Using the number of cities in which a tephritid species has been detected as a proxy for area infested, figure 2a shows that in 1960 there were only two California cities in which tephritids had been detected . However, by 1970 the number of cities with a tephritid detection had increased to 13, by 1990 to a remarkable 200 cities, and by 2010 to more than 300 cities. Although 10 different species contributed to these totals, A. ludens, C. capitata and B. dorsalis contributed the most, appearing in 77, 168 and 245 new cities, respectively, by 2012 . Reintroductions versus established populations A long-standing explanation for recurring fruit fly detections is that flies are continually being reintroduced, either in cargo shipments or by people carrying infested fruit from fruit-fly infested regions of the world. We test this hypothesis and an alternative one to account for the recurring detections; both hypotheses were originally framed by Carey for the medfly as reintroduction hypothesis—recurring tephritid detections are due to repeated introductions—and established population hypotheses—recurring detections are due to resident fly populations.
We assess the strength of these two hypotheses by comparing and identifying inconsistencies in relative numbers, square pots for plants diversity and frequency of detections in California and in other fruit-fly friendly regions.Tephritids are intercepted at all airports across the USA including all airports located in the southern states considered at risk for tephritid introductions. California ports of entry accounted for less than 20% of all insects intercepted in at-risk states . Assuming that insect interceptions can serve as proxies for the relative propagule pressure, if reintroductions were the primary source of detections, then the number of fruit fly detections in fruit-fly-friendly regions of the USA outside of California, compared with detections in California, should be roughly five to one, because California contributes about 20% of detections. Yet no tephritids were detected in the majority of states that are deemed at risk for fruit fly introduction and maintain robust monitoring programmes .Although the medfly and the olive fly are the only two tropical tephritid species that are long-term residents of fruitfly-friendly regions in the European Union , interception rates of other tephritid species at ports of entry throughout the EU are quite high. One source of evidence for this is EUROPHYT, the European notification system for plant health interceptions. This system’s database revealed that, of the total number of interceptions of harmful organisms in plants and plant products imported into the EU in 2011 , fully one-third were tephritids , and showed that, from 2007 to 2009, more than 700 individual tephritids in three genera and nine species not established in Europe were intercepted at Paris’s International Airport .
If the diversity and number of tephritid interceptions at the scores of international airports located in fruit-fly-friendly southern Europe, northern Africa and the Middle East are similar to those at the Paris airport, then the tephritid propagule pressure throughout this world region is far greater than in California. Yet, despite this pressure, with the exception of the peach fruit fly , discovered in 1998 in Egypt, no other tropical tephritids have been detected throughout the Mediterranean Basin for a century.Several lines of evidence support the hypothesis that from five to nine tephritid species have become self-sustaining populations in the state : their abrupt first appearance in the mid-1950s followed by high incidence of repeat detections, their marked seasonality and northward spread , the lack of new detections and/or introductions of new species in most other at-risk regions in the USA and Mediterranean Basin, and the high probabilities of repeatedly detecting many of the tephritid species in California while at the same time not detecting them in other at-risk areas. These findings do not rule out the possibility of multiple introductions into the state for tephritids such as the medfly. However, the multiple detections of several species in nearly the same location anywhere from 10 to 30 years after they were first detected, without any captures during interim years, suggests that, as for many other invasive species , tephritids can be present in low numbers for decades. Indeed, one of the important features of lags in invasion biology that probably also applies to the tephritid invasion of California is that invasions are often not recognized until they are over.
Our findings that multiple species of tropical tephritids have self-sustaining and thus established populations in California have profound economic implications. For example, a 1995 study estimated that medfly establishment alone would result in $493 million to $875 million in annual direct costs, and the imposition of an embargo would cause an additional loss of $564 million. The state economy could lose $1.2 billion in gross revenue and more than 14 000 jobs. However, two aspects of the invasions are advantageous for planners, programme directors and policy makers. The first is that local population sizes for all species are extremely small, and therefore likely to continue to be subdetectable. Therefore, based on phytosanitary standards of the International Plant Protection Convention, most regions of the state should continue to be classified as risk-free by trading partners. The second aspect of the invasions that can be exploited for the longer term involves the invasion lags, which imply that there can be relatively long windows of opportunity for developing new protocols and programmes. Commodity certification protocols can be developed for the creation of fly-free and low-prevalence zones, as can long-term research programmes on tephritid biology and management.Because the likelihood of slowing the spread of or eradicating an alien pest depends heavily upon its residency time, a basic invasion biology canon is that early detection is critical for rapid response . Our results reveal that, because the sources of repeat detections are captures from established populations rather from reintroduced ones, in most cases ‘early detection’ is a misnomer when applied to tephritid detections at all scales. Because this expression is often inaccurate, it is also misleading inasmuch as it implies that a policy primarily directed at preventing new introductions will solve the problem of recurrent detections or infestations.As is true for many alien insect populations, the majority of tephritid population growth and spread in the state is subdetectable because of the small size and cryptic habits of all life stages, the slow pace of naturalization processes, and