Upload
ecosu
View
0
Download
0
Embed Size (px)
Citation preview
PLEASE SCROLL DOWN FOR ARTICLE
This article was downloaded by: [Montoya, Pablo J.]On: 14 December 2009Access details: Access Details: [subscription number 917788259]Publisher Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Biocontrol Science and TechnologyPublication details, including instructions for authors and subscription information:http://www.informaworld.com/smpp/title~content=t713409232
Host discrimination and superparasitism in wild and mass-rearedDiachasmimorpha longicaudata (Hym.: Braconidae) femalesP. I. González a; P. Montoya b; G. Pérez-Lachaud a; J. Cancino b; P. Liedo a
a El Colegio de la Frontera Sur, Tapachula, Chiapas, Mexico b Programa Moscafrut, SAGARPA-IICA,Tapachula, Chiapas, Mexico
Online publication date: 14 December 2009
To cite this Article González, P. I., Montoya, P., Pérez-Lachaud, G., Cancino, J. and Liedo, P.(2010) 'Host discriminationand superparasitism in wild and mass-reared Diachasmimorpha longicaudata (Hym.: Braconidae) females', BiocontrolScience and Technology, 20: 2, 137 — 148To link to this Article: DOI: 10.1080/09583150903437266URL: http://dx.doi.org/10.1080/09583150903437266
Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf
This article may be used for research, teaching and private study purposes. Any substantial orsystematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply ordistribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss,actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directlyor indirectly in connection with or arising out of the use of this material.
RESEARCH ARTICLE
Host discrimination and superparasitism in wild and mass-rearedDiachasmimorpha longicaudata (Hym.: Braconidae) females
P.I. Gonzaleza, P. Montoyab*, G. Perez-Lachauda, J. Cancinob and P. Liedoa
aEl Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km 2.5, Tapachula, Chiapas30700, Mexico; bPrograma Moscafrut, SAGARPA-IICA, Av. Central Poniente 14, Col.
Centro, Tapachula Chiapas 30700, Mexico
(Received 11 May 2009; returned 22 July; accepted 23 October 2009)
We compared the oviposition behavior and host discrimination ability of wild andmass-reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae) femalesparasitizing Anastrepha ludens (Diptera: Tephritidae) larvae. Both kinds ofparasitoid females were presented simultaneously with parasitized and non-parasitized larvae in choice tests, and their superparasitism performance wasevaluated under a mass-rearing situation. At the time of the test, D. longicaudatahad 156 generations under mass-rearing conditions. Our goal was to determinethe effect of the mass-rearing process on the foraging decisions of this species.One of the primary findings was the apparent ubiquity of superparasitism byD. longicaudata females. Both types of females showed similar patterns in each ofthe phases of oviposition behavior evaluated. The only notable differences wereamong the percentages of transition between behaviors, mainly related to theintensity with which each activity was performed. Under a mass-rearing situation,both strains of females had a similar tendency to increase superparasitism (i.e.,number of oviposition scars per puparium and the proportion of superparasitizedlarvae) over time. The mass-rearing process appears to have induced the selectionof more aggressive, fertile and precocious females. Despite these observations, weconcluded that the process of adaptation to mass-rearing conditions has notsubstantially influenced the foraging and ovipositional behaviors in this species.
Keywords: Diachasmimorpha longicaudata; superparasitism; foraging decisions;mass rearing
Introduction
Superparasitism � a female laying eggs in an already parasitized host � is a
phenomenon frequently observed in the laboratory (e.g., van Alphen and Visser
1990; Montoya et al. 2003; White and Andow 2008) as well as in nature (van
Lenteren 1981; van Dijken and Waage 1987; Baker, Peulet, and Visser 1990).
Parasitoids used as biocontrol agents are expected to be highly efficient in finding
hosts and to be able to discriminate between parasitized and non-parasitized hosts
(van Lenteren, Bakker, and van Alphen 1978), avoiding superparasitism and
minimizing the time and energy associated with searching behavior (Godfray 1994;
Mackauer 1990).
*Corresponding author. Email: [email protected]
ISSN 0958-3157 print/ISSN 1360-0478 online
# 2010 Taylor & Francis
DOI: 10.1080/09583150903437266
http://www.informaworld.com
Biocontrol Science and Technology,
Vol. 20, No. 2, 2010, 137�148
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
In the past, superparasitism has been attributed to the inability of females to
discriminate between parasitized and non-parasitized hosts, and has been interpreted
as an error by the ovipositing female. However, different authors have stated that
under specific conditions, superparasitism may be an adaptive strategy (see van
Alphen and Visser 1990; Rosenheim and Hongkham 1996; White and Andow 2008),
resulting from a balance between the benefits and the costs of laying an egg in an
already parasitized host. The advantages of superparasitism are an increasedpossibility of producing offspring from a host and the stabilization of host�parasitoid interactions in solitary and gregarious parasitoids (van Alphen 1988;
van Alphen and Visser 1990).
