Response of the Fruit Fly Parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to Mango Fruit Volatiles

 
CHEMICAL ECOLOGY

      Response of the Fruit Fly Parasitoid Diachasmimorpha longicaudata
            (Hymenoptera: Braconidae) to Mango Fruit Volatiles
      MORFA CARRASCO,1 PABLO MONTOYA,2 LEOPOLDO CRUZ-LOPEZ,3                                     AND   JULIO C. ROJAS3

                                              Environ. Entomol. 34(3): 576Ð583 (2005)
       ABSTRACT The response of Diachasmimorpha longicaudata (Ashmead) females to mango fruit that
       were intact (healthy), mechanically damaged, or infested with Anastrepha ludens (Loew) larvae, and
       their respective hexanic and methanolic extracts, was studied using behavioral, electrophysiological,
       and chemical techniques. Female parasitoids signiÞcantly preferred to visit infested mangoes and their
       extracts over healthy and mechanically damaged mangoes in wind tunnel and Þeld cage bioassays. This
       suggests that the presence of the larvae inside the fruit is of clear importance in the host location
       behavior performed by this species. Methanolic extracts of infested mangoes evoked a signiÞcant
       electroantennography (EAG) response in female antennae compared with the responses elicited by
       solvent, healthy, and mechanically damaged mango extracts, but EAG response to hexanic extracts of
       infested mangoes was only signiÞcant compared with solvent control. Most of the compounds found
       in infested mango hexanic extracts were commonly found in healthy and mechanically damaged
       mango hexanic extracts, except 2-phenylethyl acetate, which seems to be exclusively present in
       infested mangoes. Also, infested mango extracts contain several compounds in higher amounts
       compared with the other two types of mangoes, as do the methanolic extracts from infested mangos.
       These differences could explain why female parasitoids preferred to visit infested mangos, with their
       correspondent methanolic and hexanic extracts. Our results suggest that this species uses a complex
       mixture of compounds for host location.

       KEY WORDS mango, Anastrepha ludens, Diachasmimorpha longicaudata, host location behavior

Diachasmimorpha longicaudata (Ashmead) is a soli-                      during location of their herbivore hosts, little infor-
tary fruit ßy endoparasitoid native to the Indo-Aus-                   mation exists on volatiles responsible for attraction,
tralian region, which has shown a high capacity of                     except from Greany et al. (1977), who reported that
adaptation to different environments where it has                      females prefer acetaldehyde over two other attractive
been introduced and currently is used for biological                   fermentation products: ethanol and acetic acid. How-
control of fruit ßies in several countries (Camacho                    ever, the evidence that D. longicaudata ßew upwind
1994, Sivinski et al. 1996, Montoya et al. 2000). In a                 and landed on healthy fruit (Cheng et al. 1992, Eben
multi-trophic context, success of parasitoids as biolog-               et al. 2000, this study) also suggests that other com-
ical control agents depends mostly on their host lo-                   pounds, in addition to fermentation products previ-
cation behavior, where chemical cues from herbivores                   ously reported (Greany et al. 1977), may be involved
and/or their hosts seems to be an essential component                  in host location behavior of this species.
(Vet and Dicke 1992).                                                     In this study, we evaluated the response of D. lon-
   Host location behavior of this parasitoid has been                  gicaudata females to healthy, mechanically damaged
widely studied. Several studies have shown that ripe,                  mango fruit and mango fruit infested with larvae of the
infested, and/or decomposing fruit are attractive to                   Mexican fruit ßy, Anastrepha ludens (Loew), and their
females of D. longicaudata, and thus chemical com-                     methanolic and hexanic extracts in Þeld cage and wind
pounds seem to be the most important cues used by                      tunnel bioassays; we also chemically identiÞed the
females during the host location process (Greany et al.                compounds present in active extracts and performed
1977, Cheng et al. 1992, Messing and Jang 1992, Eben                   a behavioral evaluation of some of the identiÞed com-
et al. 2000, Jang et al. 2000). Despite ample behavioral               pounds.
evidence that this parasitoid exploits chemical cues
                                                                                      Materials and Methods
  1 Instituto Tecnológico de Tapachula, Carretera a Puerto Madero
km 1, Tapachula, 30700 Chiapas, Mexico.                                   Biological Material. Female parasitoids were ob-
  2 Corresponding author: Programa Mosca del Mediterráneo,
                                                                       tained from the Moscafrut mass-rearing facilities
DGSV-SAGARPA, Central Poniente 14, Col. Centro, Tapachula,
30700 Chiapas, Mexico (e-mail: pmontoya@prodigy.net.mx).
                                                                       (Metapa de Dominguez, Chiapas), following rearing
  3 Departamento de Entomologṍa Tropical, El Colegio de la Frontera   methods described by Cancino (1997). The parasi-
Sur, Apartado Postal 36, Tapachula, 30700 Chiapas, Mexico.             toids used were naive when tested, having no previous

