Introduction

Tephritid fruit flies are one of the most important invasive and destructive crop pests globally (Follett et al. 2021). Human-assisted transport of infested fruit is responsible for long distance dispersal and introduction of tephritids into new areas (Sadler et al. 2011; EFSA 2023). Tourism and trade are key components to the economies of many countries. The ever-increasing international movement of people via tourism and fruits and vegetables via trade increases the risk of incursions of invasive plant pests (Robinson and McNeill 2022). Tephritids cause direct losses making fruit inedible, which can adversely impact our ability to feed a growing world population (Bebber et al. 2014). Additionally, detections of exotic tephritids can trigger regulatory responses to eradicate or contain the incursion (Hancock 2013; Ormsby 2021). Potentially, incursions of exotic tephritids can disrupt both domestic and international trade in fresh fruit and damage national economies (Bebber et al. 2014), and thus importing countries may impose stringent quarantine restrictions to prevent entry of potentially infested fruits or vegetables. Additionally, some invasive species displace local tephritids and force changes in fruit fly management in invaded countries (Duyck et al. 2004; Ekesi et al. 2009).

The actual risk posed by any individual tephritid species depends on the host species. Not all hosts are equal. Different hosts offer a variable capacity to support the tephritid life cycle from egg lay to emerged adults. This capacity is measured by the number of adults that emerge from one kilogram of fruit and this metric was termed the Host Reproduction Number (HRN) (Dominiak 2022). The HRN can range from 0 to > 1000 (Dominiak 2021). Follett et al. (2021) designed the Host Suitability Index (HSI) and placed these HRN into six major categories, based on the log of HRN. These are very poor (< 0.1 adults per kg), poor (0.1–1.0), moderately good (1.0–10.0), good (10–100) and very good (> 100). HRN was used previously by several authors although, often under different names. Examples include in Western Australia, Woods et al. (2005) used HRN to rank hosts of Mediterranean fruit fly (Ceratitis capitata Wiedemann). For Queensland fruit fly (Bactrocera tryoni Froggatt), Lloyd et al. (2013) used HRN to rank hosts in Queensland, and Dominiak et al. (2020) reviewed some hosts in southern Australia. These Australian papers were included in the Pacific regional review (Follett et al. 2021). A complete review of hosts of B. tryoni including known HRN and a revised host list from Australia and the Pacific islands was completed by Dominiak (2023). Additionally, the tephritid-host relationships in Africa were reviewed by Dominiak (2022). There is a need to provide similar data for the New World tephritids to optimise fruit fly surveillance, management and trade.

Here we reviewed > 50 papers based on reports in the Americas and found data on > 350 hosts of 26 tephritids in the New World and identified the reproductive capacity (HRN) where possible. There was HRN data on only 13% of tephritid-host data in the science press. There was considerable variability in the data and we only recorded the worst-case scenario. We made no effort to reconcile differences caused by season, altitude, pest population pressure, host availability or any other factors which contribute to HRN.

Materials and methods

The host status of fruit is an important component of pest risk analysis and IPPC (2016) outlined three main host statuses. The first is “natural host” and is where the target fruit fly species can infest fruit under natural conditions and fruit can sustain the development to viable adults. The second are “conditional hosts” which identifies a host status under semi-natural or artificial conditions. Non-hosts are hosts that are not able to sustain the development of viable adult flies under natural or semi-natural conditions. We searched for papers on natural host reports, wherever possible.

We examined the published literature covering the HRN for all fruit flies in the American continents and placed fruit fly hosts in alphabetic order in separate tables for Anastrepha spp. hosts and a second table for Bactrocera carambolae (Drew & Hancock), C. capitata and Rhagoletis spp. hosts. In some cases, the studies did not report an HRN but there was enough data provided so that the HRN could be calculated (e.g. Ovruski et al. 2003). These references are denoted by “calculated” in the tables. We list all references with any host status information, mainly because so little data were available. In our review, numbers of HRN > 1 were rounded up to the nearest whole number. Numbers < 1 were reported to one decimal point. We kept the reference identifiers the same in both tables for continuity even though some references were not used in one table or the other.

