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Human Urine and Chicken Feces as Fruit Fly (Diptera: Tephritidae) Attractants for Resource-Poor Fruit Growers

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We evaluated human urine and chicken feces, two naturally occurring, inexpensive, and readily available substances, as baits for the capture of Anostrepha spp. (Diptera: Tephritidae) by using glass McPhail traps. Two studies were performed simultaneously in a commercial mango orchard in Veracruz, México. In the first study, we compared a 50% water dilution of human urine against hydrolyzed protein, both compounds at the fresh and 5-d-old stages, and water alone (control treatment). In the second study, we tested fresh chicken feces mixed with water, a torula yeast/borax solution at three different ages (1-4, 5-9, and 10-15 d), and water (control treatment). Both human urine and chicken feces were attractive to Anastrepha adults compared with water alone, but attracted two and three times fewer adults than hydrolyzed protein and torula yeast/borax, respectively. However, unlike torula yeast/borax, aging of human urine did not decrease its attractiveness. Five-day old human urine attracted numerically more A. serpentina females than males, similar numbers of A. obliqua males and females, and significantly more sexually immature A. obliqua females than mature ones. Chicken feces proved to be as attractive as the aged torula yeast/borax treatments for A. obliqua and A. serpentina. We argue that because both human urine and chicken feces are cost-free and can be easily obtained, they are viable, low-technology alternatives to costly commercial attractants, particularly for low-income growers or backyard farmers in Mexico and other Latin American countries.
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ECOLOGY AND BEHAVIOR
Human Urine and Chicken Feces as Fruit Fly (Diptera: Tephritidae)
Attractants for Resource-Poor Fruit Growers
JAIME PIN
˜ERO,
1
MARTI
´N ALUJA,
1
ALEJANDRO VA
´ZQUEZ,
1
MIGUEL EQUIHUA,
1
AND JORGE VARO
´N
2
Instituto de Ecologõ´a, A.C. Apartado Postal 63, 91000 Xalapa, Veracruz, Me´xico
J. Econ. Entomol. 96(2): 334Ð340 (2003)
ABSTRACT Weevaluatedhuman urine and chicken feces, two naturally occurring, inexpensive, and
readily available substances, as baits for the capture of Anastrephaspp. (Diptera: Tephritidae) by using
glass McPhail traps. Two studies were performed simultaneously in a commercial mango orchard in
Veracruz, Me´xico. In the Þrst study, we compared a 50% water dilution of human urine against
hydrolyzed protein, both compounds at the fresh and 5-d-old stages, and water alone (control
treatment). In the second study, we tested fresh chicken feces mixed with water, a torula yeast/borax
solution at three different ages (1Ð4, 5Ð9, and 10Ð15 d), and water (control treatment). Both human
urine and chicken feces were attractive to Anastrepha adults compared with water alone, but attracted
two and three times fewer adults than hydrolyzed protein and torula yeast/borax, respectively.
However, unlike torula yeast/borax, aging of human urine did not decrease its attractiveness. Five-day
old human urine attracted numerically more A. serpentina females than males, similar numbers of
A.obliqua males and females, and signiÞcantly more sexually immature A. obliqua females than mature
ones. Chicken feces proved to be as attractive as the aged torula yeast/borax treatments for A.obliqua
and A. serpentina. We argue that because both human urine and chicken feces are cost-free and can
be easily obtained, they are viable, low-technology alternatives to costly commercial attractants,
particularly for low-income growers or backyard farmers in Mexico and other Latin American
countries.
KEY WORDS Anastrepha, Tephritidae, attractants, human urine
AMMONIA IS USED BY several species of fruit ßies
(Diptera: Tephritidae) to locate food and/or ovipo-
sition resources (Bateman and Morton 1981, Mazor et
al. 1987, Epsky and Heath 1998, Robacker 1995,
Robacker and Heath 1996, Hull and Cribb 2001).
Sources of ammonia for potential use as fruit ßy baits
include proteins (Baker et al. 1944, Steiner 1952),
emissions from bacteria (Robacker and Flath 1995,
Robacker and Moreno 1995, Robacker and Bartelt
1997,Robackeret al. 1998, Epsky et al. 1998), and avian
feces (Prokopy et al. 1993, Epsky et al. 1997, Robacker
et al. 2000). Recent investigations on ammonia deriv-
atives have yielded some commercial food-based syn-
thetic lures that have been shown to be particularly
attractive to Anastrepha ludens (Loew) and A. sus-
pensa (Loew). Such ammonia-derived baits include
AMPu (a blend of ammonium bicarbonate, methyl-
amine hydrochloride and 1,4 diaminobutane
[putrescine]) (Robacker and WarÞeld 1993), and
BioLure (a mixture of ammonium acetate and pu-
trescine; Consep Inc., Bend, OR) (Heath et al. 1995,
Thomas et al. 2001). AMPu has been shown to be as
effective as torula yeast (Robacker 1995), and more
attractive than different combinations and concentra-
tions of its own constituents and other amines
(Robacker et al. 1996, 1997). However, in spite of the
fact that some of these food-based synthetic lures
(including the traditional, commercially available hy-
drolyzed protein and torula yeast/borax) have been
proven attractive to some Anastrepha species, the
prospects on their use by low-income Latin American
growers are limited because of cost and accessibility
considerations. The majority of these growers are rep-
resented by subsistence farmers, which require inex-
pensive alternatives for monitoring fruit ßy popula-
tions (Aluja and Liedo 1986; Aluja 1996, 1999).