According to Wanjberg, Pizzol, and Babault (1989), a propensity for super-
parasitism in Trichogramma maidis Pintureau and Voegele (Hymenoptera: Tricho-
grammatidae) seems to be genetically determined in mass-reared individuals. In
contrast, results by White and Andow (2008) in Macrocentrus grandii (Hymenop-
tera: Braconidae), suggest that host availability and female environmental
perception of conspecific competitors (rather than wasp propensity), determine
self-superparasitism. Other studies have also shown that parasitoids adaptively
superparasitize when perceiving a limitation of host resources (van Alphen and
Visser 1990; Weisser and Houston 1993). Superparasitism studies should be
considered in parasitoid mass-rearing protocols and augmentative field release
biocontrol programs, to ensure production efficiency, to prevent waste of parasitoid
reproductive potential and to infer the performance of the parasitoids in the field.Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) is a fruit
fly parasitoid considered worldwide as an effective biological control agent for
release purposes (Montoya et al. 2000b, 2007; Ovruski, Colin, Soria, Orono, and
Schliserman 2003). Adult females parasitize a number of second- and third-instar
fruit fly species’ larvae in a wide variety of host fruits (Sivinski, Pinero, and Aluja
2000). The species was originally discovered in the Indo-Philippine region where it
attacked Bactrocera spp. (Wharton and Marsh 1978). In addition to wide-spread
introductions, D. longicaudata has been mass-reared and released by augmentation,
either alone or in combination with sterile male flies for the control of Ceratitis
capitata (Wong et al. 1991) and various Anastrepha spp. (Sivinski et al. 1996;
Montoya et al. 2000b). This species develops as a solitary koinobiont endoparasitoid
of larvae/prepupae and emerges from the host puparium. Unlike some other
tephritid-attacking opiines, D. longicaudata forages extensively for larval hosts in
fallen fruit (Purcell, Jackson, Long, and Batchelor 1994). Female lifespan offspring
production averages 213.494.3 (Gonzalez, Montoya, Perez-Lachaud, Cancino, and
Liedo 2007).While the capacity for host discrimination in this species has been reported
(Lawrence 1988; Montoya et al. 2003), Montoya et al. (2000a) found a strong
tendency in this species toward self-superparasitism in laboratory experiments, even
in the presence of abundant non-parasitized hosts. Recently, Gonzalez et al. (2007)
determined a high incidence of superparasitism in D. longicaudata under mass-
rearing conditions, although superparasitism was correlated with an efficacious
female-biased sex-ratio, and had no negative consequences in any of the life-history
traits studied (longevity, fecundity and flight ability). These results suggest that in
this species superparasitism could be adaptive. However, the incidence of super-
parasitism by wild females in the field is not known.
138 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
In this work, we compared the oviposition behavior and host discrimination
ability of wild and mass-reared D. longicaudata females attacking Anastrepha ludens
(Loew) (Diptera: Tephritidae) larvae under laboratory conditions. Both kinds
of parasitoid females were presented simultaneously with parasitized and non-
parasitized larvae in choice tests. We video recorded the oviposition behavioral
sequences of both types of females and recorded their preference with respect to the
kind of larvae attacked. We also studied, under a mass-rearing situation, the
superparasitism that both kinds of females exhibited with regard to the host larvae
during five consecutive days. Our goal was to find the effect (if any) that the mass-
rearing process had on the ovipositional foraging behavior of this species.
Materials and methods
Work site and biological material
This work was carried out at the Biological Control Laboratory of the MOSCAFRUT
Program, SAGARPA-IICA in Metapa, Chiapas, Mexico. Puparia of D. longicaudata
and larvae of A. ludens were provided by the MOSCAFRUT mass-rearing facility,
where insects are produced according to the methods described by Cancino (1997) and
Domınguez, Hernandez, and Moreno (1997), respectively. Wild individuals were
obtained from infested mango fruits, Mangifera indica (Anacardiaceae) var. ‘Creole’
collected in the county of Mazapa de Madero, where D. longicaudata was released 10
years ago and was not released thereafter (J. Cancino, personal observation). The
mango fruits were dissected and the larvae were placed in plastic containers with
humid vermiculite to induce pupation. Before emergence, puparia were placed in
mesh-covered wood frame (30�30�30 cm) cages. Adults of both sexes were
maintained in these cages until used for experiments and provided with food
(crystallized honey) to ensure mating. Laboratory conditions were 24928C, 70�80%
RH, and photoperiod of 12 h L:12 h D until adult emergence.
Host discrimination
Host discrimination of wild and mass-reared D. longicaudata females was examined
in choice tests. Experiments basically follow the procedures described by Montoya
et al. (2003) and the criteria proposed by van Alphen and Jervis (1996). Twenty-five
laboratory females and 20 wild females (5�8-days-old and without oviposition
experience) were individually exposed to the simultaneous presence of parasitized
and non-parasitized third instar A. ludens larvae. The parasitized larvae were
obtained by exposing A. ludens larvae to D. longicaudata females 1 day before the
experiments, for 20 min. Using a stereomicroscope we verified the presence of one to
three oviposition scars in each fruit fly larva, which, according to Montoya et al.