0046-225X/05/0576Ð0583$04.00/0 䉷 2005 Entomological Society of America
June 2005                CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES                     577

exposure to host larvae or fruit. Fruit were selected        placed 25 cm apart in the corner of the upwind end of
from mango trees (Mangifera indica L., ÔcriolloÕ) lo-        the ßight tunnel. To minimize the inßuence of visual
cated in Frontera Hidalgo, Chiapas, Mexico, in lots of       cues on wasp responses, fruit was placed into plastic
60 mangoes. After selection, the fruit were kept in          containers (9 cm high by 9 cm diameter) that were
paper bags to avoid infestation. When the fruit became       covered with aluminum wrap with a 1.5-cm opening.
ripe, they were cut and separated into three groups.         Air previously cleaned with activated charcoal was
One group was exposed to females of Anastrepha lu-           blown through the containers into the tunnel with a
dens (Loew) for infestation at a rate of 10 ßies per fruit   pump at a rate of 1 liter/min to provide a continuous
for 1 h and then held for 12 d inside an incubator (26 ⫾     ßow of mango odor through the tunnel. Positions
1⬚C and 65 ⫾ 5% RH) to allow the fruit ßy larvae to          within the tunnel were alternated for each Þve insects
develop to the third instar, which was conÞrmed by           to avoid positional bias. Each observation was begun
dissection. A second group of ripe mangoes was me-           by placing the release cylinder on a 15-cm-high plat-
chanically damaged by dropping them on the ßoor              form at the downwind end of the tunnel, and one
from 2 m high, and they were placed in maturation            insect was released and observed for 5 min. The insects
boxes for 12 d. A third group of mangoes was held            were recorded for taking off, random ßight, hovering
without damage or infestation.                               near the fruit, extract, or compound, and landing on a
   Fruit Extracts. Healthy, infested, and mechanically       source as previously deÞned by Jang et al. (2000).
damaged mangoes were weighed and placed by                      Electroantennography. Antennal receptivity of fe-
groups of three in individual 4-liter glass containers.      male D. longicaudata to extracts was determined by
Fruit were covered with 450 ml of methanol and hex-          electroantennography (EAG). An antenna was ex-
ane and left at 25⬚C for 24 h. Extracts were concen-         cised at its base, and the distal part of the terminal
trated to the equivalent of 1 g of fruit per milliliter of   segment was cut off. The antenna was mounted be-
solvent. The extracts were stored at 5⬚C for later use.      tween two glass capillary electrodes. The capillaries
   Field Cage Bioassays. The response of female para-        were Þlled with saline solution into which Ag-AgCl
sitoids to mango fruit was evaluated using a wooden          wires were inserted (Malo et al. 2002). The signals
frame cage (70 by 70 by 70 cm) wrapped with a plastic        generated by the antenna were passed through a high-
net. Bioassays were carried out from 0830 to 1030            impedance ampliÞer Syntech UN-06 (Syntech NL
hours at 29 ⫾ 2⬚C and 70 ⫾ 5% RH and with a light            1200; Hilversum, the Netherlands) and displayed on a
intensity of 1,062 lux. Healthy, mechanically damaged,       monitor using Syntech software for processing EAG.
and infested mangoes were hung 20 cm from the top            The stimulus (1-s duration) was delivered into a pu-
and bottom of the cage, and they were placed 15 cm           riÞed airstream (1 liter/min) ßowing continuously
apart. Individual parasitoids were released from small       over the preparation. Samples of the standard solu-
plastic containers in the bottom of the cage. All ßights,    tions test extracts or compounds were applied to Þlter
hovering, and landings were recorded for 5 min. One          paper strips, and the solvent was allowed to evaporate
hundred parasitoids were release individually, and the       (20 s). The paper strip was placed in the cartridge or
positions of fruit were rotated after each trial. Extracts   clean pipette and left for 40 s before applying. The
were evaluated in the same way as fruit. Extracts were       vapor from the cartridge was injected into the air-
loaded on Þlter paper positioned 20 cm from the top          stream passing over the antennal preparation by
and bottom of the cage and 15 cm apart from each             means of a second airstream. A cartridge with a clean
other. Individual parasitoids were released in the bot-      Þlter paper ⫹ hexane was used as a control. Stimula-
tom of the cage.                                             tion with the control preceded and followed every two
   Wind Tunnel Bioassays. The responses of parasitoid        test stimulations.
females to healthy, mechanically damaged, and in-               Chemical Analysis. Gas chromatographyÐmass
fested fruit, their hexanic and methanolic extracts, and     spectrometry was made with a Varian Star 3400 CX gas
some selected volatile compounds were evaluated in           chromatograph linked to a Varian Saturn 4D mass
nonchoice (extracts and synthetic compounds) and             spectrometer (Varian, Walnut Creek, CA). The hex-
two-choice (fruit) tests. Observations were carried          anic samples were analyzed using a nonpolar DB-5MS
out in a ßight wind tunnel that was 120 cm long and          capillary column (30 m by 0.25 mm inner diameter;
30 cm high and wide. A fan was used to pull air through      J&W ScientiÞc, Folsom, CA), whereas the methanolic
the tunnel at a velocity of 0.2 m/s. Activated charcoal      extracts were analyzed using a polar DB-WAX capil-
was used to Þlter intake air. Illumination was provided      lary column (60 m by 0.32 mm inner diameter; J&W
by two ßuorescent bulbs mounted 60 cm above the              ScientiÞc), both programmed from 50 to 250⬚C at
wind tunnel, giving a light intensity of 230 lux. Wasps      15⬚C/min. The carrier gas was helium. The injector
were individually placed in a 5-cm-high plastic pot (4       port temperature was held at 200⬚C. Mass spectral
cm inner diameter; release cylinder), and they were          identiÞcations were conÞrmed wherever possible by
allowed to acclimate to the wind tunnel room condi-          comparison of retention times and mass spectrum of
tions (25 ⫾ 1⬚C, 60 ⫾ 5% RH) for at least 1 h before         synthetic standards. Where pure standards were not
being observed. In the nonchoice tests, a cotton wick        available (Sigma-Aldrich, Toluca, Mexico), identiÞca-
loaded with a gram equivalent of the tested extract or       tion was based on comparison with spectral data from
1 ␮l of the selected compound was placed in the center       the computer library (NIST 2002). The relative per-
of the wind tunnel, 10 cm from the upwind end. For           centage of the components was calculated from the
two-choice experiments, fruit to be compared were            sum of areas of all recorded peaks.
578                                    ENVIRONMENTAL ENTOMOLOGY                                             Vol. 34, no. 3