Two of the most promising, low-cost alternative
baits that have been investigated recently are human
urine and chicken and duck droppings (Hedstro¨m
1988, Prokopy et al. 1993, Epksy et al. 1997, Robacker
et al. 2000). Human urine also releases ammonia (Bell
et al. 1961, Langley 1971, Anonymous 1981), and has
been tested as a potential attractant for Anastrepha
spp. by Hedstro¨m (1988) under Þeld conditions and
by Pin˜ero et al. (2002) in the laboratory with encour-
aging results. Similarly, chicken droppings, which also
1
E-mail: alujam@ecologia.edu.mx.
2
Facultad de Agronomõ´a, Universidad Nacional de Colombia, sede
Santa Fe´de Bogota´, Colombia.
0022-0493/03/0334Ð0340$04.00/0 !2003 Entomological Society of America
release ammonia, were more attractive than the
widely used proteinaceous attractant PIB-7 (Staley
Manufacturing Co., Decatur, IL) when tested in Ha-
waii with the Mediterranean fruit ßy (Prokopy et al.
1993).
Our aim in this study was to test, under Þeld con-
ditions, the attractiveness to wild Anastrepha spp.
adults of human urine and chicken feces compared
with hydrolyzed protein and torula yeast/borax. Our
long-term goal is to Þnd readily accessible and inex-
pensive low-tech attractants for use in fruit ßy mon-
itoring and control programs in rural areas of Mexico
and other Latin American countries. In these regions,
low-income growers do not produce fruit for national
or international markets, and instead harvest some
clean fruit for in-house consumption or for less-lucra-
tive local markets. Thus, inexpensive traps will be
welcome even if they are not as effective as commer-
cial, high-technology traps.
Materials and Methods
Study Site. Studies were conducted in Apazapan,
Veracruz, Me´xico, from June to August 1993. The
study site is located at 19!19"northern latitude and
96!42"western longitude, at 340 m above sea level.
Climate is characterized as Aw(W)(i)g (hot, subhu-
mid according to Ko¨ppens classiÞcation system mod-
iÞed by Garcõ´a 1981). Mean annual temperature in
Apazapan is 25.5
!
C and annual rainfall 1,250 mm.
Tests were conducted in an unsprayed commercial
mango orchard (Mangifera indica L.) ÔManilaÕ. We
selected 10 trees with similar dimensions (height, #10
m, canopy diameter, #9 m), that were #20 m apart
within the orchard. Of these 10 trees, Þve were used
to test human urine and hydrolyzed protein (study 1),
and the rest to test chicken feces and torula yeast/
borax (study 2). For experiments with human urine,
we used hydrolyzed protein because it is the most
commonly used fruitßy bait in Mexico and other Latin
American countries. We used torula yeast/borax as a
positive control in the second experiment to deter-
mine whether a cost-free and readily available sub-
stance such as chicken feces could substitute this ex-
pensive bait.
Bait Treatments. In study 1, we evaluated fresh
human urine, 5-d-old human urine, fresh hydrolyzed
protein (Captor Plus; Agroquõ´mica Tridente, S.A. de
C.V. Me´xico, D.F.), 5-d-old hydrolyzed protein, and
tap water (negative control). Human urine was tested
at a concentration of 50% (100 ml of human urine in
100 ml of water) (same concentration used by Hed-
stro¨m 1988). Hydrolyzed protein contained no borax
and wasprepared in a 1:10 dilution. Five-day-old treat-
ments were evaluated to test the effect of aging on
attractiveness. The human urine was from a single
26-yr-old donor (JP), whose diet excluded coffee,
alcohol, vitamin supplements, spicy food condiments,
and tobacco. This diet was maintained throughout the
study period and started 15 d before initiation of trap-
ping. The urea and ammonia contents fell well within
normal ranges (20Ð30 g/100 ml and 0.5Ð0.9 g/100 ml,
respectively; Bell et al. 1961, Anonymous 1981) for a
healthy individual. The complete results of this anal-
ysis are presented in Pin˜ero et al. (2002). Even though
therecan be variabilityin the chemical composition of
human urine because of factors such as age and the
quality and quantity of food ingested (Bell et al. 1961,
Langley 1971, Anonymous 1981), the two components
relevant to us (urea and ammonia), varied relatively
little.
In study 2, bait treatments tested were torula yeast/
borax pellets ERA International, Ltd., Brownsville,
TX) aged over 1Ð4, 5Ð9, or 10Ð15 d, a mixture of fresh
chicken feces and water, and tap water as a negative
control treatment. Torula baits were prepared by dis-
solving four pellets of torula yeast/borax in 200 ml of
water. Pellets weighed #5 g each and torula yeast/
boraxproportion was 4:5. The chicken feces treatment
was prepared by mixing 50 g of fresh chicken feces
(obtained from a local commercial chicken farm the
same days we baited the traps) in 150 ml of water.