Results

We found data on 564 tephritid-host relationships with only 13.3% containing specific HRN information. Table 1 contains information for 16 species of Anastrepha: A. acris (Stone), A. alveata (Stone), A. bahiensis (Lima), A. distincta (Greene), A. fraterculus (Wiedemann), A. grandis (Macquart), A. leptonozea (Hendel), A. ludens (Loew), A. obliqua (Macquart), A. pickeli (Lima), A. serpentina (Wiedemann), A. sororcula (Zucchi), A. striata (Schiner), A. suspensa (Loew), and A. turpiniae (Stone). For Anastrepha spp., the list included monophagous species such as A. acris and A. alveata, and highly polyphagous species such as A. striata, A. suspensa, A. obliqua, and A. fraterculus (Table 1). Anastrepha fraterculus had the most studies that reported HRN information, with the reproductive number ranging from 0.1 flies/kg in fig, Ficus carica, to 97 flies/kg in walnut, Juglans australis.

Table 1 Anastrepha hosts and their highest reported rating of adults/kg of fruit (HRN). Hosts are listed for each fruit fly host species in alphabetical order. Common names of hosts are provided where available. Numbers larger than ten were rounded up. All other numbers below 1 were rounded to one decimal point. All numbers above one were rounded out
Full size table

Table 2 contains information for Bactrocera carambolae, Ceratitis capitata, and eight species of Rhagoletis: R. cerasi (L.). R. cingulata (Loew), R. complete (Cresson), R. fausta (Loew), R. indifferens (Curran), R. medax (Curran), R. pomonella (Walsh), and R. zephyria (Snow). Table 2 was dominated by the long host list for C. capitata, which had 320 reported hosts. Of the 29 papers that reported HRN for C. capitata, reproductive numbers ranged from 0 in many Citrus spp. (except orange, which was a very good host with 76 flies/kg) to 376 flies/kg in Barbados cherry, Marpigha emarginata. We found 26 hosts for B. carambolae, and the HRN ranged from 0.1 flies/kg in mango, Mangifera indica to 478 flies/kg in pamarrosa, Syzygium jambos. For Rhagoletis, R. zephyria was monophagous on native snowberry, Symphoricarpos albus, and R. pomonella was the most polyphagous species with 65 reported hosts, with most hosts in the genera Vaccinium, Crataegus, Gaylussasia, Malus, Prunus, and Pyrus. Although the host list for R. pomonella is well established, information on HRN was scarce. In most cases, the studies may have reported that a plant was a host for a particular fruit fly species but did not attempt to quantify the level of infestation or HRN. In several cases studies showed that a host plant was a nonhost for a particular fruit species by attempting to rear fruit flies from the host. For example, tangerine, Citrus reticulata, Valencia orange, Citrus sinensis, and blue passion fruit, Passiflora caerulea were reported as nonhosts for (A) fraterculus (Ovruski et al. 2003). Bitter orange, Citrus aurantium was a good host for C. capitata (72 flies/kg fruit), but it appeared that mandarin, Citrus deliciosa, toranja, Citrus grandis, Rangpur lime, Citrus limonia, and Persian lime, Citrus latifolia were non-hosts for C. capitata (Raga et al. 2004). When HRN was reported, it was often the case that the fruit was a relatively poor host and supported only low numbers of fruit flies. For example, B. carambolae readily infested pamarrosa, Syzygium jambos (478 flies/kg fruit), Surinam cherry, Eugenia uniflora (58 flies/kg fruit), Calotropis procera (77 flies/kg fruit), and starfruit, Averrhoa carambola (27 flies/kg fruit) but infested Java apple, Syzygium samarangense (1.3 flies/kg fruit) and mango, Mangifera indica (0.1 flies/kg fruit) at a very low rate (Ovruski et al. 2003; Almeida et al. 2016; Belo et al. 2020).

