in risk. example, the weight of pupae is positively correlated with the size
In several cases, information was collected from both field and of resulting adult flies and adult fitness (FAO/IAEA/USDA 2019). In
laboratory studies. HSI values from field exposures cannot be com- B. dorsalis, Z. cucurbitae, and C. capitata reared from kiwifruit and
pared directly with those from laboratory trials because field expos- apple, the weight of puparia was approximately 50% of the weight
ures were for a longer duration and to an unknown number of flies, of puparia reared from papaya (Follett et al. 2019 a,b), suggesting
but the relative number of flies infesting different fruit hosts can be these fruits are suboptimal developmental hosts, and therefore the
compared for each type of study. In general, predictions from la- fitness (e.g., mating competitiveness, fecundity, longevity) of adult
boratory host status studies were consistent with field observations. flies emerging from these hosts may be reduced. Likewise, the pu-
For B. dorsalis, only 1.3 adult flies per kilogram were reared from paria of C. capitata reared on passion fruit weighed about only 25%
intact ‘Green’ kiwifruit after laboratory no-choice cage exposure as much as puparia that were reared on mango (Rengifo et al. 2011).
(Table 2) and no adults were reared from ‘Green’ kiwifruit placed
in the field for 1 wk (Follett 2019a). For B. tryoni, in both labora-
tory cage tests and in field-collected fruit, ‘Murcott’ mandarins were
Case Studies: Host Fruit Resistance Patterns in
more suitable hosts than either ‘Imperial’ or ‘Ellendale’ mandarins, B. tryoni and B. dorsalis
and all mandarin varieties were more suitable hosts than ‘Eureka’ Some fruits are intrinsically less suitable as hosts and support lower
lemons (Table 2) (Lloyd et al. 2013). HSI categorizations were also numbers of fruit flies. Such poor hosts should not require the sameTable 2. Host Suitability Index (HSI) ranking of fruit hosts based on reports of adult flies emerging from fruit from tree sampling in the field or laboratory cage tests
Average number of fruit fly adults per kilogram of fruit
Laboratory
Host In field Intact Punctured Reference Category
Bactrocera dorsalis (Oriental fruit fly)
Actinidia chinensis, kiwifruit ‘Green’ 0 1.3 30 Follett et al. (2019a) NH/MG
Solanum torvum, turkey berry 4 McQuate (2008) MG
Vaccinium reticulatum, ohelo 5 Follett and Zee (2011) MG
Mangifera casturi, Kalimantan mango 9 McQuate et al. (2017) MG
Solanum torvum, turkey berry 10 McQuate (2008) MG
Actinidia chinensis, kiwifruit ‘Gold’ 15 7 36 Follett et al. (2019a) G/MG
Malus × domestica, apples ‘Jazz’ 0 26 41 Follett et al. (2019b) NH/G
Carica papaya, papaya 11.5 131 315 Follett et al. (2019b) G/VG
Hylocereus undatus, dragon fruit 16 McQuate (2010) G
Mangifera lalijiwa, mango 87 McQuate et al. (2017) G
Carica papaya, papaya 142 500.8 625 Follett et al. (2019a) VG
Bactrocera latifrons (Solanum fruit fly)
Citrus sinensis, orange Naval 0.06 2.06 McQuate et al. (2015) VP
Journal of Economic Entomology, 2021, Vol. XX, No. XX
Citrus reticulata, clementine tangerine 0.51 0.39 McQuate et al. (2015) P
Carica papaya, papaya 276 McQuate et al. (2015) VG
Capsicum annuum, pepper Anaheim 285 McQuate et al. (2015) VG
Solanum torvum, turkey berry 316 McQuate (2008) VG
Solanum melongena, eggplant 389 McQuate et al. (2015) VG
Bactrocera tryoni (Queensland fruit fly)
Solanum lycopersicon, tomato 0.5 Dominiak et al. (2020) P
Vitis vinifera, grapes ‘Red Emperor’ 2 0.4 Jessup et al. (1998) MG
Vitis vinifera, grapes ‘Calmeria’ 2 2 Jessup et al. (1998) MG
Vitis vinifera, grapes ‘Red Globe’ 3 30 Jessup et al. 1998) MG
Citrus limon, lemon ‘Lisbon’ 3 Dominiak et al. (2020) MG
Punica granatum, pomegranate 4 Dominiak et al. (2020) MG
Mangifera indica, mango 4 Dominiak et al. (2020) MG
Citrus reticulata, ‘Murcott’ mandarin 4 83 Lloyd et al. (2013) MG/G
Averrhoa carambola, carambola 4 Lloyd et al. (2013) MG
Citrus × paradisi, grapefruit 5 Dominiak et al. (2020) MG