Trapping. In each one of the 10 mango trees se-
lected we placed Þve McPhail traps (a total of 50
traps), baited with200 ml of the above-mentioned bait
treatments. Traps were placed in the internal part of
the tree canopies, at #2 m from the periphery. Every
3 d, all ßies captured by traps were removed and
placed in plastic containers containing alcohol (70%)
for their identiÞcation. All traps were then cleaned,
rebaited, and rehung in the trees. Trap position was
rotated every 3 d clockwise within the tree canopies
using a systematic procedure. During every trap-re-
view session we also measured the pH values of Þve
samples (one for each treatment) with a pH tester
(model 59000Ð20; Cole Parmer, Chicago, IL). Overall,
21 trap inspections were performed. All adults cap-
tured were identiÞed to species with the help of an
expert taxonomist (Vicente Herna´ndez-Or´z, Insti-
tuto de Ecologõ´a, A.C.). Females were dissected using
a stereomicroscope to determine the stage of sexual
maturity after the procedures described by Martõ´nez
et al. (1995).
Data Analysis. Data for each study were analyzed
separately. The response variable used was the index
ßies/trap/day, which expresses the daily number of
adults captured per trap (Aluja 1993). To determine
the effect of attractants on captures of A. obliqua and
A. serpentina adults which represented most adults
captured in both studies, we performed an analysis of
variance (ANOVA),on transformed data (square-root
of each value plus 0.5) to homogenize variances, and
followed by a Fisher least signiÞcant difference (LSD)
separation of means procedure (P$0.05). Compar-
isons of pH values were performed separately for each
study by means of ANOVA and LSD tests. For each
species and treatment, we compared the number of
females versus males, and the number of sexually ma-
ture versus immature females captured by traps using
a nonparametric MannÐWhitney Utest. All analyses
were performed using the software Statistica (StatSoft
1999).
April 2003 PIN˜ERO ET AL.: HUMAN URINE AND CHICKEN FECES AS FRUIT FLY ATTRACTANTS 335
Results
Bait pH Values. In study 1, average pH values of
both human urine and hydrolyzed protein were not
affected by age, though pH values of both types of
human urine were signiÞcantly higher than those de-
termined for hydrolyzed protein (ANOVA: F$38.2;
df $4, 100; P%0.001) (Fig. 1). In study 2, average pH
values of all torula yeast/borax treatments were
similar, regardless of their age, but pH of chicken
feces was signiÞcantly lower than that of torula
yeast/borax (ANOVA: F$317.0; df $4, 100; P%
0.001) (Fig. 1).
Number of Flies Captured. In study 1, 2,705 adults
of seven Anastrepha species were captured. A. obliqua
was by far the most abundant species, representing
86.9% of total captures, followed by A. serpentina
(11.7%). The other Þve species (A. alveata Stone, A.
chiclayae Greene, A. ludens, A. pallens Coquillett, and
A. striata Schiner) represented 1.4% of the total num-
ber of ßies captured.
Trapsbaited witheither fresh or 5-d-old hydrolyzed
protein captured signiÞcantly more A. obliqua and
A. serpentina adults than human urine-baited traps,
independently of age. All protein and human urine
treatments attracted signiÞcantly more ßies than wa-
ter alone (ANOVA F$17.3; df $4, 495; P%0.001; and
F$10.78; df $4, 495; P%0.001 for A. obliqua and A.
serpentina, respectively) (Fig. 2, study 1).
Fig. 1. pH values (mean &SE) of bait treatments used in both studies: fresh and 5-d-old human urine, fresh and 5-d-old
hydrolyzed protein, and water (study 1), and 1Ð4-, 5Ð9-, and 10Ð15-d-old torula yeast/borax, chicken feces, and water (study
2). Within each study, columns with the same letter are not signiÞcantly different from one another (ANOVA,
!
$0.05; LSD
test).
Fig. 2. Number (mean ßy/trap/d values &SE) of A.obliqua and A.serpentina adults captured by McPhail traps baited
with either fresh and 5-d-old human urine, fresh and 5-d-old hydrolyzed protein, and water (study 1), or 1Ð4-, 5Ð9-, and
10Ð15-d-old torula yeast/borax, chicken feces, and water (study 2). For each study, data were analyzed separately by ßy
species. Columns withthe same letter within a species andstudy site arenot signiÞcantlydifferent from oneanother (ANOVA,
!
$0.05; LSD test).
336 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 2
In study 2, 3,872 adults of six Anastrepha species
were caught by traps. A. obliqua represented 86.3% of
the total captures, followed by A. serpentina (12%); A.
alveata, A. chiclayae, A. ludens, and A. zuelaniae Stone
represented 1.7% of the total number of ßies captured.
We found a decrease in A. obliqua and A. serpentina
captures as the age of the torula yeast/borax bait
increased. Traps baited with 1Ð4-d-old torula yeast/
borax captured the highest numbers of adults of both
species, followed by traps baited with 5Ð9-d-old torula
yeast/borax. For both species, the chicken feces treat-
ment was found to be as attractive as the 10Ð15-d-old
torula yeast/borax bait (ANOVA F$12.1; df $4, 495;
P%0.001; and F$11.0; df $4, 495; P%0.001, for A.
obliqua and A. serpentina, respectively). Water-baited
traps captured no ßies during the entire study (Fig. 2,
study 2).
Adult Captures According to Sex. In study 1, all bait
treatments that captured ßies attracted statistically
similar numbers of A. obliqua males and females (Ta-
ble 1, study 1). Both fresh and 5-d-old human urine
attracted numerically more A. serpentina females than
males. In study 2, all bait treatments attracted signif-
icantly more A. obliqua females than males and similar
numbers (no statistical difference) of A. serpentina
females and males (Table 1, study 2).
