In recent years, there has been renewed interest in developing more efficient baits and traps for monitoring economically important fruit flies (Diptera: Tephritidae). Even though most resources have been invested in developing Medfly (Ceratitis capitata [Wiedemann]) traps (e.g., Heath et al. 1995, Heath 1996a, Heath 1997;Epsky et al. 1995, Epsky 1999; Katsoyannos et al. 1999a, Katsoynnos 1999b), there have been some interesting trap developments for Anastrepha spp. (Heath et al. 1995, Heath 1997; Thomas et al. 2001), Rhagoletis spp. (Liburd et al. 1998;Prokopy et al. 2000; Stelinski & Liburd 2001), and Toxotrypana curvicauda Gerstaecker (Heath et al. 1996b).

A common theme in the approach followed to develop this new generation of traps has been finding optimal combinations of visual and chemical elements and the desire to find appropriate substitutes for liquid-based traps such as the McPhail (Epsky et al. 1995; Epsky & Heath 1997). Given the need to monitor female numbers in adult fruit fly populations (Casaña-Giner et al. 2001), there has been renewed interest in evaluating protein- and plant-based attractants. Although some of the resulting female-targeted traps have shown promising results (Heath et al. 1997; Epsky et al. 1999; Katsoyannos et al. 1999a, Katsoyannos 1999b), they still have to overcome questions of cost and manageability (e.g., susceptibility of traps to dust or theft). Cost considerations are of paramount importance given the trend toward phasing out large-scale governmental support for fruit fly management, and the subsequent transfer to growers of the responsibility for funding management and eradication programs. The situation in Latin America is particularly critical because large quantities of fruit are still produced by subsistence or resource-poor, small-scale growers who cannot afford expensive monitoring and management tools (Aluja & Liedo 1986; Aluja 1996, Aluja 1999). Furthermore, market niches for organically grown fruit are continuously expanding. As a result, the need for biorational management schemes has become more critical than ever.

In the case of flies in the genus Anastrepha, the challenge for developing a substitute for the McPhail trap is particularly difficult. This liquid-based trap, developed in the early 1900s (McPhail 1937, McPhail 1939), is still widely used throughout Latin America in spite of its inefficiency and high cost (Aluja et al. 1989; Aluja 1999). However, it sometimes outperforms the recently developed dry-based substitutes (e.g., Heath et al. 1995, Heath 1997) because adult flies are attracted to the humid environment in and around it, particularly during the dry season. The biggest challenge in developing an effective substitute to the McPhail trap is the occurrence of at least seven economically important Anastrepha species (A. fraterculus [Wiedemann], A. grandis [Macquart], A. ludens [Loew], A. obliqua [Macquart], A. serpentina [Wiedemann], A. striata [Schiner], and A. suspensa [Loew]; Aluja 1994), and the evidence that not all species respond with equal intensity to a single bait (Aluja et al. 1989). As discussed by Aluja (1999) and Aluja et al. (2001), the most effective Anastrepha attractant will likely end up being a complex aromatic bouquet containing native host fruit and food-based odors, as well as sexual pheromones. Formulating such a lure and assembling a trap that is easy to handle and also visually attractive to all the economically important Anastrepha species will take time. But even if such a trap design is ever produced, its cost may be prohibitive especially given the low purchasing power of the vast majority of fruit growers in Latin America. Therefore, developing cheap, low-tech baits and traps that are easily accessible to local growers should remain a high priority.

An inexpensive alternative fruit fly bait was studied by Hedström (1988) in Costa Rica. This author tested human urine (HU) in a guava orchard, and found that McPhail traps baited with this naturally occurring compound (50% dilution in water) captured 10 times more A. striata andA. obliqua adults than traps baited with the commercially available torula yeast. In a laboratory study with A. ludens, A. obliqua, A. serpentina, and A. striata adults, Piñero et al. (2002) found that responses toward human urine depended on previous diet (e.g., protein-fed adults responded weakly to baits), reproductive state (responses were always greater in sexually mature individuals than sexually immature individuals), and sex (female responses were greater than male responses, particularly for sexually mature individuals) and, importantly, such responses varied among species. More recently, Piñero et al. (2003) determined that McPhail traps baited with human urine captured a high proportion of sexually immature A. obliqua andA. serpentinafemales in a commercial mango orchard (cultivar Manila).