Table 2 Hosts and their highest reported rating of adults/kg of fruit (HRN) for Rhagoletis spp., Bactrocera carambolae and Ceratitis capitata. Hosts are listed for each fruit fly host species in alphabetical order. Common names of hosts are provided where available. Numbers larger than ten were rounded up. All other numbers below 1 were rounded to one decimal point. All numbers above one were rounded out
Full size table

Discussion

Our review summarizes the use of HRN with the potential to inform a range of activities associated with New World tephritid management, including surveillance programs, systems approach to quarantine security, alterative treatment efficacy for quarantine treatment development, and response to fruit fly outbreaks. HRN could inform surveillance programs to optimise where to hang traps and how to sample fruit for infestation after trap captures. For example, California deploys and maintains 63,000 detection traps state-wide for exotic fruit flies with weekly inspections (CDFA 2023). Many exotic fruit fly species are detected each year including Bactrocera carambolae, B. correcta (Bezzi), B. cucurbitae (Coquillett), B. dorsalis (Hendel), B. zonata (Saunders), A. suspensa, A. ludens, and A. obliqua. For significant finds, the trapping density is increased in the immediate area to delimit the tephritid population and establish a quarantine area and boundary. Within the quarantine area, detailed information is gathered on the number and types of host trees and the GPS locations. The host lists used for each species currently do not include information on host suitability or HRN and all hosts are treated equally in the eradication response. If chemical (e.g. male attractant technique or protein bait sprays) and physical (fruit removal) controls are necessary, knowing whether hosts are high risk or low risk might improve eradication efforts and allow for more efficient use of resources.

Systems approach

Systems approaches are increasingly being used to access markets in international trade (Follett and Vargas 2009; Missenden et al. 2015; Jang 2016). 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 multiple steps are applied sequentially. The concept of a poor host has been used often as part of a systems approach as a phytosanitary measure to allow movement of fruit in trade while reducing risk to an acceptable level (Follett and Hennessey 2007). Poor host status refers to fruit varieties with low host susceptibility or harvested at a poor host stage, e.g., mature green fruit (Follett 2009). For example, a systems approach might be possible for (A) fraterculus in fig because it is a very poor host (Follett et al. 2021) with 0.1 flies/kg fruit, but less suitable for walnut which is a very good host with 97 flies/kg fruit. Similarly, a systems approach might be possible to mitigate risk in mango to B. carambolae (0.1 flies/kg fruit), but less likely in starfruit (27 flies/kg fruit).

Here, we reported the highest HRN because this is the greatest risk in a given environment or time. However, this is unlikely to be the case for all environments and situations. Some hosts could be harvested at a particular time, for example before that host became attractive or susceptible to a tephritid. Trade regulators will need to identify those conditions and provide the science which make the host a non-host or a conditional host. This process was outlined by Follet and Hennessey (2007) and fully developed for avocados (Follett 2009; Follett and Vargas 2009). Similarly, Queensland fruit fly (Bactrocera tryoni Froggatt) are not known to infest hard green bananas (Hancock et al. 2000). Therefore, some hosts can be conditional hosts or conditional non-hosts, depending on the situation.

Alternative treatment efficacy

For many countries, a 99.99% mortality is required for quarantine treatment efficacy, or treatment of approximately 30,000 individuals without survivors (Follett and Neven 2006). For fruits that are poor hosts or rarely infested, requiring this level of testing may be overly stringent (Follett and McQuate 2001). Essentially, in poor hosts, the fruit itself is a significant mortality or resistance factor resulting in low levels of infestation. Different protocols could be developed for fruit flies on poor hosts which require treatment of fewer insects with no survivors due to their inherently lower risk. The alternative treatment efficacy approach calculates the risk assuming we are trying to prevent a mating pair developing in the environment after importation into a fruit fly free region (Dominiak and Fanson 2023). From the fruit infestation rate and the number of fruits in a shipment, we can calculate the treatment efficacy required to prevent the occurrence of a mating pair. For fruit flies on very poor hosts, the number of test insects required to demonstrate a treatment that provides quarantine security may be achieved with testing of 10,000 or fewer insects (Follett and McQuate 2001).