Sexual Maturity Stage of Captured Females. The
proportion of females caught by traps in study 1, ac-
cording to their stage of sexual maturation, is shown in
Table 2. All bait treatments attracted signiÞcantly
more sexually immature than mature A. obliqua fe-
males. Traps baited with fresh human urine and fresh
and 5-d-old hydrolyzed protein captured signiÞcantly
more immature than mature A. serpentina females. In
study 2, 1Ð4- and 5Ð9-d-old torula yeast/borax at-
tracted signiÞcantly more immature than mature A.
obliqua females (Table 2, study 2). For A. serpentina,
all torula-based treatments and chicken feces at-
tracted numerically, but not statistically, more imma-
ture than mature females.
Discussion
We found that human urine-baited traps captured
fewer A. obliqua and A. serpentina than protein-baited
traps. There are at least four plausible explanations for
this. First, human urine may be intrinsically less at-
tractive than hydrolyzed protein. Second, the human
urine concentration tested may have exerted some
degree of repellency, as documented by Mazor et al.
(1987) and Robacker et al. (1997) working with C.
capitata and A. ludens, respectively. In both studies, a
negative association was demonstrated between am-
monia concentration and attractiveness to adults. To
address this question, we performed a follow-up study
to determine whether concentration of human urine
had an effect on its attractancy to ßies in the genus
Anastrepha (M. Aluja and J. Pin˜ero, unpub. data). We
found, however, that in most experiments there were
no differences in captures among the three human
urine dilutions tested (50, 25, and 12.5%), and in one
experiment the 50% concentration was the most at-
tractive for A. serpentina and A. obliqua in a sapodilla
orchard, even compared with hydrolyzed protein. In
Table 1. Number of A. obliqua and A. serpentina adults cap-
tured by McPhail traps baited with either fresh and 5-d-old human
urine; fresh and 5-d-old hydrolyzed protein (study 1); or 1-4-, 5-9-,
and 10-15-d-old torula yeast/borax and chicken feces (study 2),
according to the species, bait treatment, and sex. For each bait
treatment and species, statistical comparisons between sexes were
performed using Mann-Whitney Utests (
!
"0.05)
Bait treatment n%
Females
%
Males Pvalues
Study 1
A. obliqua
Fresh human urine 403 55.6 44.4 0.25
5-d-old urine 341 62.8 37.2 0.17
Fresh protein 890 53.5 46.5 0.60
5-d-old protein 716 49.0 51.0 0.92
A. serpentina
Fresh human urine 46 65.2 34.8 0.14
5-d-old urine 52 65.4 34.6 0.07
Fresh protein 117 46.1 53.9 0.67
5-d-old protein 101 61.4 38.6 0.14
Study 2
A. obliqua
1Ð4-d-old Torula 1,274 65.5 34.5 0.02
5Ð9-d-old Torula 992 74.2 25.8 0.008
10Ð15-d-old Torula 674 72.3 27.7 0.01
Fresh chicken feces 402 61.9 38.1 0.03
A. serpentina
1Ð4-d-old Torula 171 47.4 52.6 0.34
5Ð9-d-old Torula 133 39.1 60.9 0.29
10Ð15-d-old Torula 61 36.1 63.9 0.11
Fresh chicken feces 98 41.8 59.2 0.34
Table 2. Number of A. obliqua and A. serpentina females
captured by McPhail traps baited with either fresh and 5-d-old
human urine; fresh and 5-d-old hydrolyzed protein (study 1); or
1– 4-, 5–9- and 10–15-d-old torula yeast/borax and chicken feces
(study 2), according to the sexual maturity stage. For each bait
treatment and species, statistical comparisons between sexually
immature and mature females were performed using Mann-Whitney
Utests (
!
"0.05)
Bait treatment n%
Immature
%
Mature Pvalues
Study 1
A. obliqua
Fresh human urine 207 75.7 24.3 0.008
5-d-old urine 201 76.6 23.4 0.01
Fresh protein 399 79.9 20.1 0.009
5-d-old protein 303 76.3 23.7 0.009
A. serpentina
Fresh human urine 27 75.0 25.0 0.02
5-d-old urine 31 67.7 32.3 0.45
Fresh protein 40 80.0 20.0 0.04
5-d-old protein 50 76.0 24.0 0.02
Study 2
A. obliqua
1Ð4-d-old Torula 835 62.1 37.9 0.03
5Ð9-d-old Torula 487 61.5 38.5 0.04
10Ð15-d-old Torula 349 51.3 48.7 0.53
Fresh chicken feces 256 55.2 44.8 0.24
A. serpentina
1Ð4-d-old Torula 90 65.5 34.5 0.11
5Ð9-d-old Torula 81 63.0 37.0 0.09
10Ð15-d-old Torula 39 57.5 42.5 0.66
Fresh chicken feces 57 66.7 33.3 0.09
April 2003 PIN˜ERO ET AL.: HUMAN URINE AND CHICKEN FECES AS FRUIT FLY ATTRACTANTS 337
addition, Hedstro¨m (1988) suggested that human
urine at a 50% concentration did not exert any repel-
lent effect to A. obliqua and A. striata adults; in con-
trast, they found that such a concentration of human
urine attracted 10 times more adults of each species
than torula yeast/borax inCosta Rica,even though the
same urine was used over several weeks (without
replacement). Third, pH could have played a role in
rendering hydrolyzed protein and torula yeast/borax
more attractive than human urine and chicken feces,
because pH values of human urine and chicken feces
were signiÞcantly different than those of hydrolyzed
protein and torula yeast/borax. To address this issue,
we plan to conduct a subsequent study in which pH
values of both chicken feces and human urine will be
artiÞcially manipulated and their attractiveness com-
pared to hydrolyzed protein of equal alkalinity.
