The discovery of bombykol as the sex pheromone of a domesticated insect species ( Butenandt et al., 1959) triggered the interest of entomologists and natural product chemists to jointly identify pheromones from economically important insect pests and explore their potential in Integrated Pest Management (IPM) ( Howse et al., 1998; Ridgway et al., 1990; Silverstein, 1981). This interest continues to increase to date given the need for environmentally friendly alternatives to control insect pest populations. After all, pheromones are non-polluting and usually non-toxic natural products. Strictly speaking they are nature-inspired synthetic compounds, i.e., identical to natural products, but manmade chemical signals. Additionally, pheromones are species-specific and safe for beneficial organisms; thus, they are ideal components of IPM programs ( Jutsum & Gordan, 1989). Of note, pheromones have been registered in many countries for use in pest management, and no evidence of adverse effects has been reported ( Witzgall et al., 2010). There is a consensus that successful implementation of pheromones in the field frequently involves a joint effort by chemical ecologists, entomologists and/or extension agronomists, and growers, in addition to the pheromone industry ( Witzgall et al., 2010).

There are many ways in which pheromones can be used for surveillance and IPM programs, including monitoring, attract-and-kill, and mating disruption. Pheromone-baited traps are sufficiently sensitive to detect low population densities and are therefore an effective way for tracking invasive species while they are still at the establishment stage ( El-Sayed et al., 2006; Liebhold & Tobin, 2008). Population monitoring has been a simple and widely used strategy to determine the ideal moment for application of control procedures (i.e., insecticides), using pre-defined thresholds (action levels) based on level of capture in pheromone-baited traps. This strategy reduces the use of insecticides to the minimal amount necessary to protect both crops and the environment ( Thomson et al., 1999; Witzgall et al., 2010).

One of the first systems to use an action level based on capture with pheromone-baited traps was established for the pea moth Cydia nigricana ( Wall et al., 1987). Later, many other studies were conducted with equal success in agricultural, horticultural or forestry applications, against pest species including the European corn borer Ostrinia nubilalis ( Laurent & Frérot, 2007), tufted apple budmoth Platynota idaeusalis ( Knight & Hull, 1989), lightbrown apple moth ( Bradley et al., 1998), scale insects ( Dunkleblum, 1999), Mullein bug Campylomma verbasci ( McBrien et al., 1994), grapevine moth Lobesia botrana ( Ioriatti et al., 2011), codling moth Cydia pomonella ( Madsen & Vakenti, 1973), Oriental fruit moth Grapholita molesta ( Rothschild & Vickers, 1991), pink bollworm Pectinophora gossypiella ( Qureshi et al., 1984), Old World bollworm Helicoverpa armigera ( Cameron et al., 2001), cotton leafworm Spodoptera litura ( Singh & Sachan, 1993), and yellow rice stem borer Scirpophaga incertulas ( Krishnaiah et al., 1998), just to cite a few.

Despite the clear advantages offered by the use of pheromones in IPM in recent decades, particularly the use of traps for monitoring in extensive areas, to date there are no studies on their economic benefits. While the benefits for the environment are less tangible, the economic benefits could be estimated. Evidence of economic benefits could be extremely helpful in motivating growers to employ environmentally friendly strategies for pest control, the chemical industry to participate in production and commercialization of pheromones, and the public and private sector to promote and support more translational research.

The citrus fruit borer Gymnandrosoma aurantianum Lima (Lepidoptera, Tortricidae) is a representative case for analysis of the economic benefits achieved by the use of a synthetic pheromone to manage this pest in extensive areas. Brazil is the leading worldwide producer of citrus ( USDA, 2015), and Central-Southern Brazil, an area with generalized occurrence of the citrus fruit borer, accounts for approximately 80% of all citrus production in the country ( IBGE, 2015). Females normally deposit a single egg per fruit ( Garcia & Parra, 1999); after eclosion, the larvae pierce the skin and bore into the fruit in order to feed on the pulp ( Fonseca, 1934). Once they have penetrated the fruit, larval control becomes impracticable and the fruit is rendered unfit for consumption ( Bento et al., 2001).

In the 1980s, indiscriminate use of insecticides, especially pyrethroids, against a wide variety of pest insects and mites in citrus orchards in Central-Southern Brazil contributed to a drastic reduction of natural enemies, favoring an increase in the population of G. aurantianum ( Parra et al., 2004). Starting in the 1990s, yield losses due to the citrus fruit borer were estimated at over US$50 million per year ( Anonymous, 2000).

