Crop Protection 28 (2009) 314–318
Contents lists available at ScienceDirect
Crop Protection
journal homepage: www.elsevier.com/locate/cropro
Competitiveness of fertilizers with proteinaceous baits applied in Mediterranean
fruit fly, Ceratitis capitata Wied. (Diptera: Tephritidae) control
Michal Mazor*
Institute of Plant Protection, A.R.O., The Volcani Center, P.O. Box 6, 50250 Bet Dagan, Israel
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 3 March 2008
Received in revised form
9 November 2008
Accepted 18 November 2008
The use of protein-based baits applied with insecticide or within several varieties of traps is still
a widespread tool in fruit flies control. Fruit flies’ proteinaceous baits, agricultural supplements and
animal waste just as any decomposing biological matter share a common feature of production and
emitting gaseous ammonia. This process is highly influenced by biotic and abiotic factors affecting the
instability of ammonia release rate. Several common fertilizers were as attractive as several common
commercial fruit fly baits to Mediterranean fruit fly females. Chicken litter served also as nutritional
source of protein decreasing females’ eagerness to baits. The potential of ammonia-emitting sources to
interfere with fruit fly baits during control is discussed. The implications of using fertilizers during
control procedure should be taken into account.
Ó 2008 Elsevier Ltd. All rights reserved.
Keywords:
Mediterranean fruit fly
Ceratitis capitata
Ammonia-emitting substances
Fertilizers
Protein-based baits
Control
1. Introduction
Fruit flies (Diptera: Tephritidae) are amongst the largest families
of Diptera and one of the most economically important. In 1994,
White and Elson-Harris listed 4000 species arranged in 500 genera,
within which 35% are soft-fruit attacking species including many
commercial fruits. The Mediterranean fruit fly (medfly) is one of the
most injurious members of this family since it is highly polyphagous and widely distributed. The most common procedure to
control the medfly as well as other fruit flies is the low volume
aerial or ground spraying of a blend containing insecticide and
a protein-based bait (Steiner, 1955; Rössler, 1989). The need for
external protein for sexual maturation leads fruit fly females to the
proteinaceous bait. The role of the bait is to reduce environmental
contamination as well as financial costs (Chambers et al., 1974). The
bait may also be applied in variety of traps.
Gaseous ammonia is one of the most conspicuous end-products
of decomposing processes and is the key component in attracting
the flies to protein-based bait (McPhail, 1939; Bateman and Morton,
1981). Ammonia has been used as a fruit fly attractant since the
early thirties of the 20th century (reviewed by Gow, 1954) but there
are conflicting reports on its effectiveness in attracting fruit flies
(reviewed by Bateman and Morton, 1981). The attraction of medfly
females to ammonia is dose-dependent, meaning low attraction
* Tel.: þ972 3 968 3439; fax: þ972 3 960 4180.
E-mail addresses: mmazor@volcani.agri.gov.il, michalmazor@int.gov.il
0261-2194/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cropro.2008.11.010
below the optimal rate of ammonia release and rejection above this
value. The range of unattractiveness is very narrow while the range
of rejection is much wider (Bateman and Morton, 1981; Mazor
et al., 1987; Mazor et al., 2002).
Observations on the behavior of fruit flies in nature revealed
that the flies are attracted by and feed on bird feces (Christenson
and Foote, 1960; Bateman, 1972; Malavasi et al., 1983; Hendrichs
and Hendrichs, 1990; Hendrichs and Prokopy, 1990; Hendrichs
et al., 1991; Prokopy et al., 1992; Hendrichs et al., 1993a,b; Jacome
et al., 1999). The competitiveness of bird droppings with proteinaceous bait spray droplets was studied by Prokopy et al. (1993a).
Bird feces are natural ammonia-emitting sources. Additional
ammonia-emitting sources present in an orchard are agricultural
supplements such as organic and synthetic fertilizers. The aim of
this study was to compare the attraction of several common
fertilizers to several common commercial fruit fly baits and to
correlate the attraction of these substances with the rate of
ammonia release. The results may improve the coordination
between the activities of fertilization and fruit fly control.