Fourth, it could be that the ecological characteristics
of the orchards inßuence the degree of response of
ßies in the genus Anastrepha to food-based attractants.
Also, the physiological state of adults (Rull and
Prokopy 2000, Pin˜ero et al. 2002) have to be consid-
ered in the design of more efÞcient monitoring sys-
tems and in the election of appropriate baits.
Herein, fresh human urine attracted large numbers
of A. obliqua and A. serpentina females. A similar trend
was observed in the case of chicken feces for A. obli-
qua. Thus, both human urine and chicken feces could
be considered female-targeted baits. The problem
with such an interpretation is that the proportion of
males and females in the Þeld were not determined
and this leaves the possibility open to the fact that
more females than males were present at the moment
the study was conducted. But despite the fact that we
acknowledge the latter to be a possibility, unrelated
work by one of us (MA) in which thousands of pupae
were collected from Þeld-infested fruit in two differ-
ent localities (Veracruz and Chiapas, Mexico) re-
vealed that the proportion of Anastrepha females and
males emerging from such puparia was consistently
close to 50:50% (M. Aluja, unpub. data). Furthermore,
recent work by Robacker (1999) and Pin˜ero et al.
(2002), in which female/male proportion was con-
trolled during experiments, reveal that baits such as
BioLure, or Captor Plus (hydrolyzed protein), are
indeed more attractive to females than males.
The decrease we found in A. obliqua and A. serpen-
tina captures associated with the age of the torula
yeast/borax solution had been observed previously by
Epsky et al. (1994) with A. suspensa. These authors,
also working with torula, found that the attractiveness
of this bait decreased signiÞcantly as the lure aged.
First, we thought that this result could be attributed to
bait pH, as found by Bateman and Morton (1981)
when evaluating ammonium bicarbonate with Bactro-
cera tryoni (Froggatt) and by Robacker et al. (1993),
Robacker and Flath (1995), and Robacker and Bartlet
(1997) when testing bacteria Þltrates or cultures with
A. ludens and other Anastrepha species. But, contrary
to our expectation, our results indicate that the aging
process of baits did not affect signiÞcantly their pH
values and therefore, other factors mustbe inßuencing
differences in attractiveness.
Considering the combined results of studies 1 and 2,
there seems to be an indication of a species-speciÞc
response to certain baits. Aluja (1999) and Aluja et al.
(1989, 2001) addressed the possibility that not all of
the adults of various Anastrepha species respond with
equal intensity to a particular bait. Such differences
may be due, in part, to different nutritional require-
ments of adults. Pin˜ero et al. (2002) found that, under
laboratory conditions, adults of four Anastrepha spe-
cies showed differentialresponses to human urine and
hydrolyzed protein, and that at the individual level,
responses were signiÞcantly affected by the physio-
logical state (e.g., feeding history and age) of the
adults. For example, responses toward protein baits
decreased when adults had fed on an open fruit (an
important source of protein according to Ja´come et al.
1999). It has also been demonstrated that, even within
species, different responses to closely related volatiles
can be found. For example, Robacker and WarÞeld
(1993) reported that A. ludens adults responded dif-
ferently to ammonia and methylamine which share
some chemical properties. Likewise, Prokopy et al.
(1993) found different responses of C. capitata adults
to bird feces and mammal droppings, probably a result
of the type of volatiles emitted by such droppings,
because uric acid is one of the main products of bird
catabolism and urea is one of the most important
excretory products of mammal catabolism (Prosser
1991). The latter also could explain, in part, the higher
attraction of A. serpentina adults to bird feces com-
pared with human urine, though the same might not
be true for A. obliqua.
In conclusion, our Þndings herein, combined with
those of Hedstro¨m (1988), Epsky et al. (1997), and
Pin˜ero et al. (2002) indicate that human urine and
chicken feces are indeed attractive to Anastrepha
adults. Although in this study traps baited with human
urine and chicken feces captured fewer A. obliqua and
A. serpentina adults than traps baited with hydrolyzed
protein and torula yeast/borax,these inexpensive, nat-
urally occurring substances seem to have some posi-
tive attributes. In a relatively short period (#90 d),
inefÞcienttraps such as the McPhail, baited with these
compounds, captured 779 females. For a poor farmer,
who is accustomed to losing all or a large proportion
of their crop because of fruit ßy damage, it would be
advantageous to have fewer ovipositing females in a
population. Also, being able to gauge population num-
bers and the time at which adult ßies move into the
orchard from surrounding native vegetation will allow
a grower to strategically time cultural practices such
as fruit bagging (Fang 1989). A poor farmer could have
access to a cost-free trap by simply reusing a 2-liter
plastic bottle of a soft drink (Salles 1996) with the
appropriate dilution of human urine or chicken or
duck feces (Robacker et al. 2000). When judging the
potential of human urine and chicken feces as fruit ßy
baits we should keep in mind that the end goal of this
type of research is to develop low-technology baited
traps for resource-poor farmers who are not able to
338 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 2
monitor ßy populations because commercially avail-
able baits and traps are too expensive. If inexpensive
or cost-free alternative baits and traps end up not
being as effective as the commercially available ones,
they could still be very useful for millions of small-
scale fruit growers in Latin America.