   Fig. 1. Mean ⫾ SE response of hovering (a) and landing (b) of D. longicaudata females on hexanic and methanolic extracts
of healthy (HM), mechanically damaged (MDM), and infested mango (IM) fruit evaluated in a wind tunnel. Bars in each
graph followed by the same letter indicate no signiÞcant differences in response at the 5% level according to Tukey test.

   Statistical Analysis. Behavioral (cage bioassays and           Response of D. longicaudata to Fruit Odor and
nonchoice tests in the wind tunnel) and EAG data               Extracts in the Wind Tunnel. Diachasmimorpha lon-
were analyzed with a one-way analysis of variance              gicaudata females landed signiÞcantly more often on
(ANOVA). In some cases, before ANOVA, data were                the odor of infested mangoes over odor of healthy
公x transformed to stabilize the variance, and means            mangoes (␹2 ⫽ 7.84; df ⫽ 1; P ⬍ 0.001) and on the odor
were separated by the Tukey test. A ␹2 test was used           of mechanically damaged mango over odor of healthy
to analyze behavioral data in two-choice tests. A sig-         fruit (␹2 ⫽ 18.08; df ⫽ 1; P ⬍ 0.001) in two-choice tests.
niÞcance level of 0.05 was used for all statistical tests.     In contrast, females landed equally on odors of in-
Data were analyzed using Jandel Sigma Stat (version            fested and mechanically damaged mangoes (␹2 ⫽ 1.68;
2.0, Chicago, IL) and Statistico (Kernel release 5.5 A;        df ⫽ 1; P ⬎ 0.05).
Stat Soft, Tulsa, OK).                                            The responses of females to methanolic and hexanic
                                                               extracts of uninfested, infested, and mechanically
                                                               damaged mangoes are shown in Fig. 1. Females did not
                         Results
                                                               show any apparent response when hexane and meth-
   Response of D. longicaudata to Fruit and Extracts in        anol was offered in the wind tunnel. Females ßew
Cages. D. longicaudata females signiÞcantly preferred          upwind more frequently to hexanic extracts of in-
to visit infested mangoes over healthy and mechani-            fested mango compared with healthy mango extracts
cally damaged mangoes (F ⫽ 36.50; df ⫽ 2,18; P ⬍               (F ⫽ 5.08; df ⫽ 2,12; P ⫽ 0.025). There were no
0.001). Females did not show any preference for                signiÞcant differences among females that ßew up-
healthy and mechanically damaged fruit. Female para-           wind to hexanic extracts of infested mango and me-
sitoids signiÞcantly preferred to visit methanolic ex-         chanically damaged fruit. However, signiÞcantly more
tracts of infested mangoes over methanolic extracts of         females landed on infested mango extracts than on
healthy and mechanically damaged mangoes (F ⫽                  extracts of healthy and mechanically damaged fruit
26.76; df ⫽ 2,18; P ⬍ 0.001). No female preference for         (F ⫽ 5.18; df ⫽ 2,12; P ⫽ 0.024). With respect to the
methanolic extracts of healthy over mechanically               methanolic extracts, signiÞcantly more females ßew
damaged mangoes was observed. Hexanic extracts of              upwind (F ⫽ 6.24; df ⫽ 2,12: P ⫽ 0.014) and landed
the three types of fruit did not elicit any apparent           (F ⫽ 5.56; df ⫽ 2,12; P ⫽ 0.020) on infested mangoes
response in the females.                                       than on healthy and mechanically damaged fruit.