(2003) should result in at least one parasitoid egg.
The experimental arena consisted of a 24-cell clear plastic chamber (8.5�12.5 cm,
wide�long). Each individual cell was 1.5�0.5 cm, diameter�deep, where para-
sitized and unparasitized larvae were individually placed in an alternating fashion,
then provided with an abundant semi-synthetic diet. The mesh covering the chamber
was previously impregnated with mango juice, in order to provide some host plant
stimulus to females (Greany, Tumlinson, Chambers, and Boush 1977; Carrasco,
Biocontrol Science and Technology 139
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
Montoya, Cruz-Lopez, and Rojas 2005). The behavior of each female was observed
for 30 min. Data on the first larvae chosen, the kind of larvae subsequently attacked,
the total number of ovipositions and oviposition attempts, as well as the duration of
these events, were recorded. All observations were carried out under lab conditions, at24928C temperature and 7095% RH. The behavior of 17 females (eight mass-reared
and nine wild females) was also recorded using a digital video-camera Sony† type
DCR-TRV840, in order to describe and quantify the observed behavior.
The behaviors performed by each female were transcribed sequentially in a first-
order matrix, and the transition frequencies between pairs of behaviors were calcu-
lated to determine their level of importance. Based on the transition frequencies, we
built a flow diagram for each strain of females.
Superparasitism by wild and lab females under a mass-rearing situation
Parasitoids were placed in wood frame, (30�30�30 cm) mesh-covered cages at a 2:1
host larvae:female parasitoid ratio to simulate mass-rearing conditions. Theoviposition units were lids of Petri dishes (10�1 cm, diameter�deep) into which
60 irradiated and unparasitized third instar A. ludens larvae were placed with larval
diet, and then covered with a fine mesh. Females were 5�7-days-old and without
oviposition experience at the beginning of the experiment.
Simultaneously but in independent cages, the host larvae were exposed to the
attack of females from each strain over the course of five consecutive days for 2 h per
day. Oviposition units were renewed every day. The level of superparasitism and its
evolution during the 5 days of larval exposure were determined for each type of female,by counting the number of oviposition scars per puparium per day. As shown by
Montoya et al. (2000a) the number of oviposition scars on the attacked puparia is
strongly correlated with the number of first instar parasitoid larvae found by dissection
(R2� 0.901, see their Figure 3). Seven replicates of this experiment were done.
Statistical analysis
The type of host (parasitized or non-parasitized) chosen by wild and lab reared
females for their first oviposition, and the number of self-superparasitisms were
compared using a Chi-square test. The proportions of wild and lab reared females that
selected non-parasitized larvae for the first five oviposition events in the host
discrimination experiment were compared by applying Fisher’s Exact Test (Zar 1984).Because females attacked a different number of hosts during the 30 min observation
period (see Results), we compared the number of probing events and the number and
duration of ovipositions that females of both types performed on already parasitized
hosts through covariance analyses, with the total number of attempts, the total
number of ovipositions, and the total time each female spent in oviposition as a
covariable for the corresponding analysis. Accurate data on oviposition duration were
available only for the video-recorded females. Superparasitism under the mass-rearing
situation was analyzed by a factorial analysis of variance (strain of female and day ofoviposition as factors); means were separated by the Tukey�Kramer HSD (a�0.05)
procedure. We also performed a simple lineal regression analysis between the number
of scars per puparium and the proportion of superparasitized larvae in successive
days. All statistical analyses were done using Statistica ver. 7 (Statsoft 2004).
140 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
Results
Host discrimination
While wild females, in their first oviposition attempt selected non-parasitized larvae
more frequently than mass-reared females, this difference was not significant (Table 1;
x2c1, 0.95�2.57, P�0.05). After their first oviposition, wild and lab females attacked
similar numbers of non-parasitized larvae. For example, 55% of mass-reared females
and 60% of wild females selected a non-parasitized larva for their second and third
ovipositions. Moreover, when the first five choices of each female were compared,
there was no statistical difference in the proportions of females of each strain that
selected non-parasitized larvae (Fisher test, P�0.93, 0.74, 0.63, 0.28 and 0.32 for the
first to the fifth ovipositions, respectively).
Females from the mass-rearing facility probed as many hosts as wild females,
irrespective of the type of host attacked (lab females 15.791.3, wild females 15.391.4,
mean9SEM; ANCOVA F1,25�0.04 P�0.84), although the first ones successfully
parasitized a slightly higher number of larvae during the 30 min of observation
(ANOVA, F1,43�6.34, P�0.02; lab females 890.46 vs. wild females 6.4590.38).