Outbreak response

Fruit fly incursions can have significant economic impacts due to the loss of domestic and export markets until quarantine boundaries can be put in place, and the temporary suspension of exports (Cantrell et al. 2002; Dominiak and Mapson 2017). The regulatory response to fruit fly incursions should vary depending on the host status of fruits in the invaded area that would be available to the invasive fruit fly. For example, A. ludens, the Mexican fruit fly, is native to southern and central Mexico and a frequent invader in the United States. Frequently in each year, A. ludens enters the Rio Grande Valley in Texas where citrus is grown commercially. We found that A. ludens infested 66 different kinds of fruit and backyard fruit is a threat to surrounding citrus producing states including California, Arizona, Louisiana, and Florida. Eradication tactics include surveillance, bait sprays and the sterile insect technique (SIT). Host plant status information could help focus surveillance and bait sprays on high-risk hosts during an outbreak. For example, it may make sense to destroy backyard fruit for a preferred host such as oranges in the quarantine area, compared to avocado which is a poor host, or possibly a nonhost (Aluja et al. 2004). Therefore, a less stringent approach may be warranted such as inspection of a sample of fruit for oviposition sites or fruit cutting to determine if fruit are infested. Growers stand to lose their crop during an outbreak due to fruit destruction or their inability to ship fruit outside the quarantine area. Hence, these growers might be willing to bear the costs of sampling or other non-destructive alternative measures if this is a limiting factor.

Host use patterns

There are several stark differences between the results in this review and reviews of other regions or tephritids (Follett et al. 2021; Dominiak 2022; Dominiak and Taylor-Hukins 2022). For the 16 Anastrepha spp., the HRN exceeds 30 in only one host (Table 1). In comparison, the HRN for African tephritids (mainly Ceratitis spp.) often exceeded 100. If HRN is a strong indicator of competitive ability between tephritids (Ekesi et al. 2009), then we conclude that Anastrepha spp. are likely to be outcompeted by more invasive tephritids. Conversely, Anastrepha tephritids are likely to offer a low invasive threat due to competition if introduced into countries such as Africa and Australia with established tephritid species (Dominiak et al. 2020; Dominiak and Taylor-Hukins 2022).

For the eight Rhagoletis spp., we found 12 HRN within 140 fly-host relationships. Therefore, there is little knowledge to gauge the level of threat posed by Rhagoletis spp to the Americas and any importing country (Ekesi et al. 2009). However, the host range that we found will inform any eradication programs. Conversely for C. capitata, we found 320 fly-host data with 29 HRNs. This host range (320 hosts) is much greater than for R. pomonella (65 hosts), A. fraterculus (101 hosts) or A. obliqua (97 hosts) (Table 1). However, C. capitata does not infest the same hosts. For instance, C. capitata does not infest Crataegus spp. and this allows R. pomonella to survive despite the presence of C. capitata. Dominiak and Taylor-Hukins (2022) provided HRN for 146 hosts of C. capitata compared with 29 in our review. Dominiak and Taylor-Hukins (2022) reported the worst-case scenario for C. capitata but there may be lower HRN in the Americas because of local conditions. Considerable basic research is required to provide a HRN for different locations in the New World if trade and management is to be optimised.

For B. carambola, we found 26 hosts-fly data with 11 containing HRN. Mostly, HRN did not exceed 77 except for Syzygium jambos with HRN = 478. We suggest that S. jambos is likely to be a major resource for B. carambola survival. If fruit from this plant is traded between countries, S. jambos is a possible source of incursion for areas currently free from B. carambola. This plant has a world-wide distribution and is grown for medicinal purposes and for its “rose water” fragrance.

Trade of fruit commodities is essential to feed earth’s population and for economic viability for many countries. HRN could be combined with the Systems Approach (Dominiak 2019; Follett et al. 2022) for the New World and other international trade. Follett and Hennessey (2007) noted that hosts with a low HRN may be combined with other measures to provide an acceptable level of quarantine security. For the New World, much research is needed to quantify HRN to optimise market access opportunities.