June 2005               CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES                        579

   Fig. 2. Mean ⫾ SE EAG response (mV) of female D. longicaudata to hexanic (a) and methanolic (b) extracts of healthy
(HM), mechanically damaged (MDM), and infested mango (IM) fruit. Hex, hexane; met, methanol. Bars in each graph
followed by the same letter indicate no signiÞcant differences in response at the 5% level according to Tukey test.

   EAG Female Response to Fruit Extracts. Hexanic           be exclusively present in infested mangoes. Also, there
extract of infested mangoes elicited a signiÞcant EAG       were quantitative differences of the components
response in female antennae compared with solvent           among treatments. Infested mango extracts contain
controls (F ⫽ 3.93; df ⫽ 3,72; P ⫽ 0.012). However,         several compounds in higher amounts compared with
there were no signiÞcant differences between the            the other two types of mangoes. The methanolic ex-
EAG response elicited by this extract and the re-           tract chromatogram (Fig. 3b) shows a different chem-
sponses elicited by healthy and mechanically damaged        ical composition compared with that of the hexanic
mango extracts (Fig. 2a). Methanolic extract of in-         extract. The compounds present in the methanolic
fested mangoes elicited a signiÞcant EAG response in        extracts have not been identiÞed yet, but most of them
female antennae in comparison with the responses            seem to be carboxylic acid derivatives. Similar to the
elicited by solvent, healthy, and mechanically dam-         infested mango hexanic extracts, some compounds
aged mango extracts (F ⫽ 8.52; df ⫽ 3,48; P ⫽ 0.001).       seem to be in higher amounts in the methanolic ex-
The EAG response elicited by mechanically damaged           tracts of infested mangoes than in healthy and me-
mango extracts was signiÞcantly different to that of the    chanically damaged fruit extracts.
solvent, but it was similar to that elicited by healthy        Response of D. longicaudata Females to Selected
mango extract (Fig. 2b).                                    Mango Volatiles. The responses of female parasitoids
   Chemical Analysis. Representative chromatograms          to selected synthetic compounds are shown in Fig. 4.
of the infested mango hexanic and methanolic extracts       Females ßew upwind to cotton wick loaded with
are shown in Fig. 3. The compounds identiÞed in             3-carene, caryophyllene, cis-ocimene, ␣-humulene,
hexanic extracts are listed in Table 1 with respective      ␣-pinene, limonene oxide, ethyl octanoate, and a 10-
relative amounts. They correspond to a mixture              component blend. There were no differences among
mainly of terpene and ester compounds; the major            these compounds, including the 10-component blend
component was 3-carene (Fig. 3a). Most of the com-          (F ⫽ 1.58; df ⫽ 7,23; P ⫽ 0.21). Landing was elicited
pounds found in infested mangoes were commonly              by 3-carene, cis-ocimene, caryophyllene, ␣-pinene,
found in healthy and mechanically damaged mango             and ethyl octanoate, but no signiÞcant differences
extracts, except 2-phenylethyl acetate, which seems to      were found among them (F ⫽ 0.30; df ⫽ 4,14; P ⫽ 0.87).
580                                        ENVIRONMENTAL ENTOMOLOGY                                          Vol. 34, no. 3