The sex pheromone of G. aurantianum, ( E)-8-dodecenyl acetate and ( E)-8-dodecenol, was identified by members of our group in early 2000’s ( Leal et al., 2001). At that time, Bento et al. (2001) established strategies for its use in the field, including the number of traps per area, trap positioning on trees, pheromone durability, and control level based on number of males collected per week. In November 2001, the Rural Growers Cooperative (Coopercitrus) placed the synthetic pheromone on the market, focusing on citrus growers in the state of São Paulo after an intense campaign to divulge the technology, train extension agronomists, give presentations, and distribute technical bulletins to citrus producers ( Parra et al., 2004).

In this paper, we report a benefit-cost analysis applied to the citrus industry in the period from 2001 to 2013 in the state of São Paulo, Brazil, based on gross revenues (in US$) corresponding to total production (in boxes of oranges) that growers avoided losing by using traps baited with the sex pheromone of the citrus fruit borer G. aurantianum in the monitored areas. We also discuss strategies for pheromone-baited trap use and its efficiency in the management and control of G. aurantianum.

Total losses avoided by using traps baited with sex pheromone of G. aurantianum in the period from 2001 to 2013 ranged from US$132.7 million to US$1.32 billion in gross revenues. In other words, this was the estimated aggregate total of gross revenues from the sale of oranges that growers avoided losing by using pheromone-baited traps, considering a 5–50% range of potential losses caused by citrus fruit borer infestation in citrus orchards in the state of São Paulo ( Table 1; Figure 1). Of note, it is already known that the citrus fruit borer can cause yield losses of up to 50% per tree ( Parra et al., 2004)

The total cost of trap purchases from 2001 to 2013 was US$5,065,807.81 (US$5.06 million). It should be noted that some costs were not measured in this study, such as labor costs of the inspections that used to be performed before the traps became available, and the fact that insecticide spraying was once triggered by a 3–5% yield loss caused by the caterpillars of G. aurantianum ( Gravena, 1998). Therefore, economic losses due to infested fruit were already occurring in the field, as were expenditures on chemical controls (labor, products and machine time) that were extensively used in the entire area of the orchard. Pheromone-baited traps lowered the costs of inspections (labor) in the entire orchard, in addition to reducing the costs of machine operation and insecticide use, as chemical control became targeted only at areas effectively infested with the insect at quantities above the control level. According to Bento et al. (2001), the use of pheromone-baited traps was shown to be efficient because it monitors adults at their mating stage, enabling growers to apply chemical control before oviposition and subsequent damage to fruits. The authors also showed that, when a control level of six or more males/week was adopted, the average percentage of damaged fruits was 0.6% in the monitored areas. In addition, after successive years of trap use, growers achieved a reduction of approximately 50% in insecticide use to control the citrus fruit borer G. aurantianum ( Parra et al., 2004).

The initial investment in the research that resulted in the development of pheromone-baited trap was US$ 50,000. Therefore, in terms of the governmental costs, the benefit-cost ratio of the initial investment (present value of losses avoided/total investment) ranged from US$ 2,655 to 26,548 per dollar spent with a yield loss of 5–50%, respectively ( Figure 2a). In terms of the return for the producer, in which the cost of the traps is included (US$ 5.06 million), the benefit-cost ratio was US$ 12.02 to 120.19 per dollar spent considering yield losses of 5–50% ( Figure 2b). These potential losses were based on an estimation of infestation by G. aurantianum in citrus orchards in the state of São Paulo.

Except for the year 2001, when the sex pheromone of G. aurantianum only became available on the market in November, the area monitored during the 12 subsequent years (2002–2013) ranged from 56,600 to 79,100 hectares of citrus (20.4 to 29.4 million trees), corresponding to 9.7 to 13.5% of the area planted with citrus in the state of São Paulo, the main producing region in Brazil.

These findings reveal a regularity in the sale and use of pheromone-baited traps by citrus growers during that period (2002–2013). Trap sales were relatively stable in that period, with 38,166 units sold per year on average, ranging from 31,970 units (2010) to 47,436 units (2007), possibly due to fluctuations in international prices of orange juice, the main product exported by the Brazilian citrus industry. This regularity suggests a good level of acceptance and application of the technology by growers, and certainly a benefit obtained from its use.

It worth mentioning that, according to Parra et al. (2004), the total volume of insecticide sprayed in the monitored areas fell by at least 50%. This can possibly be explained by the fact that spraying was only performed in areas (~10 ha) where the pest was found at levels exceeding the damage level thus preserving the other areas and, consequently, the natural enemies within them. In summary, the use of pheromone in traps for monitoring populations of the citrus fruit borer in 12 years led to tangible benefits to growers and priceless environmental savings.

The data referenced by this article are under copyright with the following copyright statement: Copyright: � 2016 Bento JMS et al.

Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

F1000Research: Dataset 1. Raw data for Figure 1 and Figure 2, 10.5256/f1000research.9195.d129239 ( Bento et al., 2016).