2. Materials and methods
2.1. Insects
Laboratory-reared flies from the ‘Sade’ strain were obtained as
pupae from the Citrus Marketing Board of Israel. This colony was
established about more than 30 years ago from infested citrus fruits
M. Mazor / Crop Protection 28 (2009) 314–318
collected from various orchards in Israel and was genetically
strengthened every 2–3 years by field collected males. Pupae and
emerging flies were kept in a room with windows, under natural
photoperiod conditions and a controlled atmosphere of 26 2 C
and 68 2% relative humidity.
2.2. Comparison of the attraction of different ammonia-emitting
sources in the laboratory
All the behavioral tests were conducted at the same conditions as
described above. These tests were conducted with 200 proteindeprived and mostly unmated 3- to 10-day-old females in an olfactometer developed and described by Gothilf and Galun (1982). During
the tests the flies were offered granulated sugar and water absorbed
on cotton wool. The tested commercial baits were as follows: Entomela (Vioryl, Athens, Greece), Buminal (Bayer, Leverkusen, F.D.R.),
NuLure (Miller Chemical & Fertilizer Co., USA) and Corn Steep Liquor
(CSL) (Roquette, Lestrem, France), Nasiman (Tamogan, Tel-Aviv,
Israel). Ammonium acetate (Merck, Germany) was included in this
group since it is the main component of the dry bait Biolure. The
tested manures were Guano (Lignotech, Norway), poultry litter, fresh
cattle manure, fresh separated cattle manure, separated cattle
manure, pelletized poultry manure, feather meal and grape rape
(Shacham, Givat ada, Israel). The fertilizers urea prills and solution of
ammonium nitrate (winter concentration) were supplied by Gat
fertilizers, Israel. Manures are usually applied directly to the soil while
the solution of the fertilizers urea and ammonium nitrate may also be
applied as foliar spray. The liquidly commercial baits were tested in
two concentrations, original and 10%-diluted. The original solution of
most liquidly commercial is viscous and is usually diluted upon use.
Most commercial baits are used as 10% solutions. A volume of about
1 ml of each material was pipetted into a 3-cm-long 1.5-cm i.d. glass
tube. A 10-cm metal wire was joined to the side of the glass tube
allowing to insert the bait into the trap. 6 traps, 3 with bait and 3
empty ones as control were suspended alternately from the horizontally rotating wheel of the olfactometer at a rate of 1 complete
turn/10 min for 1 h. At the end of the experiment, the entrance holes
of each trap were plugged with a piece of cotton wool and the traps
were transferred to the refrigerator for a few minutes to allow the
counting of the captured flies. Flies trapped in all 3 baited traps in one
olfactometer were considered as one replicate.
2.3. Ammonia trapping system
This system included a 100 ml round bottom flask containing 1–
3, 3-cm-long 1.5-cm i.d. glass tube(s), with the tested solution
(depending on the rate of ammonia release) connected to two
consecutive water traps, 16-ml-long 2-cm i.d. glass tubes containing 10 ml double-distilled water. Each glass tube contained
a volume of about 1 ml of the tested material. The whole system was
sunk in a water bath at a temperature of 30 C. Fresh air was pulled
into the trapping system by a vacuum pump at a rate of 100 ml/min.
The air was drawn into and through the round glass flask containing
the tested material and then through sintered glass filters to the first
and the second 10-ml water tubes. Most of the emitted ammonia
was caught in the first water tube. The trapping of ammonia lasted
1–8 h (depending on the rate of release of ammonia). The amount of
ammonium ion in the water was determined by a colorimetric
phenol chlorite method (Solorzano, 1969) and was calculated as mg
ammonia released from 1 ml experimental material per hour.
2.4. The effect of free access to poultry litter on the attraction of
females to the most attractive pure ammonia solution of 0.1 N
The attraction of two groups, one with protein-deprived
females and the other with females which had free access to
315
poultry litter since emergence, was compared toward 0.01 N pure
ammonia solution, the most attractive ammonia solution (Mazor
et al., 1987; Mazor et al., 2002) in olfactometers. Both groups were
served freely with granulated sucrose and water absorbed in
cotton wool. The poultry litter was removed during the attraction
tests to avoid interference with the ammonia solution. Each group
included 200, 3- to 7-day-old females which were tested during 5
consecutive days. Dead flies were replaced with flies of the same
group at the end and at the beginning of every experiment to
avoid feeding on them. The experiment was conducted with 10
replicates.