  Fig. 3. Representative chromatograms of hexanic (a) and methanolic (b) extracts from infested mangoes. Number on
each peak refers to compounds listed in Table 1.

However, the responses, particularly landing, were                 seems to be of clear importance in orienting the
low and did not elicit the level of olfactory response             searching behavior of this parasitoid, at least at short
that fruit and extracts evoke.                                     distances. In this sense, several authors (Knipling 1992,
                                                                   Vet and Dicke 1992, Godfray 1994, van Alphen and
                                                                   Jervis 1996) stated that any product from the herbi-
                        Discussion
                                                                   vore (e.g., feces, cuticle, pheromones, accessory
   Results obtained from Þeld cages and wind tunnel                glands) could be a signal for their enemies, and that
bioassays showed that D. longicaudata females are                  parasitoids should respond to the stimulus most
attracted to mango fruit, independently of whether                 closely associated with the host (Lewis et al. 1990).
fruit are healthy, mechanically damaged, or infested.              Godfray (1994) pointed out that parasitoids fre-
However, wasps signiÞcantly preferred infested fruit               quently orient toward cues that are derived from the
and their methanolic and hexanic extracts. This sug-               activity of the host, although not actually from the host
gests that the presence of the larva inside the fruit              itself.

  Table 1. Percentage composition of the compounds found in healthy (HM), mechanically damaged (MDM), and infested mango (IM)
hexanic extracts

                                                                               Mean proportion (range)
Peak                    Compound
                                                        HM (n ⫽ 7)                  MDM (n ⫽ 5)                 IM (n ⫽ 9)
  1a               ␣-Pinene                             6.2 (0.0Ð19.5)              9.9 (0.6Ð18.2)             2.8 (0.7Ð5.4)
  2a               Myrcene                                     T                           T                   0.1 (0.0Ð0.3)
  3a               ␤ Pinene                             0.13 (0.0Ð0.9)              0.2 (0.0Ð0.7)              1.4 (0.0Ð4.9)
  4a               Ethyl hexanoate                             T                           T                   0.2 (0.0Ð1.3)
  5a               3-Carene                            36.7 (3.6Ð64.3)             37.9 (15.4Ð59.2)           51.0 (28.4Ð82.2)
  6a               Limonene                             0.2 (0.0Ð0.81)              0.2 (0.0Ð0.81)             1.4 (0.0Ð3.6)
  7a               cis-Ocimene                          0.1 (0.0Ð0.62)              0.3 (0.0Ð0.78)             0.7 (0.0Ð1.8)
  8                Isopentyl isobutyrate                       T                         ND                    0.6 (0.0Ð2.8)
  9a               Terpinolene                               ⬍0.1                   0.7 (0.0Ð3.8)              2.0 (0.0Ð5.9)
 10a               Limonene oxide                      11.4 (0.0Ð48.3)             24.2 (0.0Ð54.9)             2.1 (0.0Ð9.0)
 11a               Ethyl octanoate                      5.8 (0.0Ð20.6)              1.9 (0Ð4.4)                6.6 (0.0Ð34.2)
 12                2-Phenylethyl acetate                     ND                          ND                    0.5 (0.0Ð3.4)
 13                Phenylethyl acetate                       ⬍0.1                        ND                    5.5 (0.0Ð23.6)
 14                ␤-Gurjunene                               ND                            T                   0.3 (0.0Ð1.5)
 15a               ␤-Caryophyllene                      1.0 (0.0Ð2.1)               0.3 (0.0Ð1.3)              0.8 (0.0Ð1.7)
 16a               ␣-Humelene                           5.5 (0.0Ð18.6)              1.5 (0.0Ð2.6)              2.9 (0.0Ð4.9)
 17                ␣-Gurjunene                               ND                    0.14 (0.0Ð0.45)             2.2 (0.0Ð11.8)
 18                ␤ ÐCubebene                          1.5 (0.0Ð3.2)               0.3 (0.0Ð1.3)              1.4 (0.0Ð2.4)
 19                ␥-Gurjunene                          7.1 (0.0Ð21.0)              3.9 (0.0Ð7.1)              1.4 (0.0Ð2.5)