Diospyros kaki, persimmon 5 Lloyd et al. (2013) MG
Citrus limon, lemon 5 2 Lloyd et al. (2013) MG
Opuntia sp., prickly pear 6 Dominiak et al. (2020) MG
Vitis vinifera, grapes ‘Flame Seedless’ 8 138 Jessup et al. (1998) MG
Prunus avium, cherry 9 Dominiak et al. (2020) MG
Citrus sinensis, orange Valencia 10 8 Lloyd et al. (2013) MG
Ficus carica, edible fig 10 Lloyd et al. (2013 MG
Malus domestica, apple 12 Dominiak et al. (2020) G
Juglans regia, walnut 14 Dominiak et al. (2020) G
Mangifera indica, mango 15 Lloyd et al. (2013) G
Citrus paradise, grapefruit 17 Lloyd et al. (2013) G
5
Persea americana, avocado 22 Lloyd et al. (2013) G
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Table 2. Continued
Average number of fruit fly adults per kilogram of fruit
Laboratory
Host In field Intact Punctured Reference Category
Capsicum annum, capsicum 24 Dominiak et al. (2020) G
Fortunella japonica, kumquat 25 Lloyd et al. (2013) G
Citrus reticulate, mandarin Ellendale 26 20 Lloyd et al. (2013) G
Annona reticulata, custard apple 26 Dominiak et al. (2020) G
Syzygium paniculatum, magenta brush cherry 27 Lloyd et al. (2013) G
Olea europaea, olives 33 Dominiak et al. (2019) G
Phoenix dactyifera, date palm 34 Lloyd et al. (2013) G
Vitis vinifera, grapes ‘Thompson Seedless’ 35 12 Jessup et al. (1998) G
Rosa sp., rose hips 40 Dominiak et al. (2018) G
Thevetia peruviana, yellow oleander 43 Lloyd et al. (2013) G
Citrus reticulata, mandarin 43 Dominiak et al. (2020) G
Acca sellowiana, Burret, Feijoa 46 Dominiak et al. (2020) G
Vitis vinifera, grapes ‘Menindee Seedless’ 50 79 Jessup et al. (1998) G
Malus domestica, apple 54 Lloyd et al. 2013) G
Pyrus communis, pear 56 Dominiak et al. (2020) G
Cydonia oblonga, quince 63 Dominiak et al. (2020) G
Prunus armeniaca, apricot 63 Dominiak et al. (2020) G
Pyrus pyrifolia, Nashi pear 73 Dominiak et al. (2020) G
Psidium guajava, guava 92 Dominiak et al. (2020) G
Pyrus communis, pear 111 Lloyd et al. (2013) VG
Citrus sinensis, orange 142 Dominiak et al. (2020) VG
Eribotrya japonica, loquat 148 Lloyd et al. (2013) VG
Prunus persica var. mucipersica, nectarine 176 Dominiak et al. (2020) VG
Prunus persica, peach 179 Dominiak et al. (2020) VG
Morus nigra, mulberry 209 Lloyd et al. (2013) VG
Psidium littorale, cherry guava 226 Lloyd et al. (2013) VG
Citrus japonica, kumquat 234 Dominiak et al. (2020) VG
Citrus aurantium, orange Seville 237 Lloyd et al. (2013) VG
Psidium guajava, guava 318 Lloyd et al. (2013) VG
Eribotrya japonica, loquat 324 Dominiak et al. (2020) VG
Diplocyclos palmatus, striped cucumber 406 Lloyd et al. (2013) VG
Ceratitis capitata (Mediterranean fruit fly)
Passiflora edulis, passion fruit 0 Rengifo et al. (2011) NH
Actinidia chinensis, kiwifruit ‘Gold’ 0 6 Follett et al. (2019a) NH
Actinidia chinensis, kiwi fruit ‘Green’ 3 32 Follett et al. (2019a) MG
Malus × domestica, apples ‘Jazz’ 14 25 Follett et al. (2019b) G
Carica papaya, papaya 246 560 Follett et al. (2019a) VG
Solanum torvum, turkey berry 250 McQuate (2008) VG
Carica papaya, papaya 514 387 Follett et al. (2019b) VG
Zeugodacus cucurbitae (melon fly)
Sicyos lasiocephalus, feral melon 0 Uchida et al. (1990) NH
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level of treatment (pre- and/or postharvest) or regulatory response
G = good host; MG = moderately good host; NH = nonhost; P = poor host; VG = very good host; VP = very poor host. Hosts are listed for each species in ascending order of infestation rate. HSI rankings were assigned from
Category
NH/MG
as hosts that can support high numbers of fruit flies (Bateman 1991,
G/VG
MG
NH
NH
NH
Jessup et al. 2007). Host susceptibility may be influenced during ovi-
VG
VG
VG
VG
VG
VG
G
G
position by characteristics such as fruit size, peel toughness and Brix
level (Muthuthantri and Clarke 2012), the stage of fruit maturity, or
the abundance of alternative host fruit in the environment (Clarke
et al. 2011). Bactrocera tryoni and B. dorsalis are discussed below
to illustrate the diversity in host fruit use.
