ARTHROPOD BIOLOGY

Biology of Dineulophus phtorimaeae (Hymenoptera: Eulophidae)
and Field Interaction With Pseudapanteles dignus

(Hymenoptera: Braconidae), Larval Parasitoids of Tuta absoluta
(Lepidoptera: Gelechiidae) in Tomato

MARÍA G. LUNA,1 VERÓNICA I. WADA, AND NORMA E. SÁNCHEZ

CEPAVE (CCT-La PlataÐCONICETÐUNLP), Calle 2 Nro. 584 (1900) La Plata, Argentina

Ann. Entomol. Soc. Am. 103(6): 936Ð942 (2010); DOI: 10.1603/AN10021

ABSTRACT Some biological characteristics of the ectoparasitoid Dineulophus phtorimaeae (de
Santis) (Hymenoptera: Eulophidae) and Þeld interaction with the endoparasitoid Pseudapanteles
dignus (Muesebeck), both larval parasitoids of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae),
were examined. In addition, we completed the original description of D. phtorimaeae. Preimaginal
developmental time of the ectoparasitoid was 11.17 � 0.60 d for both sexes, and adult life span was
11.73 � 0.92 d for females and 8.78 � 0.93 d for males. The proportion of males to females was equal.
In the Þeld, hosts were parasitized at the third larval instar. On average, a female attacked ca. four hosts
throughout her lifetime and deposited eggs in �50% of cases. The most successful female attacked six
hosts, yielding a potential fecundity of �10 eggs. Host paralysis without parasitism was observed,
suggesting stinging for host feeding. The daily oviposition curve is compatible with a synovigenic-type
parasitoid. Our prediction stating thatD. phtorimaeaewould succeed when competing for hosts with
P. dignus was correct, because the former species had greater parasitism rates. In the Þeld, both T.
absoluta parasitoids were able to coexist at leaf scale. The negative aspects of differences in feeding
behavior, narrower host range (third instar), and lower fecundity of D. phtorimaeae would be
compensated by its better attributes as natural enemy, in comparison with P. dignus, enabling
coexistence.

KEY WORDS Dineulophus phtorimaeae, Pseudapanteles dignus, parasitoid, coexistence, Tuta abso-
luta

Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)
is a major pest of greenhouse and open-Þeld tomato,
Solanum lycopersicum L., crops in South America
(Fernández and Montagne 1990; Botto 1999; Ecole et
al. 2000; Siqueira et al. 2000, and references therein).
It has recently been introduced to Europe (Urbaneja
et al. 2009, Netherlands Plant Protection Service 2009,
Speranza et al. 2009). Larvae cause plant damage by
mining leaves and fruit; therefore, the use of chemical
pesticides is a widespread practice to control this pest.
Considering the adverse effects of pesticides to human
health and environment quality, it is important that
alternative methods, such as biological control, are
developed for incorporation into a tomato integrated
pest management (IPM) program (Lewis et al. 1997,
Sánchez et al. 2009).

Successful biological control programs in horticul-
tural crops have been obtained by seasonal augmen-
tative releases of parasitoids (Bale et al. 2008). In
Argentina, T. absoluta has two main native larval para-
sitoids in tomato crops. They belong to different para-

sitoid guilds: the endoparasitoid Pseudapanteles dignus
(Muesebeck) (Hymenoptera: Braconidae), which is
currently under study as a moth control agent (Luna
et al. 2007, Sánchez et al. 2009); and the ectoparasitoid
Dineulophus phtorimaeae (de Santis) (Hymenoptera:
Eulophidae) (de Santis 1983, Colomo et al. 2002). P.
dignus shows some positive biological traits that make
it a promising candidate for conservation biological
control, seasonal augmentative releases, or both
(Luna et al. 2007, Sánchez et al. 2009).D. phtorimaeae
is less well known, with only partial morphological
description (de Santis 1983) and historical reports of
its presence in tomato crops from Argentina and Chile
(Vargas 1970, Larraṍn 1986, Colomo et al. 2002).