There were no statistical differences among the number of ovipositions that females of
the two strains made into already parasitized hosts (ANCOVA, F1, 42�0.06, P�0.81),
or in the mean duration of ovipositions (ANCOVA, F1,14�0.07, P�0.798) (Table 1).It is interesting to note that females of both strains self-superparasitized their
hosts, 28% of mass-reared females (7/25) and 30% of wild females (6/20) self
superparasitized at least one host, with no significant difference between female
types (x2c1, 0.95�0.2, P�0.05). There was no significant difference in the type of
larva (parasitized�non-parasitized) either type of female chose to self-superparsitize,
(x2c1, 0.95�0.52, P�0.05).
Host-searching behavior
Five relevant behaviors were described: walking, host searching, attempts at
oviposition, oviposition, and resting. These behaviors were previously described in
Biosteres longicaudatus (�D. longicaudata) by Lawrence (1981), who considered
only four sequential behaviors: (1) aleatory host searching (behavior that we
Table 1. First choice, number and duration (Mean9SEM) of ovipositions performed by wild
and mass reared D. longicaudata females on parasitized and non-parasitized A. ludens larvae,
during 30-min choice test.
First choice Ovipositions1
Type of female Type of larva Number Number Duration (s)2
Mass reared Parasitized 16 3.390.59 a 50.294.6 a
Non parasitized 9 3.890.37 a 48.292.7 a
Wild Parasitized 8 2.390.33 a 57.596 a
Non parasitized 12 4.090.37 a 6095.8 a
Different letters in the same column indicate significant difference (Ancova, a�0.05).1Mean number and mean duration based on n�8 mass reared females, and n�9 wild females recorded.2Duration includes exploration and oviposition on the same larva.
Biocontrol Science and Technology 141
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
considered as walking), (2) Non-aleatory searching (�host searching), (3) ovipositor
insertion, behavior that we separated into attempts of oviposition and oviposition, and
(4) cleaning of ovipositor and antennae at the end of host searching, that we defined
as the resting period.
These behaviors were defined as follows: (1) Walking. The females walked in the
experimental arena with rapid movements. Their antennae were kept parallel to the
substrate with a 458 angle between them. (2) Host searching. The females walked
slowly in the experimental arena, with the antennae touching the substrate at varying
time intervals. During their host searching, females turned in half circles over the
inspected area, making oscillating movements with their ovipositor. (3) Oviposition
attempts (probing): The female inserted her ovipositor into the substrate, but
withdrew it quickly to continue host searching. (4) Oviposition. The female raised
her abdomen and inserted her ovipositor, usually making gentle motions until she
made contact with the host larva. Then, she remained immobile and spread her
antennae to an angle of 180o, which may be coincident with the moment of egg-
laying. Finally, the female made gentle abdominal movements withdrew her
ovipositor and slipped it into its sheath. (5) Resting. Following oviposition, the
females remained motionless, cleaning their antennae and legs, before continuing the
search for more host larvae. Figure 1 shows the flow diagrams for the behavioral
sequences performed by both kinds of females. There were no noticeable differences
between the behavioral sequences of wild and mass-reared females.
Superparasitism by lab and wild females under mass-rearing situation
Both kinds of females tended to superparasitize their hosts, and that super-
parasitism was more intensive (i.e., a higher proportion of exposed larvae was
superparasitized) in direct relation to time (Figure 2; F9, 60�7.90, PB0.001). There
were significant differences between wild and mass-reared females for both
parameters (F1, 60�169.48, PB0.001 for number of scars/puparium, and F1, 60�
59
19
49
24
5026
21
50
59
959
42
4950
21
50
59
9
33
5959
42
49495050
21
31
5050
59
9
WALKING
HOST SEARCHING
OVIPOSITIONATTEMPTS
OVIPOSITION
RESTING
Lab females Wild females
40
36 13
53
23
37
20
39
61
52
44
30
18
4040
36
5353
23
3737
20
39
6161
52
44
WALKING
HOST SEARCHING
OVIPOSITIONATTEMPTS
OVIPOSITION
RESTING
42
a b
Figure 1. Oviposition ethogram of mass-reared (a) and (b) wild Diachasmimorpha long-
icaudata females attacking third-instar Anastrepha ludens larvae. The transition arrows
connect sequential behaviors. The width of the arrows is proportional to the relative transition
frequency. Numbers indicate the observed frequencies.
142 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
36.16, PB0.001 for proportion of superparasitized hosts). The interaction between
factors (female type and day number) was significant in the case of number of scars
(F4,60�4.76, PB0,0021), but not in the proportion of superparasitized larvae
(F 4,60�0,68, P�0,6071); The superparasitism inflicted by wild females was always
significantly lower. The relationship between the number of scars per puparium and
the proportion of superparasitized larvae was highly significant, but different in
both strains, R2�0.98 for wild females, R2�0.89 for lab females (Figure 3).
Discussion
One of the major findings in this study is the apparent ubiquity of superparasitism in
D. longicaudata females, whether mass reared or field collected. We observed high
Figure 2. Proportion (Mean9SD) of Anastrepha ludens superparasitized larvae (a) and
number of oviposition scars per puparium (b), caused by wild and lab Diachasmimorpha
longicaudata females under mass-rearing conditions. Different letters above bars mean
significant differences between type of female and among days. (a�0.05, PB0.0021 for scars
number; P�0.6071 for proportion of superparasitized larvae).