Acknowledgments
We thank Vicente Herna´ndez-Ortõ´z for help during the
identiÞcation process of Anastrepha adults. We alsothank the
technical supportprovidedby Isabel Ja´come, Enrique Piedra,
and Alberto Zu´n˜iga. We express gratitude to Nancy Epsky
(USDA-ARS),Ronald J. Prokopy,Juan Rull-Gabayet, Starker
Wright, Sara Hoffmann (University of Massachusetts, Am-
herst), and Francisco Dõ´az-Flesicher and Diana Pe´rez-Sta-
ples (Instituto de Ecologõ´a, A.C.) for reviewing an early
version of thismanuscript. Financialsupport wasprovidedby
the Secretary of Public Education (SEP) (Reg. DGICSA-
913096), the National Council for Science and Technology
(CONACyT)(Reg. 0702-N9109),and the Campan˜a Nacional
Contra Moscas de la Fruta (Agreement SAGARPA-IICA).
We thank the United States Department of Agriculture
(USDA-ARS-PPQ, facilities in Mexico City), for providing
torula yeast/borax pellets.
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340 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 2
... These pellets were developed in the 1970s (López et al., 1971). The torula pellets have often been used for comparative studies of fruit fly attractants and have proved to be as attractive or more attractive than other food-based lures for species including A. obliqua (Piñero et al., 2003;Thomas et al., 2008), A. suspensa (Burditt, 1982;Epsky et al., 1993), Anastrepha ludens Loew (Conway & Forrester, 2007;Heath et al., 1994;Mangan & Thomas, 2014;Thomas & Robacker, 2006), Anastrepha serpentina Wiedemann (Piñero et al., 2003), ...
... These pellets were developed in the 1970s (López et al., 1971). The torula pellets have often been used for comparative studies of fruit fly attractants and have proved to be as attractive or more attractive than other food-based lures for species including A. obliqua (Piñero et al., 2003;Thomas et al., 2008), A. suspensa (Burditt, 1982;Epsky et al., 1993), Anastrepha ludens Loew (Conway & Forrester, 2007;Heath et al., 1994;Mangan & Thomas, 2014;Thomas & Robacker, 2006), Anastrepha serpentina Wiedemann (Piñero et al., 2003), ...
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The production and trade of fresh fruit is currently increasing in Africa, as is the movement of people into and within the region. This increases the risk of new fruit fly invasions. The increase in production of fresh fruit also requires for more effective management of established insect pests like fruit flies in order to maximise yield and facilitate trade. It is imperative, therefore, that effective fruit fly detection and monitoring systems are developed, set up and maintained in Africa in order to protect and expand the fresh fruit sector which brings income and employment to the region. Effective trapping systems have been developed for many fruit fly pests and they enable the early detection and monitoring of these pests. However, for a number of important established fruit fly pests in Africa, notably in the Dacus group, trapping systems are yet to be developed and optimised. Moreover, new recently developed fruit fly attractants have yet to be tested on African species.
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Adult tephrids require sugar and protein for survival and for development of eggs, and volatile chemicals from these substances are the basis for food-based lures developed as baits for these pests. In this chapter, we discuss food-based lures that mimic food sources for adults other than host fruit. These have been primarily nitrogen sources that provide the protein needed by adult flies, although non-nitrogen-containing volatile chemicals are also included in this category. After male lures, food-based lures have been the predominant attractants used in traps for tephritid fruit flies. Although typically not as powerful as male lures, food-based lures have several advantages over male-specific attractants. They can be used for species for which there are no male lures known; they capture both females and males of target species; they tend to be female-biased, that is, they capture a higher percentage of females than males; and, at least for the Mediterranean fruit fly, traps baited with food-based lures tend to capture flies earlier than traps baited with male lure. There has been a long history of research on the development of food-based attractants for pest tephritids. Several review articles have documented the early history, which started with investigations of sugar-based food lures and lead to the development of the liquid protein baits and synthetic protein-based food lures, the standard food-lures that are currently in use. In this chapter, we discuss the development of and, as much as possible, the diversity of food-based lures that have been tested and/or are used in traps for pest tephritids. Future research directions are also discussed.