Bactrocera tryoni
McQuate et al. (2015)
McQuate et al. (2015)
McQuate et al. (2015)
Jackson et al. (2003)
Follett et al. (2019b)
Follett et al. (2019b)
Follett et al. (2019a)
Follett et al. (2019a)
Follett et al. (2019a)
Uchida et al. (1990)
Uchida et al. (1990)
Uchida et al. (1990)
Uchida et al. (1990)
Based on a review of historical records and databases, B. tryoni is
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McQuate (2010)
believed to infest 117 hosts from 49 plant families (Hancock et al.
2000). As is often the case, some historical records are dubious,
Reference
and a fruit may have been classified as a host in one report but a
nonhost in another (Hancock et al., 2000), with no gradation within
the host category to acknowledge the fruit’s capacity to support
the fly’s life cycle. Also, many occasional or marginal hosts may be
attacked when B. tryoni populations are high (Clarke et al. 2011).
Within Citrus, lemon was the least preferred host for B. tryoni,
‘Murcott’ mandarins and grapefruit were the most preferred, and
Navel and Valencia oranges were intermediate (Muthuthantri and
Clarke 2012). Citrus peel toughness was negatively correlated with
Punctured
B. tryoni oviposition preference (Muthuthantri and Clarke 2012). In
168
432
595
0.4
25
6
5
tests combining preference and performance, Balagawi et al. (2013)
observed that the oviposition preference of B. tryoni did not vary
across fruit host families, but overall fitness did. Bactrocera tryoni
Laboratory
eggs had low survivorship in grapes, but if eggs did hatch, larvae
had a much higher survival rate (Dominiak 2011). Bactrocera tryoni
can complete its life cycle in rose hips (Rosa sp.) but field infestation
may only be a late season occurrence when many other hosts are not
available (Dominiak et al. 2018). If B. tryoni population densities
307,310
become high, even nonhost fruits may be infested in the field, al-
Intact
285
315
515
0
0
2
2
though B. tryoni would not complete its life cycle on such nonhosts
(Dominiak 2011). For tephritids in general, including B. tryoni, the
capacity to successfully penetrate the skin during oviposition is a key
factor in host fruit resistance. For example, relatively thin-skinned
tomato varieties ‘Grosse Lisse’ and ‘Roma’ were very good hosts for
B. tryoni, whereas the thicker-skinned cherry tomato cultivars were
much less infested (Balagawi et al. 2005). No differences were found
in oviposition behavior or numbers of eggs laid when apples, plums,
In field
109
254
272
564
field sampling and laboratory trials with intact fruit, only (not punctured fruit).
15
81
12
and pears (Rosaceae) were exposed to B. tryoni in no-choice tests,
0
0
0
but B. tryoni ignored pear altogether when exposed to these three
hosts in a choice test, indicating how no-choice tests may overesti-
mate the ability of flies to infest fruit species (Balagawi et al. 2013).
Average number of fruit fly adults per kilogram of fruit
Bactrocera dorsalis
Bactrocera dorsalis has a wide range of fruit crop hosts and prob-
ably also has many wild hosts, but these are not well documented.
