The failure of success: cyclic recurrences of a globally invasive pest

Abstract

In the six decades since 1960, the oriental fruit fly, Bactrocera dorsalis (Hendel), has been announced successfully eradicated in California by the U.S. Department of Agriculture a total of 564 times. This includes eradication declarations in one city a total of 25 different years, in 12 cities 8-19 different years, and in 101 cities 2-7 different years. We here show that the false negatives in declaring elimination success hinge on the easily achieved regulatory criteria, which have virtually guaranteed the failure of complete extirpation of this pest. Analyses of the time series of fly detection over California placed on a grid of 100-km 2 cells revealed (1) partial success of the eradication program in controlling the invasion of the oriental fruit fly; (2) low prevalence of the initial detection in these cells is often followed by high prevalence of recurrences; (3) progressively shorter intervals between years of consecutive detections; and (4) high likelihood of early-infested cells also experiencing the most frequent outbreaks. Facing the risk of recurrent invasions, such short-term eradication programs have only succeeded annually according to the current regulatory criteria but have failed to achieve the larger goal of complete extirpation of the oriental fruit fly. Based on the components and running costs of the current programs, we further estimated the efficiency of eradication programs with different combinations of eradication radius, duration, and edge impermeability in reducing invasion recurrences and slowing the spread of the oriental fruit fly. We end with policy implications including the need for agricultural agencies worldwide to revisit eradication protocols in which monitoring and treatments are terminated when the regulatory criteria for declaring eradication are met. Our results also have direct implications to invasion biologists and agriculture policy makers regarding long-term risks of short-term expediency.

Seasonal and Year-Round Distributions of Bactrocera dorsalis (Hendel) and Its Risk to Temperate Fruits under Climate Change

“…Distinguishing the seasonal and year-round distributions of B. dorsalis is crucial for its management. For example, in seasonal distribution areas, control strategies can focus on preventing the invasion of this pest through trade or transport; for instance, the detection and eradication efforts in California show that the prevention work may need to be performed constantly [ 11 ]. Monitoring efforts should emphasize the corridors or routes connecting the current overwintering areas to each other or to all suitable habitats.…”

“…Detection and eradication of B. dorsalis is necessary, and often needs to be repeated, e.g., the situation in California [ 11 ]. To prevent their establishment, information about a species’ likelihood of invasion is necessary.…”

Global drivers of historical true fruit fly (Diptera: Tephritidae) invasions

“…While surveillance and eradication represent an important component of biosecurity measures targeting exclusion of non-native Tephritidae species, questions have been raised about the efficacy of some of these programs (Carey 1991, Papadopoulos et al 2013. Specifically, some scientists believe that detections of insects in the same general area of the site of an earlier eradication most likely reflect the persistence of the initial population (i.e., as a result of eradication failure) rather than a new invasion following successful invasion (Zhao et al 2019). However, this theory has been lively debated in the scientific literature (Gutierrez et al 2014, McInnis et al 2017).…”

The Fallacy of Year-Round Breeding in Polyphagous Tropical Fruit Flies (Diptera: Tephritidae): Evidence for a Seasonal Reproductive Arrestment in Bactrocera Species

“…Endemic to the tropical rainforests of South-east Asia and the western Pacific [ 1 ], Bactrocera Macquart species are invasive in both tropical and temperate zones [ 2 , 3 ] where they are highly disruptive to crop production and trade [ 4 ]. While not yet established in either mainland Europe or North America, Bactrocera dorsalis (Hendel) (Oriental fruit fly) is regularly detected as incursive populations on both continents [ 5 , 6 , 7 ] and has the potential to establish in both under current [ 8 ] and future climates [ 9 ]. In Australia and China, which are large enough to have distinct tropical and temperate regions, Bactrocera tryoni (Froggatt) (Queensland fruit fly) and B. dorsalis , respectively, are endemic to their tropics but invasive in temperate areas [ 10 , 11 ].…”