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Pi ñero, J., M. Aluja, M. Equihua and M. M. Ojeda. 2002. Feeding history, age and sex influence the response of four economically importan! Anastrepha species (Díptera: Tephritidae) to human urine and hydrolyzed protein. Folia Entamo/. Mex., 41(3): 283-298. ABSTRACT. We studied the effect of dietary history and age on the response of Anastrepha /udens, A. obliqua, A. serpentina and A. striata (Díptera: Tephritidae) females and males to two types offood baits: human urine and hydrolyzed protein, both at the fresh and 5 day old stages. Baits were offered simultaneously to flies with water as the control treatment. Diets offered (along with water) to adults at the moment of emergence were either 1) sucrose, 2) a mixture ofsucrose and protein, 3) sucrose plus bird feces, 4) an open fruit, or 5) water alone. Adults evaluated were either sexually immature (unmated, 2-3 day old) or mature (presumably mated, 16-20 day old). For each ofthe four species, adult responses to the baits varied as a function ofage, sex and feeding history. Responses were always greater for sexually mature individuals (primarily females) when compared to sexually immature individuals. Feeding regime influenced the response of sexually immature males and fe males of all four species. The response of sexually immature individuals toward the baits was both weak (particularly when adults were fed on either open fruit ora mixture of sucrose and protein) and non-selective. Sexually mature protein-fed A. ludens andA. striata males and fe males exhibited a weak response to pro te in baits. Open fruit elicited a strong response to the baits in sexually mature A. ludens andA. serpentina females. Fresh and 5-day old urine baits were attractive to sexually mature A. /udens females, regardless of adult feeding history. Human urine was particularly attractive to sucrose-fed, A. striata females, and hydrolyzed protein was more attractive than urine toA. striata females that had previously fed on a combination ofsucrose and bird feces. We conclude that adult responses toward different baits strongly depend on sex, adult diet, and reproductive state, and that such responses vary substantially among species. These findings have importan! practica! implications with respectto fruit fly monitoring and control.
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Trap/lure combinations were tested against populations of Anastrepha suspensa (Loew) and Anastrepha ludens (Loew) as substitutes for the traditional glass McPhail trap. Open-bottom, plastic traps baited with a two component synthetic lure (ammonium acetate and putrescine) caught as many and sometimes more fruit flies than the McPhail trap baited with torula yeast. Sex ratio of flies caught with the synthetic lure was similar to that caught with torula yeast, i.e., generally female biased, but variable among seasons and locations. The synthetic lure attracted fewer non-target insects giving a substantial time savings in trap maintenance. Moreover, the synthetic lure was effective for ten weeks without replacement. Propylene glycol antifreeze increased captures significantly and improved preservation of specimens when used as the trap liquid compared to water. Dry jar traps and cardboard sticky traps were ineffective in comparison with the liquid baited traps. /// Combinaciones de varias trampas con diferentes cebos fueron evaluadas contra poblaciones de Anastrepha suspensa (Loew) y Anastrepha ludens (Loew) para substituir para la tradicionál trampa vídrio de McPhail. Trampas de plastico con un cebo syntético de dos componientes (acetato amoniaco y putrescina), capturaron igual o mas moscas de fruta que la trampa McPhail cebada con torula en agua. La proporción sexuál de las moscas capturadas con el cebo syntético fue igual que las capturadas con torula; generalmente hubo mas hembras, pero, variable con respecto a ubicación y temporada. El cebo syntético atrayeron menos insectos de otros tipos por su mejor eficiéncia resultando en menos tiempo manejando las trampas. Además, el cebo syntético fue efectivo por diéz semanas sin recebar. El anti-congelante (glycol propilico), mezclado con el agua, aumenta las capturas y preserva mejor los especimenes capturadas. Trampas secas y laminas pegajosas no fueron efectivas en comparación con las trampas cebadas con líquido.
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We tested the hypothesis that Mexican fruit flies [Anastrepha ludens (Loew)] are attracted to odor of tryptic soy broth cultures of Staphylococcus aureus (Rosenbach) because they are hungry for protein. First, we demonstrated that attraction to the odor was attenuated by feeding on a relatively complete diet containing sugar, protein, fats, vitamins, and minerals compared to feeding on sugar only; second, we showed that feeding on a diet of casein hydrolysate and sugar in which the percentage of protein was equal to that in the complete diet attenuated attraction to the same degree as the complete diet; and third, we showed that attraction to bacterial odor decreased as percentage of protein increased in a diet containing casein hydrolysate and sugar. Results of the three experiments support the hypothesis that flies are attracted to odor of S. aureus cultures largely to find protein. Dietary vitamins, minerals, fats, and percentage of protein as amino acids had no effect.
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Headspace above tryptic soy broth culture filtrates of Klebsiella pneumoniae contained greater amounts of ammonia, methylamine, 3-methylbutanamine, 1-pyrroline, 2,3,4,5-tetrahydropyridine, and two pyrazines than were found above tryptic soy broth. It also contained chemicals not found above tryptic soy broth, including dimethyldisulfide and several alcohols and ketones. Headspace above tryptic soy broth culture filtrates of Citrobacter freundii contained greater amounts of ammonia, 1-pyrroline, and several pyrazines than were found above tryptic soy broth. It also contained chemicals not found above tryptic soy broth including dimethyldisulfide, some of the same alcohols as above K. pneumoniae filtrates, a different ketone, and phenol. Additional chemicals were detected above filtrates that were saturated with sodium chloride or had their pH adjusted up or down. In laboratory bioassays with protein-starved, sugar-fed Mexican fruit flies, chemicals that did not contain protonizable nitrogen were not attractive. All chemicals containing protonizable nitrogen, except 2-methylpyrazine, were attractive. Synthetic mixtures of ammonia, trimethylamine, 1-pyrroline, 3-methylbutanamine, pyrazine, 2,3,4,5-tetrahydropyridine, 2,5-dimethylpyrazine, and trimethylpyrazine in concentrations similar to those in filtrates of the two bacteria were 73–87% as attractive as bacterial filtrates.