Parasitoids are classiÞed as koinobionts or idio-
bionts (Haeselbarth 1979, Askew and Shaw 1986).
Koinobionts allow the host to develop beyond the
stage attacked, whereas idiobionts permanently par-
alyze or kill the host in the stage attacked. In addition,
idiobionts are relatively more generalist (i.e., have
broader speciÞc host range), have larger eggs, faster
larval development, and longer adult life span, and
they live in more protected sites (the majority attack1 Corresponding author, e-mail: lunam@cepave.edu.ar.

0013-8746/10/0936Ð0942$04.00/0 � 2010 Entomological Society of America



concealed hosts) than koinobionts. Furthermore, they
do not elicit physiological defense mechanisms of the
host, e.g., encapsulation. The majority of successful
cultures, including in vitro rearings, have involved
idiobionts, and, in particular, ectoparasitoids (Quicke
1997).

Multiparasitism, i.e., the use of a single host indi-
vidual by two or more parasitoid species, is very
common in nature (Lane et al. 2006). As a result,
parasitoids can experience intra- and interspeciÞc
competition. Categorization of parasitoids in koino-
and idiobionts is a practical indication useful to ana-
lyze their potential as a biological control agent as well
as their ability to compete within a particular parasi-
toid assemblage (Mills 2006). Life history traits such as
host immobilization, shorter developmental times,
and higher searching abilities allow predicting that
ectoparasitoid idiobionts are competitively superior to
koinobionts (Hawkins 2000, Strand 2000). The study
of potential coexistence of two parasitoid species on
the same host and their impact on to top-down limi-
tation of a pest population is a relevant topic in bio-
logical control.

The goals of this research were two-fold: 1) to study
some general biological aspects ofD. phtorimaeae and
2) to assess its interaction with P. dignus in tomato
Þelds. Based on the hypothesis that the idiobiont D.
phtorimaeae would be a better competitor than the
koinobiont P. dignus,we predicted that in the ÞeldD.
phtorimaeae would produce higher parasitism rates
than the endoparasitoid P. dignus.

Materials and Methods

Biology of D. phtorimaeae. Field collections of to-
mato leaves with T. absoluta damage were made in
commercial crops located in the vicinity of La Plata, a
major horticultural region of Buenos Aires province,
Argentina (34� 58� S, 57� 59� W) (Sánchez et al. 2009).
Host stage attacked, preimaginal developmental time
of the parasitoid, and sex ratio were determined and
recorded.

Mines were dissected under a stereomicroscope to
search for presence of miners and parasitoids and to
observe the instar attacked. All hosts with the pres-
ence ofD.phtorimaeae larvae were individually reared
in 5-ml glass vials. To allow proper pupal formation
and prevent degradation of plant material, vials were
provided with one by 0.5-cm Þlter paper card wetted
with distilled water and kept sealed. They were
checked daily to correct water saturation or dryness
inside. Sexes were identiÞed at pupal stage based on
dimorphic differences, such as shorter body length
and a translucent area on the gaster in males, visible
�24 h before adult emergence (de Santis 1983). In-
sects were kept in a walk-in-chamber at 25 � 3�C, 70 �
10% RH, and a photoperiod of 14:10 (L:D) h.

The specimens obtained through these collections
wereobservedundera stereomicroscope(modelSMZ
800, Nikon, Melville, NY) to describe pupal and imag-
inalmorphology.Tenwaspsofeach sexweredissected
in distilled water and transferred into glycerin to mea-

sure pupal and adult body sizes (length). Means and
SEs were calculated as descriptive statistics. In addi-
tion, illustrations of adults of both sexes were made,
because only partial visual descriptions made by de
Santis (1983) were available thus far. The parasitoid
preimaginal developmental time for both sexes was
calculated as the mean number of days from larvae at
early instars (L1 to L2) to adult emergence. The sex
ratio was calculated as the total number of males/
(number of males � number of females).