  a
   Compounds conÞrmed with standard retention times.
  ND, not detected; T, traces.
June 2005                 CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES                            581

  Fig. 4. Mean ⫾ SE response of D. longicaudata females to synthetic compounds found in mango extracts tested in a wind
tunnel. Bars within each activity followed by the same letter indicate no signiÞcant differences in response at the 5% level
according to Tukey test.

   Similar results to those found in this study were           fested fruit. The presence of acetaldehyde, ethanol,
reported by Cheng et al. (1992) and Eben et al. (2000).        and acetic acid in the extracts cannot be ruled out
For example, Eben et al. (2000) found that D. longi-           because they may have been hidden by the solvent
caudata females visited more guava, grapefruit, and            peak in the chemical analysis. The above quantitative
mango fruit infested with A. ludens larvae than healthy        differences may explain why infested mangoes and
ones. In contrast, Greany et al. (1977) reported that D.       their respective extracts elicited more landing re-
longicaudata females were equally attracted to me-             sponses than fruit and extracts from healthy and me-
chanically damaged peaches and peaches infested                chanically damage mangoes.
with A. suspensa (Loew) larvae, and healthy peaches               The fact that females were also attracted to healthy
were not attractive at all.                                    fruit (e.g., Eben et al. 2000) suggests that some vola-
   Our chemical analysis showed that there are some            tiles are common in both types of fruit. Some of the
qualitative and quantitative differences among fruit           compounds identiÞed from mango volatiles are also
extracts. 2-Phenylethyl acetate seems to be exclusively        commonly found in many fruit, such as citrus
present in hexanic extracts of infested mangoes, and           (Takeoka et al. 1988, Kekelidze et al. 1989), guava
some other compounds (i.e., 3-carene, limonene, ter-           (Ekundayo and Ajani 1991), coffee (Mathieu et al.
pinolene, ␣-gurjenene) show a higher concentration             1998), and apricots (Takeoka et al. 1990, Chassagne
in infested mangoes. Although 2-phenylethyl acetate            and Crouzet 1995). Thus, a generalist parasitoid like D.
has been reported to be several fresh fruit and ßowers         longicaudata could use these compounds, in combi-
(Honda et al. 1998, Jordan et al. 2003, Pino et al. 2003),     nation with fermentation compounds, as cues for host
it also can be produced by microorganisms such as              habitat location. For host location, females can use
yeast, which may have the ability to ferment carbo-            short-range volatile compounds derived from the me-
hydrates to produce the volatiles (Nout and Bartelt            dium and/or excretion of the feeding larvae (Law-
1998). The chemical analysis also revealed that com-           rence 1981, Duan and Messing 2000) and sound or
pounds occurring in the methanolic extracts are dif-           vibration produced by host larvae feeding or crawling
ferent to those present in the hexanic extracts and that       inside the fruit.
there are quantitative differences among methanolic               We found that D. longicaudata females exhibit a
extracts of healthy, mechanically damaged, and in-             lower response to mango extracts than to mango fruit
582                                         ENVIRONMENTAL ENTOMOLOGY                                                  Vol. 34, no. 3