Fruit maturity stage can be important to host status for commer-
Citrus reticulata, clementine tangerine
cial fruits. Mangosteen is considered a nonhost for B. dorsalis and
Actinidia chinensis, kiwifruit ‘Green’
Actinidia chinensis, kiwifruit ‘Gold’
B. carambolae Drew & Hancock, with resistance probably due to
Hylocereus undatus, dragon fruit
Malus × domestica, apples ‘Jazz’
Sicyos pachycarpus, feral melon
pericarp hardness and thickness and latex secretion (Unahawutti
Citrus sinensis, orange Naval
Sicyos erostratus, feral melon
et al. 2014); however, the flesh can support high numbers of both
Coccinia grandis, ivy gourd
Coccinia grandis, ivy gourd
species if fruit are damaged. In Hawaii, B. dorsalis oviposits in ripe
Carica papaya, papaya
Carica papaya, papaya
Carica papaya, papaya
lychee (Litchi chinensis) on the tree, but eggs deposited in the flesh
Cucumis dipsaceus
Table 2. Continued
generally do not hatch and the fruit is a very poor host (McQuate
and Follett 2006); however, when unharvested lychee fruit fall to
the ground, resistance is lost and B. dorsalis eggs will hatch, and
larvae can develop (P. A. Follett, personal observation). Banana is
a nonhost for tephritid fruit flies, including B. dorsalis, in the ma-
Host
ture green stage but becomes a host as fruit ripen (Armstrong 1983);8
Table 3. Host Suitability Index (HSI) ranking of fruit hosts based on reports of fruit fly puparia developing from fruit from tree sampling in the field or laboratory cage tests
Average number of fruit fly pupae per kilogram of fruit
Laboratory
Host In field Intact Punctured Reference Category
Bactrocera dorsalis (Oriental fruit fly)
Vaccinium reticulatum, ohelo 5 Follett and Zee (2011) MG
Vaccinium corymbosum, blueberry ‘Berkeley’ 60 Follett et al. (2009) G
Persea Americana, avocado ‘Sharwil’ 110 Follett (2009) VG
Vaccinium corymbosum, blueberry ‘Legacy’ 200 Follett et al. (2011) VG
Carica papaya, papaya 206 464 Follett et al. (2019b) VG
Vaccinium corymbosum, blueberry ‘Biloxi’ 230 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Springhigh’ 250 Follett et al. (2011) VG
Malus × domestica, apples ‘Jazz’ 269 619 Follett et al. (2019b) VG
Vaccinium corymbosum, blueberry ‘Southern Belle’ 330 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘O’Neal’ 340 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Windsor’ 380 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Misty’ 440 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Sunshine Blue’ 520 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Blue Crisp’ 530 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Jewel’ 560 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Jubilee’ 570 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Sharpblue’ 630 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Emerald’ 700 Follett et al. (2011) VG
Carica papaya, papaya 790 Follett (2009) VG
Carica papaya, papaya 1,220 Follett et al. (2011) VG
Carica papaya, papaya ‘Rainbow’ 1,440 Follett and Zee (2011) VG
Vaccinium corymbosum, blueberry ‘Bluecrop’ 1,060 Follett et al. (2009) VG
Vaccinium corymbosum, blueberry ‘Sapphire’ 1,429 Follett et al. (2011) VG
Bactrocera latifrons (Solanum fruit fly)
Citrus sinensis, orange Naval 0.4 6 McQuate et al. (2015) P
Citrus reticulata, clementine tangerine 0.5 0.4 McQuate et al. (2015) P
Carica papaya, papaya 333 McQuate et al. (2015) VG
Capsicum annuum, pepper Anaheim 379 McQuate et al. (2015) VG
Solanum melongena, eggplant 454 McQuate et al. (2015) VG
Bactrocera tryoni (Queensland fruit fly)
Cucurbita pepo, pumpkin ‘Queensland Blue’ 0 2 Jessup and McCarty (1993) NH
Vitis vinifera, grapes ‘Red Emperor’ 2 0.4 Jessup et al. (1998) MG
Vitis vinifera, grapes ‘Calmeria’ 2 3 Jessup et al. (1998) MG
Vitis vinifera, grapes ‘Red Globe’ 3 34 Jessup et al. (1998 MG
Vitis vinifera, grapes ‘Flame Seedless’ 8 158 Jessup et al. (1998) MG
Vitis vinifera, grapes ‘Thompson Seedless’ 40 14 Jessup et al. (1998) G
Vitis vinifera, grapes ‘Menindee Seedless’ 58 94 Jessup et al. (1998) G