Biocontrol Science and Technology 143
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
levels of superparasitism inflicted by the two strains, both when females singly
exploited a patch (as in Montoya et al. 2000a, 2003) and when other females were
present. However, both strains seemed to select non-parasitized larvae more
frequently after their first oviposition experience. These results suggest that 156
generations under mass-rearing conditions have not significantly influenced the
ovipositional decisions in this species.
Wild and laboratory females also showed similar behavioral patterns in each one
of the phases of oviposition. The observed differences in the behavioral sequences
were mainly related to the intensity of each activity rather than to some variation in
the process of oviposition behavior. According to our data, it seems that the mass-
rearing process has selected for more aggressive, more fertile, and precocious females.
This is reflected in the number of hosts parasitized and the level of superparasitism
observed among mass-reared females under our experimental conditions. A similar
phenomenon has been observed in fruit flies (Liedo and Carey 1996; Miyatake 1998;
Cayol 2000; Liedo, Salgado, Oropeza, and Toledo 2007; Hernandez, Toledo,
Artiaga-Lopez, and Flores 2009), where females become more fertile and precocious
as a consequence of their adaptation to mass-rearing conditions.Ethograms suggested that the behavioral sequences in the choice of either
parasitized larvae or non-parasitized larvae did not differ in wild and lab females.
Foraging behavior was very similar in both strains. There were differences only in the
percentages of transition among behaviors. For example, ‘walking’ was the random
initial behavior prior to host searching for both strains (42% for lab females; 36% for
the wild ones). During this activity, females walked slowly around the experimental
arena, touching the substrate at intervals with their antennae (49% for lab females;
40% for wild females). This activity probably served to locate host larva, although
females also use the mechanoreceptors located in their tarsi for this process (Leyva,
Martınez, and Valdez 1988). According to Lawrence (1981), the duration of this
behavior depends on the ability of the female to orient herself to the body-position of
the host larva inside the fruit.
y = 0,0402x + 0,4784 R2 = 0,8958
y = 0,146x + 0,1339 R2 = 0,9865
0
0,1
0,2
0,3
0,4
0,5
0,6
0,7
0,8
0,9
1
0 2 4 6 8 10
Number of scars / pupa
Pro
port
ion
of s
uper
para
sitiz
ed la
rvae Wild
Laboratory
Figure 3. Relationship between number of scars per puparium and proportion of super-
parasitized larvae in Anastrepha ludens for wild (diamonds) and mass-reared (squares)
Diachasmimorpha longicaudata females.
144 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
Superparasitism by both wild and lab females under the ratio used in mass rearing
(two host larvae/wasp female), showed that both strains had a similar tendency to
increase the level of superparasitism (i.e., number of oviposition scars per puparium as
in Montoya et al. 2000a) and the proportion of superparasitized larvae over time. This
can be interpreted as a consequence of experience as well as of physiological maturity.
Lawrence, Greany, Nation, and Baranowski (1978) stated that in D. longicaudata
females, the number of mature oocytes tends to increase as experience of ovipositionincreases. The strong tendency of this species to superparasitize even when large
quantities of hosts are available (Montoya et al. 2000a), supports the notion that
superparasitism behavior in D. longicaudata could be an adaptive response. Notably,
adults emerging from host populations with moderate levels of superparasitism
showed the highest percentage of female emergence and adult flyers, without any
deleterious effect in other parameters such as fertility and longevity (Gonzalez et al.
2007). The tendency to superparasitize a host seems to be widespread even among
parasitoid species that show an innate ability for host discrimination (van Lenteren
1981; Tenna, Kapranas, Garcia-Marı, and Luck 2008).
It has been acknowledged that females of solitary parasitoids do not obtain any
benefits from self-superparasitism, except when the total fitness for two immatures in
self-superparasitized hosts is higher than the fitness for a single immature in
parasitized hosts, and when it reduces the risk of further superparasitism by other
females (Waage 1986; Godfray 1994). This improved fitness is probably attributable
to two immatures depressing the host immune system more effectively than one, orincreasing the feeding of the host (Waage 1986; Mackauer and Chau 2001). This may
be the case in D. longicaudata females who introduce entomopoxvirus (DlEPV) into
their hosts during oviposition (Lawrence and Akin 1990). These virus replicate in the
cytoplasm of the host’s hemocytes and inhibit the host’s encapsulation response
(Lawrence 2005). The incidence and intensity of encapsulation decrease as the
number of parasitoid eggs laid in a host increases (including superparasitism;
Blumberg and Luck 1990; Sagarra, Peterkin, Vincent, and Stewart 2000).