odor. A possible explanation for this low female re-                  Ekundayo, O., and F. Ajani. 1991. Volatile constituents of
sponse to extracts is that all compounds needed for                       Psidium guajava L. (guava) fruits. Flav. Fragr. J. 6: 233Ð
female attraction have not been extracted with the                        236.
method used or that some compounds were missing                       Godfray, H.C.J. 1994. Parasitoids. Behavioral and evolution-
during the extraction process. Also, the fact that the                    ary ecology. Princeton University Press, Princeton, NJ.
                                                                      Greany, P. D., J. H. Tumlinson, D. L. Chambers, and G. M.
behavioral activity of compounds evaluated (e.g.,
                                                                          Boush. 1977. Chemical mediated host Þnding by Bios-
some terpenes such as ␣-pinene, ethyl octanoate, or its                   teres (Opius) longicaudatus, a parasitoid of tephritid fruit
blend) was not comparable with that elicited by ex-                       ßy larvae. J. Chem. Ecol. 3: 189 Ð195.
tracts or fruit that may be caused by some other com-                 Honda, K., H. Omura, and N. Hayashi. 1998. IdentiÞcation
pounds identiÞed in the extracts but not evaluated                        of ßoral volatiles from Ligustrum japonicum that stimulate
may be important in eliciting attraction by themselves                    ßower-visiting by cabbage butterßy, Pieris rapae. J. Chem.
or functioning as synergist of a blend. The behavioral                    Ecol. 24: 2167Ð2180.
evaluation of all compounds and their possible mix-                   Jang, E. B., R. H. Messing, and L. A. Carvalho. 2000. Flight
tures is a time-demanding task, but the fact that ex-                     tunnel responses of Diachasmimorpha longicaudata (Ash-
tracts elicited antennal responses opens the possibility                  mead) (Hymenoptera: Braconidae) to olfactory and vi-
                                                                          sual stimuli. J. Insect Behav. 13: 525Ð538.
of analyzing fruit volatiles with coupled electrophysi-
                                                                      Jordan, M., C. Margaria, P. Phillip, and K. Goodner. 2003.
ologyÐ gas chromatography and facilitating the iden-                      Volatile components and aroma active compounds in
tiÞcation of behavioral active compounds.                                 aqueous essence and fresh pink guava fruit puree
   In conclusion, results of this study extend our un-                    (Paidium guajava L.) by Gc/ms and multidimensional
derstanding of the host location behavior of D. longi-                    Gc-Gc/o. J. Agric. Food Chem. 51: 1421Ð1426.
caudata. First, these results showed that females prefer              Kekelidze, N. A., E. P. Lomidze, and M. I. Janikashvili. 1989.
infested fruit and their extracts over healthy and me-                    Analysis of terpene variation in leaves and fruits of Citrus
chanically damaged mango fruit, which conÞrms pre-                        unshiu Marc. during ontogenesis. Flav. Fragr. J. 4: 37Ð 42.
vious studies with this species. Second, this study in-               Knipling, E. F. 1992. Principles of insect. Parasitism anal-
dicates that other compounds (e.g., terpenes), in                         ysed from new perspectives. Agriculture handbook 693,
                                                                          ARS-USDA, Washington, D.C.
addition to the previously reported compounds by
                                                                      Lawrence, P. O. 1981. Host vibration a cue to host location
Greany et al. (1977), may also mediate female orien-                      by parasite, Biosteres longicaudatus. Oecologia (Berl.). 48:
tation toward infested fruit. The latter suggests that                    249 Ð251.
this species uses a complex mixture of compounds for                  Lewis, W. J., L.E.M. Vet, J. H. Tumlinson, J. C. Van Lenteren,
host location.                                                            and R. P. Papaj. 1990. Variations in parasitoid foraging
                                                                          behavior: essential elements of a sound biological control
                                                                          theory. Environ. Entomol. 19: 41Ð 48.
                     Acknowledgments                                  Malo, E. A., N. Medina-Hernandez, A. Virgen, L. Cruz-
                                                                          López, and J. C. Rojas. 2002. Electroantennogram and
   We thank E. Malo for advice in EAG analysis, J. Valle-Mora             Þeld responses of Spodoptera frugiperda males (Lepidop-