2.5. Statistical analyses
All the data were analyzed by analyses of variance (ANOVA) and
multiple comparisons of means by Tukey’s HSD test using the GLM
procedure available on SAS software.
3. Results
3.1. Attraction of the different sources releasing ammonia
The various sources of ammonia release, i.e., commercial
protein-based baits and the fertilizers were divided into 4 groups
according to their level attraction (Table 1). The excellent
attractants, as shown by statistical analyses (a), were pelletized
poultry manure and solution of ammonium nitrate which caught
44% and 45.9% of females/olfactometer/hour respectively. Less
attractive but still good (b, c) were crystalline ammonium acetate,
the key component of the dry bait Biolure which caught 38.57%
females/olfactometer/hour, and both guano and poultry litter
which caught 32.84 and 32.78 of females/olfactometer/hour
respectively. The 3rd group is of moderate attraction (d–f and
captures higher than 10% of females/olfactometer/hour) includes
undiluted and 10%-diluted solutions of Entomela, undiluted
solution of Buminal, fresh cattle manure, separated cattle manure
and grape rape. The 4th group of poor attractants which caught
less than 10% of females/olfactometer/hour included undiluted
solutions of the commercial baits NuLure, CSL and Nasiman, 10%diluted solutions of Buminal, NuLure, CSL and Nasiman and the
fertilizers fresh separated cattle manure, feathers meal and urea
belong to this group. Categories A and B, include only fertilizers,
apart from the exceptional ammonium acetate, category C
includes 3 fertilizers and 3 commercial baits while category D
with the inferior attractants includes only 3 fertilizers and 7
commercial baits.
An interesting point appears while comparing the attraction
between the original solutions of the commercial baits and
10%-diluted solutions. The attraction of the original solutions of
Entomela, Buminal, CSL and Nasiman is higher than that of the 10%diluted solution while in NuLure the situation is reversed, more
females were attracted to the diluted solution. The explanation
cannot be based on the rate of ammonia release since it is very low
in both concentrations. The composition of commercial bait solutions is usually unknown. There is a possibility that the original
solution of NuLure contains repulsive components that when
diluted become less repulsive.
3.2. Ammonia trapping system
The rate of ammonia release of some of the ammonia-emitting
materials was measured. The results are present in Table 1. The
highest rates of ammonia release were demonstrated by ammonium acetate, Guano and poultry litter which were of 2 orders of
magnitude higher than the others. The rate of ammonia released
from pelletized poultry manure, fresh cattle and separated cattle
316
M. Mazor / Crop Protection 28 (2009) 314–318
Table 1
The attraction of protein-deprived Ceratitis capitata females to fertilizers and fruit fly commercial baits.
Source of
attraction
Category of
attraction
Number
of replicates
Commercial baits
Entomela (undiluted)
Entomela 10%
Buminal (undiluted)
Buminal 10%
NuLure (undiluted)
NuLure 10%
CSL (undiluted)
CSL 10%
Nasiman (undiluted)
Nasiman 10%
Ammonium acetate (Crystalline)
Cb
C
C
D
D
D
D
D
D
D
B
36
20
40
40
36
36
40
36
24
32
20
Fertilizers
Guano
Poultry litter
Fresh cattle manure
Fresh separated cattle manure
Separated cattle manure
Pelletized poultry manure
Feathers meal
Grape rape
Urea
NH4NO3 solution
B
B
C
D
C
A
D
C
D
A
16 (39)
16 (34)
16 (17)
16 (6)
16 (12)
20 (12)
16
16
20
20
(10)a
(10)
(21)
(13)
(4)
(10)
(12)
Number of trapped females
(olfactometer/hour) (Average SD)
Trapped females
(out of 200) (%)
44.67 11.99 d
21.30 6.63 ef
25.35 7.33 ef
15.67 7.42 fghi
4.19 1.94k
17.47 4.64 efg
14.77 6.51 fghij
8.25 4.72 jk
16.71 5.77 efghi
6.75 2.77 k
77.15 15.69 b
22.33
10.65
12.67
7.83
2.09
8.73
7.38
4.12
8.35
3.35
38.57
65.69 7.11 c
65.56 9.65 c
36.37 12.88 d
12.62 4.26 fghijk
24.75 4.57 e
91.8 15.98 a
17.0 8.14 efgh
21.37 5.41 ef
10.55 5. 57 ghijk
88.0 15.26 a
32.84
32.78
18.18
6.31
12.37
45.9
8.5
10.68
5.27
44
Ammonia release
(mg/ml/hour)
5.07 0.75
0.54 0.17
2.82 0.86
0.28 0.16
0.15 0.20
0.26 0.15
219.01 65.44
206.99 133.51
110.43 10.51
26.72 6.46
0.65 0.18
11.37 4.57
35.70 8.53
a
Numbers within the brackets are the number of replicates of ammonia release determinations. Means in the 4th column followed by different letters are significantly
different at 0.05 level.