Ceratitis capitata (Mediterranean fruit fly)
Passiflora edulis, passion fruit 0.4 Rengifo et al. (2011) P
Vaccinium corymbosum, blueberry ‘Berkeley’ 20 Follett et al. (2009) G
Journal of Economic Entomology, 2021, Vol. XX, No. XX
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Average number of fruit fly pupae per kilogram of fruit
Laboratory
Host In field Intact Punctured Reference Category
Vaccinium corymbosum, blueberry ‘Sharpblue’ 30 Follett et al. (2011) G
Persea Americana, avocado ‘Sharwill’ 48 Follett (2009) G
Vaccinium corymbosum, blueberry ‘Biloxi’ 60 Follett et al. (2011) G
Malus × domestica, apples ‘Jazz’ 70 129 Follett et al. (2019b) G
Vaccinium corymbosum, blueberry ‘Millennia’ 80 Follett et al. (2011) G
Vaccinium corymbosum, blueberry ‘Springhigh’ 100 Follett et al. (2011) G
Vaccinium corymbosum, blueberry ‘Jewel’ 170 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Sunshine blue’ 170 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Misty’ 200 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Emerald’ 220 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘South Moon’ 220 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Sapphire’ 240 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Star’ 280 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Legacy’ 410 Follett et al. (2011) VG
Journal of Economic Entomology, 2021, Vol. XX, No. XX
Vaccinium corymbosum, blueberry ‘Windsor’ 430 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Jubilee’ 440 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Blue Crisp’ 500 Follett et al. (2011) VG
Vaccinium corymbosum, blueberry ‘Bluecrop’ 600 Follett et al. (2009) VG
Carica papaya, papaya 676 573 Follett et al. (2019b) VG
Carica papaya, papaya 990 Follett (2009) VG
Carica papaya, papaya 1,070 Follett et al. (2011) VG
Zeugodacus cucurbitae (melon fly)
Vaccinium corymbosum, blueberry ‘Sunshine blue’ 0 Follett et al. (2011) NH
Vaccinium corymbosum, blueberry ‘Misty’ 0 Follett et al. (2011) NH
Vaccinium corymbosum, blueberry ‘Legacy’ 0 Follett et al. (2011) NH
Vaccinium corymbosum, blueberry ‘Blue Crisp’ 0 Follett et al. (2011) NH
Vaccinium corymbosum, blueberry ‘Berkeley’ 0 Follett et al. (2009) NH
Citrus sinensis, orange Naval 0 85 McQuate et al. (2015) NH
Vaccinium corymbosum, blueberry ‘Emerald’ 2 Follett et al. (2011) MG
Benincasa hispida, Toghan squash 3 Jang et al. (2008) MG
Malus × domestica, apples ‘Jazz’ 4 0.8 Follett et al. (2019b) MG
Vaccinium corymbosum, blueberry ‘Sharpblue’ 7 Follett et al. (2011) MG
Vaccinium corymbosum, blueberry ‘Jewel’ 10 Follett et al. (2011) MG
Vaccinium corymbosum, blueberry ‘Biloxi’ 12 Follett et al. (2011) G
Cucumis dipsaceus, hedgehog cucumber 15 Uchida et al. (1990) G
Cucumis melo, cantaloupe 17 Jang et al. (2008) G
Citrullus lanatus, watermelon 17 Jang et al., (2008) G
Vaccinium corymbosum, blueberry ‘Jubilee’ 19 Follett et al. (2011) G
Vaccinium corymbosum, blueberry ‘Windsor’ 28 Follett et al. (2011) G
Cucurbita pepo, zucchini 55 Jang et al. (2008) G
Momordica charantia, bitter gourd 69 Jang et al. (2008) G
9
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G = good host; MG = moderately good host; NH = nonhost; P = poor host; VG = very good host; VP = very poor host. Hosts are listed for each species in ascending order of infestation rate. HSI rankings were assigned from
evaluation of culled fruit showed that even mature green stage ba-
Category
nanas showing faults or damage that compromised the integrity of
VG
VG
VG
VG
VG
VG
VG
VG
the skin could be infested by B. dorsalis (Armstrong et al. 2001). The
G
G
avocado variety ‘Sharwil’ is a poor host for B. dorsalis and a nonhost
for C. capitata when harvested at the hard, mature green stage but
becomes an increasingly good host over time after harvest as fruit
ripen and soften (Oi and Mau 1989, Follett 2009). Poor host status
and maturity stage can be used in a systems approach to reduce risk
to an acceptable level for market access. The HSI quantifies the rela-
tive suitability and risk reduction for poor hosts.