Mechanisms

Many factors are likely to influence HRN but the physical or physiological mechanisms that make a fruit a suitable host or a poor or nonhost are often not understood (Follett et al. 2021). Psidium guajava is a conditional non-host for A. ludens, possibly due to its high fruit firmness (2x to 3x greater than other tested fruit) (Birke and Aluja 2018). Conversely, P. guajava is a high HRN host from many other tephritids (Dominiak 2021). In citrus, peel thickness, mainly flavedo thickness, and peel resistance both contribute to minimising tephritid egg lay (Birke et al. 2006). Anastrepha ludens has a particularly long ovipositor and can place eggs beneath the toxic flavedo; other species such as C. capitata and other Anastrepha spp. suffer higher egg death because they cannot avoid this layer (Birke et al. 2006). Several species of Anastrepha specialise in attacking latex-producing plants within the Aponcynaceae, Asclepiadaceae and Sapotaceae (Orono et al. 2019). Aluja and Mangan (2008) provided a detailed treatment of host-fly association. For instance, in some species, aculeus width decreased as host cutile thickness increased (Jonesm 1989). There may be a high positive correlation between adult emergence and sugar content in many species (Orono et al. 2019). High sucrose diets can influence fecundity in some species (Wang et al. 2023). Additionally, there is a negative correlation between adult emergence and toxic secondary metabolites, such as total phenols and tannins, in fruit (Orono et al. 2019).

Location in the canopy may be a factor. Anastrepha alveata is more abundant in the lower portions of the tree while A. striata is more abundant in the upper tree (Sivinski et al. 2004). Anastrepha fraterculus is uniformly distributed throughout the canopy. Also, altitude influences species distribution. Along the altitudinal cline, A. striata is more abundant than A. fraterculus at sea level and relatively less abundant up to altitudes of 1000 m ASL (Sivinski et al. 2004). Additionally, A. striata prefers warmer and drier environments than A. fraterculus (Sivinski et al. 2004).

Host reproduction number

Our host list is not exhaustive due to the variability in the available data. There are many hosts of New World tephritids referenced in literature which clearly identify the host of a particular tephritid species. However, the HRN could not be calculated based on data provided. Infestations were reported as larvae or pupae per kg and therefore we could only record these as hosts but no HRN (adults). Also, it is important to acknowledge that even though the data suggests that some hosts are “non-hosts” (IPPC 2016), these need to be considered carefully. “Non-hosts” should not be ruled out as a host based on our review alone. It is known that factors such as climate, competition with other fruit fly species and time of year of sampling can influence number of flies found and may account for some “non-host” results.

Here, we have reported the worst-case HRN however these numbers may not apply to all circumstances. Tephritids have preferred habits and our worst case HRN may not apply to all locations or countries.

The HRN may be lower than our reported figures based on the local environment, particularly at the margins of its range. For instance. for B. tryoni in Australia, in Valencia oranges, Lloyd et al. (2013) found a HRN of 10 in central Queensland whereas Dominiak et al. (2020) reported a HRN of 142 in southern New South Wales, 1120 km further south. Conversely, roses ranged from 354 (Queensland) (May 2022) to 40 (NSW) (Dominiak et al. 2020). Guava has a high HRN for many fruit flies (Dominiak 2021) but the HRN for guava ranged from 92 (NSW) (Dominiak et al. 2020) to 4,065 (Pacific Islands) (Vargas et al. 2007). Therefore, we suspect that the HRN may be higher in ideal environmental situations. The management of tephritids in the New World could be optimised and we encourage all fruit fly researchers to report the HRN for all tephritids.