The tendency to superparasitize has also been observed in other species of
Hymenoptera under mass-rearing conditions, such as in Trichogramma spp. Smith
(1996) mentioned that a high female: egg host ratio is conducive to superparasitism,
with the adverse consequence of highly male biased offspring sex ratios and low
quality in the insects produced. According to Wanjberg et al. (1989), superparasitism
in T. maidis must be avoided in mass rearing, in order to reduce the risk of low field
efficiency. However, it is important to highlight that the origin of superparasitism in
each species can be due to different factors, such as host availability, a female’s
previous oviposition experience, host physiological resistance, or the adaptivemechanisms exhibited by parasitoids (Vinson 1984; van Alphen and Visser 1990;
Godfray 1994; Rosenheim and Hongkham 1996). Our findings suggest that super-
parasitism must be carefully evaluated in all contexts. Under mass rearing
conditions, it could have adverse consequences or benefits, and influence the success
or failure of biocontrol programs. The prevalence and implications of this
phenomenon under natural field conditions also needs to be investigated. Pre-
liminary observations on D. longicaudata (P. Montoya, unpublished data), indicate
that superparasitism is not unusual in nature.
In summary, our data showed that wild and laboratory reared females possessed
the same basic host discrimination and oviposition behaviors, and that mass rearing
Biocontrol Science and Technology 145
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
for 156 generations has only selected females that are more active during host
searching, perhaps because of the historically high densities of competitors. Our
results highlight why mass rearing of this species has been successful and why
D. longicaudata is one of the most effective biological control agents for augmentativereleases against fruit flies (e.g., Sivinski et al. 1996; Montoya et al. 2000b; Ovruski
et al. 2003).
Acknowledgements
We are grateful to John Sivinski (USDA-ARS) for helpful review of this manuscript, Lia Ruizand Patricia Lopez (Moscafrut Program, SAGARPA-IICA) for technical assistance, JavierValle-Mora (ECOSUR) for assistance in statistical analysis and Julio Dominguez (Moscafrutfacility, SAGARPA-IICA) for providing insects. The study received financial support fromCONACYT project no. 185672 to P.G.
References
Baker, T., Peulet, P.H., and Visser, M.E. (1990), ‘The Ability to Distinguish between HostsContaining Different Numbers of Parasitoid Eggs by the Solitary Parasitoid Leptopilinaheterotoma (Thomson) (Hym., Cynip.)’, Netherlands Journal of Zoology, 40, 514�520.
Blumberg, D., and Luck, R.F. (1990), ‘Differences in the Rates of Superparasitism betweenTwo Strains of Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) ParasitizingCalifornia Red Scale (Homoptera: Diaspididae): An Adaptation to Circumvent Encapsula-tion?’, Annals of the Entomological Society of America, 83, 591�597.
Cancino, J. (1997), ‘Procedimientos y fundamentos de la crıa masiva de Diachasmimorphalongicaudata (Ashmead) parasitoide de moscas de la fruta’, in Memorias del Curso Regionalsobre Moscas de la Fruta y su Control en Areas Grandes con Enfasis en la Tecnica del InsectoEsteril. SAGAR-OEIA, Metapa de Domınguez, Chiapas, Mexico, pp. 415�424.
Carrasco, M., Montoya, P., Cruz-Lopez, L., and Rojas, J.C. (2005), ‘Response of the Fruit FlyParasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to Mango FruitVolatiles’, Environmental Entomology, 34, 576�583.
Cayol, J.P. (2000), ‘Changes in Sexual Behavior and Life History Traits in Tephritid SpeciesCaused by Mass Rearing Processes’, in Fruit Flies (Tephritidae): Phylogeny and Evolution ofBehavior, eds. M. Aluja and A.L. Norrbom, USA: CRC Press, pp. 843�860.
Domınguez, J.C., Hernandez, C., and Moreno, P. (1997), ‘Metodos de crıa masiva de moscasde la fruta’, in Memorias del Curso Regional sobre Moscas de la Fruta y su Control en AreasGrandes con Enfasis en la Tecnica del Insecto Esteril, SAGAR-OEIA, Metapa deDomınguez, Chiapas, Mexico, pp. 355�367.
Godfray, H.C.J. (1994), Parasitoids Behavioral and Evolutionary Ecology, Princeton, NJ:University Press, Princeton.
Gonzalez, P., Montoya, P., Perez-Lachaud, G., Cancino, J., and Liedo, P. (2007), ‘Super-parasitism in Mass Reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera:Braconidae), a Parasitoid of Fruit Flies (Diptera: Tephritidae)’, Biological Control, 40, 320�326.
Greany, P.D., Tumlinson, J.H., Chambers, D.L., and Boush, G.M. (1977), ‘Chemical MediatedHost Finding by Biosteres (Opius) longicaudatus, a Parasitoid of Tephritid Fruit FlyLarvae’, Journal of Chemical Ecology, 3, 189�195.
Hernandez, E., Toledo, J., Artiaga-Lopez, T., and Flores, S. (2009), ‘Demographic Changes inAnastrepha obliqua (Diptera: Tephritidae) Throughout the Laboratory ColonizationProcess’, Journal of Economic Entomology, forthcoming.
Lawrence, P.O. (1981), ‘Host Vibration � A Cue to Host Location by the Parasite Biostereslongicaudatus’, Oecologia, 48, 249�251.