Here, we report the results of a study aimed at determining the attractiveness of three aqueous dilutions of human urine in glass McPhail traps. In an effort to make this study as useful as possible to subsistence or small-scale, resource poor farmers, we tested this naturally occurring compound in four types of environments (guava, grapefruit, mango, and sapodilla orchards), comparing its effectiveness against the commercially available hydrolyzed protein bait (Captor Plus®) and tap water.

Materials and Methods

Results

Discussion

We found that human urine-baited traps were, in certain cases (i.e., guava and sapodilla orchards), similar or superior to protein-baited traps with respect to the total number of adult A. fraterculus, A. obliqua and A. serpentina captured. In other cases (i.e., mango and grapefruit orchards), traps baited with human urine captured fewer adults than traps baited with hydrolyzed protein. We also found that with one exception (sapodilla orchard), human urine concentrations tested did not vary significantly in their attractiveness to flies. The latter has important practical implications as a farmer could fill more traps with a small amount of human urine.

Our results partially confirm those obtained by Hedström (1988). That is, we also found that human urine is attractive to Anastrepha adults, but not to the extent this author did. Some possible explanations for the latter are: (1) differences in the nature of the commercially available baits used by Hedström (torula yeast) and us (hydrolyzed corn protein), (2) possible effect of bait aging since Hedström did not replace the urine contained in traps throughout his study, (3) the ecological characteristics of the study orchard and the fact that A. striata was the predominant species in Hedström’s study (a species not evaluated here), (4) differences in population size, and (5), probable differences in attractiveness of the human urine used in both studies.

The favorable response to human urine shown by A. fraterculus adults in the guava orchard, and in some instances (e.g., sapodilla orchard) by A. obliqua and A. serpentina, suggests that individuals of these Anastrepha species could be responding to nitrogenous compounds such as ammonia present in human urine (Piñero et al. 2003). Given that ammonia plays an important role in attracting fruit flies (e.g., Morton & Bateman 1981; Bateman & Morton 1981;Mazor et al. 1987; Prokopy et al. 1992; Epksy et al. 1995; Heath et al. 1995), and that some ammonium salts (e.g., ammonium acetate or carbonate) and amines (e.g., methylamine, putrescine) are also known to attract adults of    A. suspensa (e.g., Burditt et al. 1983; Thomas et al. 2001), A. striata, A. obliqua (e.g., Hedström & Jiménez 1988), and A. ludens (e.g., Robacker 1995; Robacker et al. 1996; Robacker 1997; Heath et al. 1997; Thomas et al. 2001), a study aimed at identifying the attractive elements of human urine to Anastrepha spp. is, in our opinion, warranted.

Bateman & Morton (1981) and Mazor et al. (1987) clearly demonstrated a close relationship between ammonia concentration and attraction of female C. capitata to protein-based baits. In our case, however, we did not find such an association as all three human urine dilutions were similarly attractive to adult A. fraterculus, A. ludens, A. serpentina and A. obliqua in the guava, grapefruit, and mango orchards. The notable exception was the sapodilla orchard, in which the less-diluted human urine (HU 50%) was significantly more attractive to A. serpentina and A. obliqua than any other human urine dilution. Robacker (1995) found results similar to current data. Liquid baits with different concentrations of ammonia and amines were similar in attractiveness over a range of over 10×, but became less attractive at very high concentrations. The latter can be explained by the fact that pH regulates emission of ammonia, amines, acids, and other ionizable compounds. At pH > 9, emission of ammonia increases greatly and can become repellent, depending on the concentration in the bait. Bateman & Morton (1981) and Mazor et al. (1987), also determined that adult females responded more strongly to baits with pH values between 7 and 8.5, a result later confirmed by Robacker et al. (1993), Robacker & Flath (1995) and Robacker & Bartelt (1997). We note, that such pH values coincided with the pH values found for the three human urine concentrations used in our study (average pH values of approximately 8 in all three cases).

In guava trees, HU25 and HU50 attracted significantly more A. fraterculus females than males and, in the sapodilla orchard, the same baits also attracted more females than males of both A. serpentina and A. obliqua. This agrees with previous results found for A. serpentina in a mango orchard (Piñero et al. 2003), and in a laboratory setting (Piñero et al. 2002). Given that Piñero et al. (2002) controlled the proportion of females and males in the experimental population, we are confident that our results in the field do not reflect a situation in which more females than males were present and as a consequence, more females were captured. Furthermore, in our study HU25 attracted a large proportion of sexually immature A. serpentina females when tested in the sapodilla orchard.