for advice in statistical analysis, and A. del Mazo and A.                tera: Noctuidae) to plant volatiles and sex pheromone.
Santiesteban for technical assistance.                                    Folia Entomol. Mex. 41: 329 Ð338.
                                                                      Mathieu, F., C. Malosse, and B. Frérot. 1998. IdentiÞcation
                                                                          of the volatile components released by fresh coffee ber-
                      References Cited                                    ries at different stages of ripeness. J. Agric. Food Chem.
Camacho, H. 1994. The integrated use of sterile ßies and                  46: 1106 Ð1110.
   parasitoids in fruit ßy control in Costa Rica. Fourth In-          Messing, R., and E. Jang. 1992. Response of the fruit para-
   ternacional Symposium on fruit ßies of economic impor-                 sitoid Diachasmimorpha longicaudata (Hymenoptera:
   tance, Sand Key, Fla. 5Ð10 June 1994.                                  Braconidae) to host-fruit stimuli. Biol. Control. 21: 1189 Ð
Cancino, J. 1997. Procedimientos y fundamentos de la crṍa                1195.
   masiva de Diachasmimorpha longicaudata, parasitoide                Montoya, P., P. Liedo, B. Benrey, J. Cancino, J. F. Barrera, J.
   de moscas de la fruta, pp. 415Ð 428. In Memorias del                   Sivinski, and M. Aluja. 2000. Biological control of Anas-
   curso regional sobre moscas de la fruta y su control en                trepha spp. (Diptera: Tephritidae) in mango orchards
   areas grandes con enfasis en la técnica del insecto estéril.         through augmentative releases of Diachasmimorpha lon-
   In E. Hernandes, S. Flores, and C. Garcia (eds.),                      gicaudata (Ashmead) (Hymenoptera: Braconidae). Biol.
   SAGAR-OEIA, Metapa de Domṍnguez, Chis, Mexico.                        Control. 18: 216 Ð224.
Chassagne, D., and J. Crouzet. 1995. Volatile components of           NIST (National Institute of Standard Technology). 2002.
   temperate and tropical fruits. ACS Symp. Ser. 525: 23Ð24.              Mass Spectral Library on CD rom, Version 2.0a. Gaith-
Cheng, C. C., A. L. Yao, L.W.Y. Lee, and J. C. Chang. 1992.               ersburg, MD.
   Olfactory responses of Diachasmimorpha longicaudata                Nout, M.J.R., and R. J. Bartelt. 1998. Attraction of a ßying
   and Opius incisi to animal plant host related volatile                 nitidulid (Carpophilus humeralis) to volatiles produced
   sources. Bull. Inst. Acad. Sinica. 31: 131Ð135.                        by yeast grown on sweet corn and a corn-based medium.
Duan, J. J., and R. H. Messing. 2000. Effects of host substrate           J. Chem. Ecol. 24: 1217Ð1239.
   and vibration cues on ovipositor-probing behavior in two           Pino, J. A., R. Marbot, A. Rosado, and C. Vázquez. 2003.
   larval parasitoids of tephritid fruit ßies. J. Insect Behav. 13:       Volatile constituents of Malay rose apple [Syzygium ma-
   175Ð186.                                                               laccense (L.) Merr. & Perry]. Flav. Frag. J. 19: 32Ð35.
Eben, A., B. Benrey, J. Sivinski, and M. Aluja. 2000. Host            Sivinski, J. M., C. O. Calkins, R. Baranowski, D. Harris, J.
   species and host plant effects on preference and perfor-               Brambila, J. Diaz, R. E. Burns, T. Holler, and D. Dobson.
   mance of Diachasmimorpha longicaudata (Hymenoptera:                    1996. Suppression of Caribbean fruit ßy (Anastrepha sus-
   Braconidae). Environ. Entomol. 29: 87Ð94.                              pensa (Loew) Diptera: Tephritidae) population through
June 2005                 CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES                           583

   augmented releases of the parasitoid Diachasmimorpha            natural enemies. Practical approaches to their study and
   longicaudata (Ashmead) (Hymenoptera: Braconidae).               evaluation. Chapman & Hall, London, UK.
   Biol. Control. 6: 177Ð185.                                   Vet, L.E.M., and M. Dicke. 1992. Ecology of infochemical
Takeoka, G. R., R. A. Flath, M. Guentert, and W. G. Jennings.      used by natural enemies in a tritrophic context. Annu.
   1988. Nectarine volatiles: vacuum steam distillation ver-       Rev. Entomol. 37: 141Ð172.
   sus headspace sampling. J. Agric. Food Chem. 36: 553Ð560.
Takeoka, G. R., R. A. Flath, T. R. Mon, R. Teranishi, and M.
   Guentert. 1990. Volatile constituents of apricot (Prunus
   armeniaca). J. Agric. Food Chem. 38: 471Ð 477.
van Alphen, J.J.M., and M. A. Jervis. 1996. Foraging behav-       Received for publication 24 March 2004; accepted 31 Janu-
   ior, pp. 32Ð36. In M. A. Jervis and N. Kidd (eds.), Insect   ary 2005.
You can also read
Next slide ... Cancel