Lawrence, P.O. (1988), ‘Superparasitism of the Caribbean fruit fly, Anastrepha suspensa(Diptera: Tephritidae), by Biosteres longicaudatus (Hymenoptera: Braconidae): Implica-tions for Host Regulation’, Annals of the Entomological Society of America, 81, 233�239.
146 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
Lawrence, P.O. (2005), ‘Morphogenesis and Cytopathic Effects of the Diachasmimorphalongicaudata Entomopoxvirus in Host Haemocytes’, Journal of Insect Physiology, 51, 221�233.
Lawrence, P.O., and Akin, D. (1990), ‘Virus-like Particles in the Accessory Glands of Biostereslongicaudatus’, Canadian Journal of Zoology, 68, 539�546.
Lawrence, P.O., Greany, P.D., Nation, J.L., and Baranowski, R.M. (1978), ‘OvipositionBehavior of Biosteres longicaudatus, a Parasite of the Caribbean Fruit Fly, Anastrephasuspense’, Annals of the Entomological Society of America, 71, 253�255.
Leyva, J.L., Martınez, L., and Valdez, J. (1988), ‘Mecanismos de deteccion de huespedutilizados por Diachasmimorpha longicaudata y estructura de los organos de recepcion’,Folia Entomologica Mexicana, 6, 165�176.
Liedo, P., and Carey, J.R. (1996), ‘Demography or Fruit Flies and Implications to ActionPrograms’, in Fruit Fly Pests: A World Assessment of Their Biology and Management, eds.D.A. McPheron and G. Steck, Delray Beach, FL: St. Lucie Press, pp. 299�308.
Liedo, P., Salgado, S., Oropeza, A., and Toledo, J. (2007), ‘Improving Mating Performance ofMass-Reared Sterile Mediterranean Fruit Flies (Diptera: Tephritidae) Through Changes inAdult Holding Conditions: Demography and Mating Competitiveness’, Florida Entomol-ogist, 90, 33�40.
Mackauer, M. (1990), ‘Host Discrimination and Larval Competition in Solitary Endopar-asitoids’, in Critical Issues in Biological Control, eds. M. Mackauer, L.E. Ehler andJ. Roland, Andover: Intercept, pp. 41�62.
Mackauer, M., and Chau, A. (2001), ‘Adaptive Self Superparasitism in a Solitary ParasitoidWasp: The Influence of Clutch Size on Offspring Size’, Functional Ecology, 15, 335�343.
Miyatake, T. (1998), ‘Genetic Changes of Life History and Behavioral Traits During Mass-rearing in the Melon Fruit Fly, Bactrocera cucurbitae (Diptera: Tephritidae)’, Researches onPopulation Ecology, 40, 301�310.
Montoya, P., Liedo, P., Benrey, B., Barrera, J.F., Cancino, J., and Aluja, M. (2000a),‘Functional Response and Superparasitism by Diachasmimorpha longicaudata (Hymenop-tera: Braconidae), a Parasitoid of Fruit Flies (Diptera: Tephritidae)’, Annals of theEntomological Society of America, 93, 47�54.
Montoya, P., Liedo, P., Benrey, B., Barrera, J.F., Cancino, J., Sivinski, J., and Aluja, M.(2000b), ‘Biological Control of Anastrepha spp. (Diptera: Tephritidae) in Mango orchardsthrough augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenop-tera: Braconidae)’, Biological Control, 18, 212�224.
Montoya, P., Benrey, B., Barrera, J.F., Zenil, M., Ruiz, L., and Liedo, P. (2003), ‘OvipositionBehavior and Conspecific Host Discrimination in Diachasmimorpha longicaudata (Hyme-noptera: Braconidae), a Fruit Fly Parasitoid’, Biocontrol Science and Technology, 13,683�690.
Montoya, P., Cancino, J., Zenil, M., Gutierrez, J.M., and Santiago, G. (2007), ‘TheAugmentative Biological Control Component in the Mexican Campaign against AnastrephaFruit Flies’, in Area-Wide Control of Insects Pests: From Research to Field Implementation,eds. M.J.B. Vreysen, A.S. Robinson and J. Hendrichs, Dordrecht, The Netherlands:Springer, pp. 661�670.
Ovruski, S.M., Colin, C., Soria, A., Orono, L.E., and Schliserman, P. (2003), ‘Introduccion yproduccion en laboratorio de Diachasmimorpha tryoni y Diachasmimorpha longicaudata(Hymenoptera: Braconidae) para el control biologico de Ceratitis capitata (Diptera:Tephritidae) en la Argentina’, Revista de la Sociedad Entomologica de Argentina, 62, 49�59.
Purcell, M.F., Jackson, C.G., Long, J.P., and Batchelor, M.A. (1994), ‘Influence o f guavaripening on parasitism levels by Diachasmimorpha longicaudata (Ashmead) and otherparasitoids of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae)’, Biological Control, 4,396�403.