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We analyze the extremely complex problem of fruit fly management in Mexico suggesting the establishment of a long term, well planned and flexible country-wide orchard management program based among others on the following premises: a consideration of the entire fruit fly species complex instead of the common practice of singling out Anastrepha ludens as the unique source of problem; a multistrategy approach in which measures to control fruit flies are integrated with other pest and disease control efforts and all the other agronomic practices used in the orchard; a redirection of the control efforts putting most emphasis in the planting and orchard maintenance phase as opposed to the harvest and marketing phases; the development of novel approaches and the implementation of established control strategies based on ecologically sound principles and that are within the cultural and economic reach of the recipient (more than 70% of the fruit produced in the country comes from small scale, resource poor farmers); a biogeographical division of the fruit growing regions, with the application of management practices adapted to each particular situation; a thorough understanding of the socio-economic, socio-political, cultural and historical milieu of the farmer; the enhancement of alternative means of fruit commercialization through the creation of agroindustries and the enhancement of strong grower associations.
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A mixture of ammonium bicarbonate or ammonium carbonate, methylamine HCl and putrescine (AMPu) was evaluated for attractiveness to gamma-irradiated Mexican fruit flies, Anastrepha ludens (Loew), in a citrus orchard in 1-day tests. AMPu (10:10:1 mixture of ammonium bicarbonate:methylamine HCl:putrescine) was tested both in dilute aqueous solutions in the reservoir of McPhail traps and in more concentrated form in polypropylene tubes suspended in McPhail traps or fastened to yellow sticky ball traps. The most attractive concentration of AMPu used in aqueous solution captured only half as many flies as Torula yeast in McPhail traps. AMPu (6:10:1 mixture of ammonium carbonate:methylamine HCl:putrescine) formulated into agar and tested in tubes fastened to sticky ball traps captured as many male and female flies as Torula yeast in McPhail traps. /// Fue evaluada la atractividad de una mezcla de bicarbonato de amonio o carbonato de amonio, metilamina HCl y putrescina (AMPu) sobre moscas mexicanas de la fruta gamma-irradiadas, Anastrepha ludens (Loew), en un campo de cítricos en pruebas de un día de duración. La mezcla AMPu (mezcla de 10:10:1 de bicarbonato de amonio:metilamina HCl:putrescina) fue probada en soluciones acuosas diluídas en el reservorio de trampas de McPhail y en forma más concentrada en tubos de polipropileno suspendidos en trampas de McPhail o atados a trampas pegajosas de bolas amarillas. La concentración más atractiva de AMPu, usada en solución acuosa, capturó solamente la mitad de las moscas capturadas con levadura Torula en las trampas de McPhail. La mezcla AMPu (mezcla de 6:10:1, de carbonato de amonio:metilamina HCl:putrescina) fromulada en agar y probada en tubos atados a trampas pegajosas de bola capturó tantos machos y hembras como la levadura Torula en las trampas de McPhail.
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Attraction of laboratory-strain Mexican fruit flies, Anastrepha ludens (Loew), and wild-type flies to two synthetic lures was evaluated in a wind-tunnel. The lures were BioLure(R) (ammonium acetate and putrescine) and AMPu (ammonium carbonate, methylamine HCl, and putrescine). In one experiment, wild-type flies from the state of Nuevo Leon, Mexico, were evaluated against laboratory-strain flies that originated in Nuevo Leon. Yellow panels containing AMPu attracted >2.5 times more females and >3.5 times more males of both fly strains than panels containing BioLure(R). In another experiment. wild-type Hies from the state of Chiapas, Mexico, were evaluated against the Nuevo Leon laboratory strain. Results of this experiment were similar to the first except the differences in attractiveness between AMPu and BioLure(R) to flies of both strains were less pronounced The difference in relative attractiveness of AMPu and BioLure(R) in the two experiments was related to the time of year when the experiments were conducted rather than to inherent differences between the fly strains. In both experiments, BioLure(R) was about two times more attractive to females than to males whereas AMPu was only slightly more attractive to females. Both lures rvere more attractive to laboratory-strain flies than to wild-type flies from either region of Mexico.
Article
Traps for tropical pest tephritids have relied primarily on chemical cues while traps for temperate pest tephritids have relied primarily on visual cues. Here we review research on the interactions between chemical and visual cues that have been observed in the development of traps for the tropical Mediterranean fruit fly, Ceratitis capitata (Wiedemann), and the temperate apple maggot, Rhagoletis pomonella (Walsh). By exploiting these interactions, it may be possible to produce efficacious trapping systems that could be used in a behavioral approach to fruit fly population control. /// Trampas para plagas de tefrítidos tropicales han dependido principalmente de señales químicas mientras que trampas para plagas de tefrítidos templados han dependido principalmente de señales visuales. Se revisan investigaciones sobre las interacciones entre señales químicas y visuales que se han observado en el desarrollo de trampas para la mosca del Mediterráneo, Ceratitis capitata (Wiedemann), de lugares tropicales y para la mosca de la manzana, Rhagoletis pomonella (Walsh), de lugares templados. Aprovechando estas interacciones desde un enfoque de comportamiento, es posible crear sistemas de trampeo eficaces para controlar poblaciones de moscas de la fruta.
Article
Lures containing CEHO, a synthetic attractant emitting four components of host-fruit volatiles, were evaluated for attractiveness to Anastrepha ludens in a citrus orchard. CEHO lures were at least 12 times more attractive than water, but only about 29-56% as attractive as Torula yeast in three experiments. CEHO attracted male and female flies equally. Lure age (up to one month) did not affect attractiveness.