suppression of populations by intervention programmes. In cancer diagnostics, this is referred to as the ‘rare-event detection problem’ ; in the context of fruit fly detections, the parallel concept is the difficulty in discovering exceedingly rare, scattered, ultra-small populations of tephritids that are mostly in pre-adult stages, hidden among millions of properties and tens of millions of micro-niches. The scores of examples of repeat tephritid finds within a small region of California, separated by decades, large square planting pots suggest that the efficiency of detecting small populations of fruit flies is grossly overestimated, and that the actual chances of discovering populations that are so tiny and scattered is vanishingly small. Our findings are consistent with two interrelated invasion biology principles that underlie the ability of tephritid populations to establish and maintain residency at ultra-low, cryptic and insidious population levels. The first involves what Simberloff refers to as the ‘mysterious lag phase’ in which new populations experience delayed growth. It is unlikely that the magnitude of the lag period in tephritids would be similar to the 150þ years reported for some introduced plant species. However, it is likely that tropical species of tephritids that are introduced to different climatic regions experience major population lags much like the multidecade lags observed in the melon fly in Africa and the cherry fruit fly in Europe. Recent studies suggest that many species’ invasion success may depend more heavily on their ability to respond to natural selection than on broad physiological tolerance or plasticity, and could also result from the need for multiple invasions to facilitate a sufficient evolutionary response.Although it is widely believed that human movement of infested plant material plays a major role in spreading introduced pests, capture patterns for the Mexican fruit fly suggest that this is not the case for this species and, by extension, may not be the case for many of the other invasive tephritids. For example, in 2011, 43 million vehicles and 17 million pedestrians crossed the six ports of entry from Mexico to California.
Assuming that the direction of movement for roughly half of these vehicles and people was from Mexico to California, and if humans entering and dispersing around the state were responsible for the Mexico-to-California as well as the within-state movement of the Mexican fruit fly, then this species should have been detected more or less randomly throughout the state. But the vast majority of all A. ludens detections for nearly 60 years have been in the same areas in which this species continually reoccurs. At the same time, there have been virtually no discoveries of A. ludens in the regions of the state with extraordinarily high movement of Latino populations , such as the main agricultural areas in the Central, Salinas and Imperial Valleys .We know of no historical precedent in the invasion biology literature similar to the tephritid situation in California, where not only are several insect species within a single family invading a region at the same time, but the group also contains species within multiple genera. The California tephritid invasion thus provides unique opportunities to compare the invasive properties of species across different genera with similar life histories, to explore reasons why 17 tephritid species have been detected in California but few to none in many other fruit-fly-friendly regions of the USA and the world, and to develop new population theory for ultra-low, cryptic populations.CDFA and USDA declared 100% success for each of the several hundred eradication programmes that were launched against fruit flies in California . These declarations were accurate according to legal criteria specified by the USDA and the International Phytosanitary Commission; that is, a region is declared fruit-fly-free when no flies have been detected for a time period corresponding to three generations. Although these legal criteria are required for regulatory compliance to enable growers to ship their produce, our results reveal that the more stringent ecological requirements for eradication declaration were not met in the majority of cases. This underscores the continuing problem in the insect eradication literature of loosely and inaccurately applying a term that has a clear definition. Those interested in insect eradication can learn much from the epidemiological literature on eradication programmes regarding frameworks for evaluating systematically the potential for eradication, clear definitions of concepts and terms, and perspectives on the preconditions, difficulties and challenges of successfully eradicating insects.Although some authors have characterized population establishment as self-sustaining populations , none has attempted to specify criteria. The likely reason is that, because of the uncertainty resulting from a combination of demographic stochasticity and detection constraints, it is virtually impossible to define a precise point at which a small population becomes self-sustaining. In the light of this problem, we propose that early-stage invasions can be categorized using methods similar to those we used for Californian tephritids . The establishment category for each species is necessarily subjective and can be based on a combination of detection metrics, including capture span , total number of years captured, inter-year frequency of detections , total numbers of individuals detected, within-state distribution and spatial patterns of apparent spread.The organoleptic properties of tomato fruit are defined by a set of sensory attributes, such as flavor, fruit appearance and texture. Flavor is defined as the combination of taste and odor. Intense taste is the result of an increase in gluconeogenesis, hydrolysis of polysaccharides, a decrease in acidity and accumulation of sugars and organic acids, while aroma is produced by a complex mixture of volatile compounds and degradation of bitter principles, flavonoids, tannins and related compounds . Fruit color is mainly determined by carotenoids and flavonoids, while textural characteristics are primary controlled by the cell wall structure in addition to cuticle properties, cellular turgor and fruit morphology . In last years, tomato fruit organoleptic quality has been investigated both at the genetic and biochemical levels in order to obtain new varieties with improved taste. Recently, the genomes of traditional tomato cultivars such as San Marzano and Vesuviano , considered important models for fruit quality parameters, have been sequenced. SM, originating from the Agro Sarnese-Nocerino area in southern Italy, produces elongated fruits with a peculiar bittersweet flavor.