Ekesi et al. (2009) proposed that reproductive capacity was at least partially responsible of invasive success. This success is likely to result in a competitive hierarchy among tephritids (Duyck et al. 2004). Clarke and Measham (2022) reflected the widely held view that generally Bactrocera was more competitive than Ceratitis which was more competitive than Anastrepha species. Given the low number for Rhagoletis in Table 2, we might speculate that the competitive hierarchy is Bactrocera > Caratitis > Anastrepha > Rhagoletis. In Australia, this competition hierarchy was thought to be responsible for B. tryoni displacing C. capitata from Eastern Australia (Dominiak and Mapson 2017). Following a worldwide review, Augustin et al. (2012) found the Bactrocera spp. from Asia provided the highest incursion risk, followed by C. capitata, followed by the least threat from Anastrepha spp. We found data to support, at least partially, a competitive hierarchy. Recent papers frequently report much higher HRN figures for fly-host relationships (Follett et al. 2021; Dominiak 2022; Dominiak and Taylor-Hukins 2022). We think that the overall lower HRN values for Anastrepha and Rhagoletis is indicative of the lower placement in the competitive hierarchy. Therefore, Rhagoletis offers the least invasive threat for importing countries and there is opportunity to develop less draconian trade agreements for those hosts. However, this view needs to be used with caution. We found HRN for only about 13% of known hosts in the New World. This may reflect past risk averse desires to recognise host without assessing the level of risk; treatments such as methyl bromide fumigation reduced most risks to acceptable levels. In today’s risk assessment environment, the development of a HRN library is likely to be more relevant.

International standards and invasion threats

Globally, there are a set of standards, International Standards for Phytosanitary Measures (ISPM) to guide management and trade. ISPM 37 has served the international trading community well and the New World seems to have followed the host or non-host approach in ISPM37 (IPPC 2016). However, all hosts are treated the same, irrespective of the threat they pose. This all-or-nothing strategy may be less appropriate in a world where the available pesticides is declining or are becoming less acceptable (Dominiak and Ekman 2013). Alternative methods of risk management are being developed (Follett and Hennessey 2007; Dominiak 2019). The all-or-nothing approach to disinfestation takes no account of commodities which pose a lower risk and might require a lesser treatment. A better understanding of HRN and how modified disinfestations would better inform international trade community to achieve the same level of risk, i.e. equivalent to a probit level. Towards a more informative document, we suggest a new ISPM needs to be considered. This HRN ISPM would list hosts and all the related tephritids with their known HRN. This document may contain a range of HRN to account for different countries or altitude or other pertinent situations.

Therefore, considerable research into the basic HRN for both Anastrepha and Rhagoletis is required to better inform New World tephritid activities. For New World tephritid management, our revised competitive hierarchy and HRN may provide some insight. Rhagoletis spp. is unlikely to outcompete Anastrepha spp. and therefore is likely to be a lesser invasion threat. Where Rhagoletis pomonella is a concern, the Crataegus spp. are likely to remain a refuge for survival and these hosts need to be removed or treated particularly if near Prunus crops. Rhagoletis pomonella has 65 known host data but only four hosts with HRN. Therefore, the understanding of risk might be calculated as 6% (4/65) and this needs to improve to optimise management. For Rhagoletis mendax, Galussacia spp. may act as a refuge for Vaccinium producers. Similar comparisons can be made with Anastrepha spp.

We found HRN on 16 Anastrepha spp. Six of these Anastrepha had > 50 hosts. When we compare the number of known hosts with the known HRN, A. fraterculus has 101 known host data and we know 28.7% of the risks posed by this tephritid. At the other end of the spectrum of these six hosts, A. suspensa has data on 95 hosts but we could find only 4.2% of the risk posed by this tephritid. We could find about 10% of the risk posed by the other four Anastrepha spp. More HRN data needs to be collected if Anastrepha management is to be improved.

However, the biggest biosecurity threat to the New World is posed by C. capitata. We found data on 320 hosts, considerably more hosts than for Anastrepha and Rhagoletis. We could find New World data on 9% of the risk posed by C. capitata but other data is available from other countries (Dominiak and Taylor-Hukins 2022). Where feasible, C. capitata should be controlled and prevented from invading new countries. Additionally, we found data for B. carambolae on only 26 hosts but understand 42% of the risk posed. By comparison, the New World is better informed about the risks posed by B. carambolae (based on the proportion of HRN of all known hosts) than C. capitata. Trade and tourism need to be managed to prevent further incursions of both tephritids. Our review should be seen as a starting point to better inform tephritid issues in the New World.

Our data may provide comfort to countries such as Australia that Anastrepha and Rhageletis do not provide a high invasion threat because these species are unlikely to out compete the established tephritids. Australia’s focus on invasion threat from Asia may be well placed. More HRN data needs to be researched if tephritid management and trade is to be better understood and optimised.