b
Capital letters appearing the second column describes groups of attraction; A – excellent attraction (a); B – good attraction (b, c); C – moderate attraction (d–f), higher than
10% captures; D – describes inferior attraction, less than 10% captures.
manures was of 1 order of magnitude higher. Undiluted solutions of
Entomela and Buminal released only few micrograms of ammonia
under the experimental conditions and all the other tested materials emitted less then 1 mg ammonia.
3.3. The effect of free access to poultry litter on the attraction of
females to the most attractive pure ammonia solution of 0.1 N
Almost twice as much females which had no access to poultry
litter hence may be considered as protein-deprived were trapped
by the most attractive ammonia solution than those which did had
an access to the chicken litter. This tendency was kept during the
five consecutive test days (Fig. 1).
Number of Females Trapped
(Olfactometer/Hour)
Control
Poultry Litter
100
80
60
40
20
0
3
4
5
6
7
Age (Days)
Fig. 1. The effect of exposure of protein-deprived Ceratitis capitata females to poultry
litter on their attraction by the most attractive pure ammonia solution during 5
consecutive days (n ¼ 10).
4. Discussion
Fruit flies’ proteinaceous baits, agricultural supplements such as
synthetic fertilizers and animal waste, just as any decomposing
biological matter produce and release ammonia during putrefaction. The course and speed of the decomposition process, hence the
rate of ammonia release to the atmosphere, is the outcome of
interactions between biotic (microbial activity) and abiotic
(temperature, precipitation, wind etc.) factors (Broce and Haas,
2000; Sommer and Hutchings, 2001).
Ammonia releasing substances play a role as attractants in fruit
flies control. The outcome of the highly influenced process of
ammonia production results in inconsistency and variability of the
baits. Seasonal effects on the performance of proteinaceous baits on
catches of the oriental fruit fly, Dacus dorsalis were already
mentioned by Gow (1954). Proteinaceous food baits in McPhail
traps were more attractive in trapping oriental fruit flies, D. dorsalis,
the melon fly, D. cucurbitae and the medfly, C. capitata in dry
climate than in wet climate (Cunningham et al., 1978) and on the
other hand the attraction of PIB-7/malathion bait spray droplets
wanes dramatically within 1 day under dry condition (Prokopy
et al., 1992). Droplets of GF-120 were highly attractive to melon fly
females, Bactrocera cucurbitae, within 1 h of bait spray application
but lost almost about half of their attraction within 5 h and all of it
within 24 h under dry greenhouse conditions (Prokopy et al., 2003).
Changes of proteinaceous bait pH affect ammonia release and its
attraction (Bateman and Morton, 1981; Mazor et al., 1987). Sodium
borate (borax) added to PIB-7 to inhibit bait decomposition and to
repel Muscidae flies, affected fruit fly catches. Increasing pH by
borax caused immediate release of ammonia (Lopez and Becerril,
1967). Addition of borax to NuLure increased its pH and its
attraction to Caribbean fruit fly (Epsky et al., 1993). Bait concentration may also affect its attraction (Fabres et al., 2003). Development of microflora on yeast hydrolysate bait within a trap caused
strong putrefaction odors which influenced bait attractany to
oriental fruit flies, D. dorsalis (Gow, 1954). Bateman and Morton
(1981) demonstrated that bacterial decomposition of hydrolysate
M. Mazor / Crop Protection 28 (2009) 314–318
bait that is accompanied by an increase in ammonia evolution
increased bait attraction.