Interestingly, we found important differences in the response to human urine by A. obliqua and A. serpentina adults according to the type of orchard and other conditions prevalent where trapping was performed. For example, in the mango orchard (1996), traps baited with hydrolyzed protein captured the highest numbers of both A. serpentina and A. obliqua adults. In contrast, in the sapodilla orchard (1997) traps baited with HU50 captured more adults of both species than protein-baited traps. Since the two orchards are adjacent to each other, we believe that such differences might be due to variations in the type, abundance, and quality (i.e., nutritional value) of host fruits, both within and outside the orchards (e.g., presence of wild hosts). For instance, at the time the study was carried out in the mango orchard, there was very little fruit left on trees, and there was no fruit available in the contiguous sapodilla orchard. Thus, the higher capture of A. serpentinaadults in protein-baited traps (when compared to urine-baited traps) may be explained in terms of protein hunger, since sapodilla fruit is an important protein source for A. serpentina adults (Jácome et al. 1999). In contrast, when trapping took place in the sapodilla orchard (in 1997), fruit was abundant and traps baited with hydrolyzed protein were not as attractive to adult A. serpentina as urine-baited traps. This clearly illustrates that the effectiveness of an attractant depends on the prevailing ecological conditions in a given orchard (Robacker 1992; Celedonio-Hurtado et al. 1995; Heath et al. 1997; Epsky et al. 1999), as well as on adult physiological state (Robacker 1991; Robacker et al. 1996; Rull & Prokopy 2000; Piñero et al. 2002). The latter aspects, in addition to others such as annual variations in adult fly populations in fruit orchards (Aluja et al. 1996), must be considered in the design of fruit fly monitoring systems and underscores the challenge faced by those trying to develop a replacement for the McPhail trap for use in orchards in which flies in the genus Anastrepha are predominant.

As a final point, we would like to address the economic benefit of using cost-free human urine. In Mexico, the value of a liter of a commercially available protein-based bait (e.g., Captor Plus®) is approximately USD $6.00 (10.9/1 US dollars/Mexican peso). Considering that each trap is baited with 10-40 ml of bait diluted per liter of water, the cost of the bait per trap is USD $0.06-0.20. The latter multiplied by 52 (weeks in a year) raises the cost of the bait per trap per year to ca. USD $3.10-10.40 (average of $6.75). Considering that in Mexico a glass McPhail trap costs USD $4.00, and the placement of 10-20 traps in an orchard (USD $40.00-80.00), the total cost of trap placement and servicing per year would range between USD $46.75 and 86.75 or ca $510.00-945.00 Mexican pesos (not considering salaries). In the case of commercially available Anastrepha spp. synthetic lures (multi-component lure) and yellow plastic traps the cost in the US (not considering handling and shipping charges to Mexico) ranges between USD $3.30-4.50 and 8.50 per dispenser (lure) and trap, respectively (Great Lakes IMP, Vestaburg, MI; IPM Technologies, Portland, OR). All the latter would be unmanageable for a subsistence farmer (one that uses all his fruit for self-consumption) and hard to handle for a small-scale producer selling fruit locally. Therefore the alternative of using a cost-free bait like human urine becomes highly attractive.

In conclusion, we believe that human urine represents a low-tech alternative Anastrepha bait for subsistence or low income, small-scale fruit growers in rural areas in Latin America who cannot afford costly inputs such as commercial baits and traps. Human urine was capable of attracting adult flies of various species of Anastrepha and, at least in two orchards (guava and sapodilla), it performed as well as, or even better, than a commercially available protein bait. Even though in some instances human urine did not attract as many flies as hydrolyzed protein, qualitatively it proved to be equal or superior to this bait (i.e., it usually attracts more females than males and a large proportion of sexually immature females). A poor farmer would have access to a cost-free trap by simply reusing a two-liter plastic bottle of a soft drink or serum flask (see Salles 1996) and filling it with human urine diluted in water. There will sometimes be a trade off between cost and trap quality/efficiency, but for growers accustomed to regularly loosing between 60 to 100% of their harvest because of fruit fly damage, the benefit of a cheap, low-technology and relatively efficient trap would be very valuable. If such growers could be alerted in a timely fashion of an increasing influx of flies into their orchards or backyard gardens from surrounding native vegetation, they could protect their fruit by, for example, bagging it (Fang 1989). Further, if the bait is particularly attractive to sexually immature females, even a low capture rate could reduce fruit damage to the extent of allowing the production of a certain proportion of clean fruit (i.e., free of larvae) for local markets. One should keep in mind that the principal objective of peasant farmers in Latin America is not to produce fruit for export markets but for in-house consumption or local markets that do not demand blemish-free products.