McQuate et al. (2015)
McQuate et al. (2015)
McQuate et al. (2015)
Jackson et al. (2003)
Follett et al. (2019b)
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Follett et al. (2009)
Follett et al. (2011)
Follett et al. (2011)
Systems Approach
Jang et al. (2008)
Jang et al. (2008)
Systems approaches are increasingly being used to access mar-
Reference
kets in international trade. A systems approach integrates two or
more independent phytosanitary measures to cumulatively provide
quarantine security (Follett and Neven 2006, Sequeira and Griffin
2014, Dominiak 2019). Adequate quarantine security might not be
achieved by each individual step but could be achieved when mul-
tiple steps are applied sequentially. The concept of a poor host has
been used as part of a systems approach as a phytosanitary measure
to allow movement of fruit in trade while reducing risk to an ac-
ceptable level. In a retrospective analysis of 60 protocols targeting
Punctured
arthropods and pathogens, poor host status was a component in
240
735
20% of all systems approaches and 15% of those targeting fruit
flies (van Klinken et al. 2020); in this case, poor host status referred
Laboratory
to fruit varieties with low host susceptibility or harvested at a poor
host stage, e.g., mature green fruit. Theoretically, each phytosani-
tary measure in the systems approach could be quantified so that an
overall risk reduction could be calculated and evaluated for efficacy
to guide pest risk assessment and pathway risk management deci-
1,440
Intact
sions (Jamieson et al. 2016, Moore et al. 2016, Brown et al. In press).
112
310
341
457
467
90
An HSI approach would help identify candidates for a systems ap-
proach, help quantify the level of poor host status in calculating pest
risk, and improve risk-based inspection schemes that depend on an
estimate of pest prevalence (Sequeira and Griffin 2014).
The components of a systems approach, apart from the use of
an HSI estimation of pest prevalence, could vary widely, but they
In field
commonly would include pest survey, trapping and sampling, field
93
101
612
treatment, sanitation, postharvest safeguards, limited harvest period,
field sampling and laboratory trials with intact fruit, only (not punctured fruit).
limited sales distribution, and restrictions on crop maturity at har-
vest (Follett and Neven 2006, van Klinken et al. 2020). For example,
Citrus fruits are shipped from Florida to other states and foreign lo-
cations using a systems approach to prevent infestation by Caribbean
fruit fly, Anastrepha suspensa (Loew), that includes poor host status,
removal of alternative hosts, established growing areas with buffers,
Average number of fruit fly pupae per kilogram of fruit
trapping, field treatment, restricted harvest periods, and fruit cutting
(Riherd et al. 1994). The avocado cultivar Sharwil can be exported
Vaccinium corymbosum, blueberry ‘Bluecrop’
Vaccinium corymbosum, blueberry ‘Sapphire’
from Hawaii to the continental United States using a systems ap-
proach to prevent B. dorsalis infestation, based on poor host status,
Citrus reticulata, clementine tangerine
Cucurbita maxima, crookneck squash
harvest of hard, mature, green fruit, field monitoring, sanitation,
limited sales distribution (northern states during the winter months,
Cucurbita moschata, pumpkin
only), and low pest prevalence (Follett and Vargas 2010).