Fruit flies’ literature, dealing with the efficiency of different
ammonium salts, as well as protein-based baits, had conflicting
results. This discrepancy may probably be attributed to the fact that
different rates of ammonia emitted by the tested materials unfortunately were not measured. Furthermore, since the beginning of
the last century until these days, assessments of baits were mostly
carried out under field conditions and therefore were easily influenced by the factors mentioned above. In the studies where the rate
of release of ammonia was measured, correlation between attraction and rate of release was observed. The very low attraction
characterizing the proteinaceous baits may be explained by the low
rate of ammonia release as compare to the fertilizers which were of
1–2 orders of magnitude more attractive and had higher rates of
ammonia release.
The attraction of substance of fecal origin to tephritid flies has
been studied by several researchers (Prokopy et al., 1993a,b; DeMilo
et al., 1997; Epsky et al., 1997; Thomas, 1998; Robacker et al., 2000;
Pinero et al., 2003; Aluja and Pinero, 2004). The source and
condition of animal excrement affects its attraction to C. capitata
(Prokopy et al., 1993b). Droppings from birds and lizards were more
attractive than droppings from mammals and high protein diet of
these animals will result in more attractive droppings. The manures
of avian origin, the guano, the poultry litter and the pelletized
poultry manure in our study confirmed these conclusions by being
more attractive than the several kinds of cattle manures.
The odor of ammonia plays probably a role as indicator that
informs fruit fly female on the presence of protein which is needed
for egg production but not on the nutritional value of the ammonia
source. Incomplete and different food digestion systems, within and
between animal taxa, result in animal excrements which have
different chemical composition and therefore different nutritional
values for female flies. Free access of protein-deprived females to
poultry litter resulted in lower tendency of the fed females to search
for protein and hence lower trapping in olfactometer tests. Poultry
litter contains an average of crude protein of 20–30% and the true
protein content is 16% (Tagari, 1978). The availability of proteinaceous components in the poultry litter has probably fulfilled
females’ protein hunger and reduced the number of females
responding. The nutritional value of several animal wastes was
measured by Tagari (1978) who even considered recycling and using
them as ruminant feed. Bird droppings may contribute to fecundity
of fruit fly females (Hendrichs et al., 1991; Hendrichs et al., 1993b;
Manrakhan and Lux, 2006). The lack of contribution to the fecundity
of the Mexican fruit fly females by the white-wing dove, Zenaida
asiatica, droppings (Thomas, 1998) is because doves have an
exceptional digestive system which result in droppings with very
poor nutritional value (Plavnik, I. personal communication).
Prokopy et al. (1995) stated that the physiological state of an
insect is a result of several variables that may affect the pattern of
its foraging behavior for an essential resource. Degree of hunger
and size of egg load are two components of insect physiological
state known to influence an individual’s propensity to seek or
accept resources of varying nutritional or ovipositional quality.
Galun et al. (1981) described the specific hunger to protein of the
medfly and Lachman (1983) showed that the amounts of protein
consumed by medfly females and the number of eggs lay were in
direct correlation. He also described two distinct cycled of oogenesis coincides with protein consumption.
Agricultural supplements, animal waste, just as any decomposing biological matter which release ammonia may reduce bait
efficiency in two ways. Females searching for protein may go to
ammonia-emitting substances other than the bait and may even
find materials which contain nutritional components that will
reduce their willing to locate other potential sources. The control of
317
fruit flies by using baits leans on the need to locate proteinaceous
food and to consume it either with poison or by being captured in
traps. Removal of every natural decomposing biological materials
scattered in orchard habitat is almost a mission impossible but the
timing and mode of applications, as well as the nature of the
fertilizers have to be taken into account.
Acknowledgement
I wish to thank Alexander Peysakhis for his supportive technical
assistance. I am grateful to Ruth Akiva (Board of Fruit and Vegetable
Growers, Israel) who was always ready to supply the needed flies
for the experiments. Many many thanks to Prof. Rachel Galun, my
guide and friend, for comments on previous drafts of this manuscript. I wish to dedicate this paper to the late Miri Zarhey who
helped me with the statistical analyses and recently passed away.
This research was supported by the Chief Scientists of the Ministry
of Environmental Protection and the Ministry of Agricultural and
Rural Development.
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