Rosenheim, J.A., and Hongkham, D. (1996), ‘Clutch Size in an Obligately Siblicidal ParasitoidWasp’, Animal Behaviour, 51, 841�852.
Sagarra, L.A., Peterkin, D.D., Vincent, C., and Stewart, R.K. (2000), ‘Immune Response ofthe Hibiscus Mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae), toOviposition of the Parasitoid Anagyrus kamali Moursi (Hymenoptera: Encyrtidae)’, Journalof Insect Physiology, 46, 647�653.
Biocontrol Science and Technology 147
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009
Sivinski, J.M., Calkins, C.O., Baranowski, R.M., Harris, D., Brambila, J., Diaz, J., Bums,R.E., Holler, T., and Dodson, D. (1996), ‘Suppression of Caribbean Fruit Fly (Anastrephasuspensa (Loew) Diptera: Tephritidae) Population through Releases of the ParasitoidDiachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae)’, Biological Con-trol, 6, 177�185.
Sivinski, J., Pinero, J., and Aluja, M. (2000), ‘The Distributions of Parasitoids (Hymenoptera)of Anastrepha Fruit Flies (Diptera: Tephritidae) Along an Altitudinal Gradient in Veracruz,Mexico’, Biological Control, 18, 258�269.
Smith, S.M. (1996), ‘Biological Control with Trichogramma: Advances, Successes, andPotential of Their Use’, Annual Review of Entomology, 41, 375�406.
Statsoft, Inc. (2004), STATISTICA (data analysis software system), Version 7. Available from:www.statsoft.com
Tenna, A., Kapranas, A., Garcia-Marı, F., and Luck, R.F. (2008), ‘Host Discrimination,Superparasitism and Infanticide by a Gregarious Endoparasitoid’, Animal Behaviour, 76,789�799.
van Alphen, J.J.M. (1988), ‘Patch-time Allocation by Insect Parasitoids: Superparasitismand Aggregation’, in Population Genetics and Evolution, ed. G. de Jong, Berlin: Springer,pp. 215�221.
van Alphen, J.J.M., and Visser, M.E. (1990), ‘Superparasitism as an Adaptive Strategy forInsect Parasitoids’, Annual Review of Entomology, 35, 59�79.
van Alphen, J.J.M., and Jervis, M.A. (1996), ‘Foraging Behavior. Host Discrimination’, inInsect Natural Enemies. A Practical Approach to their Study and Evaluation, eds. M.A. Jervisand N. Kidd, UK: Chapman and Hall, pp. 32�36.
van Dijken, M.J., and Waage, J.K. (1987), ‘Self and Conspecific Superparasitism by theEgg Parasitoid Trichogramma evanescens’, Entomologia Experimentalis et Applicata, 43,183�192.
van Lenteren, J.C. (1981), ‘Host Discrimination by Parasitoids’, in Semiochemicals. Their Rolein Pest Control, eds. A.D. Nordlun, R.L. Jones and W.L. Lewis, New York: John Wiley &Sons, pp. 153�179.
van Lenteren, J.C., Bakker, K., and van Alphen, J.J.M. (1978), ‘How to Analyze HostDiscrimination’, Ecological Entomology, 3, 71�75.
Vinson, S.B. (1984), ‘How Parasitoids Locate Their Host: A Case of Insect Espionage’, inInsect Communication, ed. S.B. Vinson, London: Royal Entomological Society of London,pp. 325�347.
Waage, J.K. (1986), ‘Family Planning in Parasitoids: Adaptive Patterns of Progeny and SexAllocation’, in Insect parasitoids, eds. J.K. Waage and D.J. Greathead, London: AcademicPress, pp. 63�95.
Wanjberg, E., Pizzol, J., and Babault, M. (1989), ‘Genetic Variation in Progeny Allocation inTrichograma maidis’, Entomologia Experimentalis et Applicata, 53, 177�187.
Weisser, W.W., and Houston, A.I. (1993), ‘Host Discrimination in Parasitic Wasps: When is itAdvantageous?’, Functional Ecology, 7, 27�29.
Wharton, R.A., and Marsh, P. (1978), ‘New World Opiinae (Hymenoptera: Braconidae)Parasitic on Tephritidae (Diptera)’, Journal of Washington Academic Science, 68, 147�167.
White, J.A., and Andow, D.A. (2008), ‘Benefits of Self-superparasitism in a PolyembryonicParasitoid’, Biological Control, 46, 133�139.
Wong, T.T.Y., Ramadan, M.M., Mcinnis, D.O., Mochizuki, N., Nishimoto, J.I., and Herr, J.C.(1991), ‘Augmentative Releases of Dichasmimorpha tryoni (Hymenoptera: Braconidae) toSuppress a Mediterranean Fruit Fly Population in Kula, Maui, Hawaii’, Biological Control,1, 2�7.
Zar, J.H. (1984), Biostatistical Analysis, New Jersey: Prentice-Hall.
148 P.I. Gonzalez et al.
Downloaded By: [Montoya, Pablo J.] At: 17:29 14 December 2009