Coccinia grandis, ivy gourd
Carica papaya, papaya
Carica papaya, papaya
Carica papaya, papaya
Carica papaya, papaya
Alternative Treatment Efficacy
Table 3. Continued
To validate the efficacy of quarantine measures intended to be suf-
ficient for biosecurity by themselves (not part of a larger risk reduc-
tion strategy) requires access to very large numbers of the fruit fly
of concern in the fruit of interest. A probit 9 response level, equiva-
lent to 99.9968% mortality (95% CI) requires treatment of at least
Host
93,613 individuals, all of which must be killed (Couey and ChewTable 4. Host Suitability Index (HSI) ranking of fruit hosts based on reports of third instars recovered from fruit from tree sampling in the field or laboratory cage tests
Average number of fruit fly third-instar larvae per kilogram of fruit
Laboratory
Host In field Intact Punctured Reference Category
Bactrocera latifrons (Solanum fruit fly)
Cucumis sativus, cucumber 0.9 Liquido et al. (1994) P
Lagenaria siceraria, ipu, upu 1 Liquido et al. (1994) P
Solanum melongena, eggplant 4 Liquido et al. (1994) MG
Benincasa hispida, tunka, tankoy, zit-kwa 6 Liquido et al. (1994) MG
Journal of Economic Entomology, 2021, Vol. XX, No. XX
Solanum torvum, turkey berry 9 Liquido et al. (1994) MG
Solanum melongena, eggplant 13 Liquido et al. (1994) G
Coccinea grandis, ivy gourd, scarlet-fruit gourd 28 Liquido et al. (1994) G
Physalis peruviana, poha 34 Liquido et al. (1994) G
Lycopersicon pimpinellifolium, currant tomato 31 Liquido et al. (1994) G
Solanum nigrescens, dull popolo 55 Liquido et al. (1994) G
Lycopersicon lycopersicum, tomato 75 Liquido et al. (1994) G
Solanum pseudocapsicum, Jerusalem cherry 109 Liquido et al. (1994) VG
Capsicum frutescens, tabasco pepper 190 Liquido et al. (1994) VG
Lycopersicon esculentum cv cerasiforme, cherry tomato 200 Liquido et al. (1994) VG
Solanum sodomeum, Sodom apple 264 Liquido et al. (1994) VG
Capsicum annum, capsicum 301 Liquido et al. (1994) VG
Solanum nigrum, popolo 373 Liquido et al. (1994) VG
Ceratitis capitata (Mediterranean fruit fly)
Passiflora edulis, passion fruit 3.9 Rengifo et al. (2011) MG
G = good host; MG = moderately good host; NH = nonhost; P = poor host; VG = very good host; VP = very poor host. Hosts are listed for each species in ascending order of infestation rate. HSI rankings were assigned from
field sampling and laboratory trials with intact fruit, only (not punctured fruit).
11
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1986, Schortemeyer et al. 2011). For many countries, a 99.99% (Cantrell et al. 2002, Dominiak and Mapson 2017). The regulatory
mortality level is acceptable for quarantine treatment efficacy, treat- response to fruit fly incursions should vary depending on the host
ment of only about 30,000 individuals (Follett and Neven 2006). status of fruits in the invaded area that would be available to the
While generally appropriate, these protocols may be overly stringent invasive fruit fly. For example, New Zealand had eight detections
for risk control in commodities that are poor hosts or are rarely in- (flies caught in surveillance traps) from 1995 to 2019, and two in-
fested. For such cases, a less stringent treatment protocol may well cursions (breeding population found) of pest fruit flies, including
be sufficient to provide quarantine security (Follett and McQuate Oriental fruit fly, B. dorsalis (one detection), Mediterranean fruit fly,
2001). Also, problems arise currently when quarantine tests apply C. capitata (one incursion), Zeugodacus tau (Walker) (one detec-
the current standard to fruits that are poor hosts for the fruit fly tion), and Queensland fruit fly, B. tryoni (six detections and one in-
of concern because of difficulties in successfully infesting enough cursion) (Kiwifruit Vine Health 2014). The fruit fly incursions were
fruit with adequate numbers of larvae to allow for large-scale successfully eradicated as a result of a biosecurity response following
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testing. Deviations from protocol are needed in many cases, such as detection. Knowing the host suitability of fruits near the point of
puncturing or otherwise damaging the fruits to facilitate fly ovipos- detection or incursion would better inform managers about delimi-
ition, and, if the fruit is a poor developmental host, it may be neces- tation strategies, e.g., more intense sampling of good hosts compared
sary to artificially create cavities in the fruit and insert test insects. with poor hosts, or in areas of mainly poor hosts, the need for a
It may also then be necessary to open infested fruits, remove larvae greater sampling effort to increase the probability of detecting rare
after treatment, and place them on a preferred host or artificial diet infestations (FAO 2008).
to avoid the high mortality from the fruit itself (Barkai-Golan and In 2015, an incursion of B. tryoni in Auckland resulted in ex-
Follett 2017). Different protocols should be developed for use with port restriction zones within 3.5, 7.5, or 27 km from the incursion
poor hosts in quarantine tests; doing so is justified because of the site for exports to Western Australia, the United States, and Chinese
inherently lower risk of poor hosts vectoring the target fly into new markets, respectively. Auckland is not an area of significant fruit pro-
areas (Follett and McQuate 2001). duction and no fruit fly outbreaks have occurred in areas of signifi-
cant apple or kiwifruit production in New Zealand. If B. tryoni (or
B. dorsalis, Z. cucurbitae, or C. capitata) had arrived in a one of
Regulatory Response to Outbreaks the major fruit-growing areas, rather than Auckland, the economic
Fruit fly incursions can have significant economic impacts due to consequences would have been much larger (Kiwifruit Vine Health
the loss of domestic and export markets until quarantine bound- 2014). The severity of impact following a detection or incursion
aries can be put in place, and the temporary suspension of exports would depend on the timing relative to fruit harvest, the extent of
the invasion (a single fly catch versus a breeding population), the
duration of the quarantine response, and over how large an area
fruit movement was restricted. In this case, information about the
host status of apple or kiwifruit to the invasive fruit fly would also be
important. Bactrocera dorsalis and Z. cucurbitae are not established
in areas for apple or kiwifruit production worldwide and therefore
their host status for those crops would be valuable information.
Apples and kiwifruit from New Zealand were shipped to Hawaii
to evaluate their host status for three potential invaders, B. dorsalis,
Z. cucurbitae, and C. capitata. Apple and kiwifruit are known hosts
(albeit poor hosts) of C. capitata. In cage tests, apples were a moder-
ately good host for B. dorsalis and a very poor host for Z. cucurbitae,
but when apples were suspended from papaya trees in the field,
none became naturally infested by B. dorsalis or Z. cucurbitae (Fig.
3). Likewise, field exposures of kiwifruit in papaya trees led to no
infestation by B. dorsalis in green kiwifruit and only a low infest-
ation rate in gold kiwifruit. Similarly, in the same trial, there was
no infestation in either kiwifruit cultivar by Z. cucurbitae (Tables
2 and 3) (Follett et al. 2019a,b). These data suggest that incursions
by B. dorsalis or Z. cucurbitae into areas of commercial apple or
green kiwifruit production in New Zealand would probably result in
no fruit infestations; consequently, export restrictions in such a case
would not be scientifically justified. However, the suggestion that
apple or green kiwifruit ‘would probably’ remain uninfested is un-
likely to be acceptable to a regulator unless backed-up by some form
of quantification with statistical equivalence to 99.99% or Probit
9 treatment efficacy. At a minimum, the size of the export restric-
tion zone could be reduced for poor or very poor hosts with low
but uncertain risk. New Zealand has begun developing preapproved
quarantine treatments against invasive fruit flies for use in the event
Fig. 3. Apples suspended from the trunk of a papaya tree to examine natural
of an incursions and subsequent export restrictions. The availability
infestation by the tropical fruit flies Bactrocera dorsalis and Zeugodacus of preapproved quarantine treatments for B. tryoni, B. dorsalis,
cucurbitae in Hawaii where apples are not grown commercially. Z. cucurbitae, and C. capitata and other invasive fruit flies wouldJournal of Economic Entomology, 2021, Vol. XX, No. XX 13
minimize the economic impact of an incursion and subsequent quar- Brown, S., L. E. Jamieson, O. Woodberry, S. Mascaro, N. Meurisse,
antine response, as fruit exports would not be disrupted. R. Jaksons, and M. Ormsby. In press. An Integrated Biosecurity Risk
Assessment Model (IBRAM) for evaluating the risk of import pathways
for the establishment of invasive species. Risk Analysis.
Conclusions CAB International and the European and Mediterranean Plant Protection
Organization (CABI/EPPO). 1997. Quarantine pests for Europe. 2nd ed.
We illustrate the concept of a general-purpose HSI using host status CAB International, Wallingford, Oxon, United Kingdom.
information for adults, pupae, and larvae of five species of polypha- Cantrell, B., B. Chadwick, and A. Cahill. 2002. Fruit fly fighters: eradication
gous tephritid fruit flies in the Pacific region. Results from labora- of the papaya fruit fly. CSIRO Publishing, Collingwood, VIC, Australia.
tory and field studies were mostly consistent, but fruits designated as Carey, J. R., D. A. Krainacker, and R. I. Vargas. 1986. Life history response
very poor hosts based on laboratory studies may in fact prove to be of female Mediterranean fruit flies, Ceratitis capitata, to periods of host
nonhosts in nature. Adult emergence (rather than larval infestation deprivation. Entomol. Exp. Appl. 42: 159–167.
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an endorsement or a recommendation by USDA for its use. USDA is Development of Australia’s eastern trading block. J. Econ. Entomol. 110:
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