For the adult stage, the following biological char-
acteristics were recorded in the laboratory: longevity
(both sexes), oviposition behavior (host feeding and
egg laying), daily oviposition rate, total fecundity, and
mean brood size. Newly emerged adults were paired
and placed in 5-ml glass vials containing a 1- by 0.5-cm
Þlter paper card with honey solution (50%). Couples
were allowed to mate for 24 h, and then mated females
were relocated to 60-ml vials and provided with Þve
third-instar host larvae from a laboratory colony (see
below). Vials were monitored daily and batches of Þve
hosts were replaced when signs of parasitoid attack
were detected, until each female died. Males were
kept apart, provided with honey solution until death.

Hosts were produced by rearing aT. absolutacolony
as reported previously (Luna et al. 2007). All hosts
used during the experiment were already installed in
mines.

To determine host parasitoid attack (host paralysis
or presence of D. phtorimaeae eggs or larvae) indi-
viduals were checked under a stereomicroscope. All
parasitized hosts were transferred to 5-ml vials until
parasitoid pupa formation. Mean adult longevity of
both sexes was measured as the mean number of days
wasps lived, from adult emergence to death.

Fecundity was measured by two means: 1) lifetime
fecundity, as the mean number of eggs per female
wasp; and 2) potential fecundity (as in Zaviezo and
Mills 1999),bymultiplying theaveragenumberofeggs
laid per host by each female by the number of hosts
parasitized by the most successful female.

Life history data are presented as mean � SE. Dif-
ferences in preimaginal developmental time and adult
longevity between sexes of D. phtorimaeae were an-
alyzed by one-way analysis of variance (ANOVA).
Before analysis, data were checked for normality and
homogeneity of variances. When ANOVA assump-
tions were violated, a KruskalÐWallis test was used.
Differences were considered signiÞcant at P � 0.05.
Analyses were performed with Statistica 7.0 (StatSoft
2007).
Field Interaction With P. dignus. To assess inter-

action between D. phtorimaeae and P. dignus in the
Þeld, we carried out a sampling of both parasitoid
species in an organic open-Þeld tomato crop in the
study area. The inßuence of the spatial scale of analysis
on patterns of parasitism has been widely discussed
previously (Heads and Lawton 1983, Lill 1998). A
previous study indicated that P. dignus concentrates
on tomato crops with greater host density but displays
a density-independent rate of parasitism in relation to
T. absoluta larval density, at the leaf spatial scale

November 2010 LUNA ET AL: BIOLOGY OF D. phtorimaeae IN TOMATO 937



(Sánchez et al. 2009). Thus, we analyzed the interac-
tion between both parasitoids at that spatial scale, and
established groups according to host density recorded
(from one to the maximum number of larvae found)
per leaf.

The sampling took place in late March 2004, when
host and parasitoid populations were conspicuously
settled in crops. Samples consisted of the third apical
part (containing approximately eight expanded
leaves) of 20 plants, randomly selected. In the labo-
ratory, plants were sorted in all component leaves and
then viewed under a stereomicroscope to search forT.
absoluta larvae and for the ectoparasitoid (egg, larva,
or pupa). To Þnd the endoparasitoid, living host larvae
were placed individually in petri dishes, provided with
fresh tomato leaves as food, and maintained in a
walk-in rearing chamber at 25 � 2�C temperature, 70%
RH, and a photoperiod of 14:10 (L:D) h until P. dignus
cocoon formation. Dead hosts were dissected to check
whether they were parasitized by the endoparasitoid
(egg and larva).

The number of T. absoluta larvae and the number of
ecto- and endoparasitoids per leaf were recorded. The
proportions of parasitized T. absoluta for each para-
sitoid species, and for both species in the same leaf,
were estimated as the number of parasitized larvae/
total number of hosts collected. Proportions were av-
eraged by each host density group and arcsine trans-
formed for further analyses.

The differences in mean proportions of parasitism
(response variable) by each parasitoid species, occur-
ring alone or together in the same leaf (categorical
independent variable with three categories: P. dignus
only,D. phtorimaeae only, or both), at each host den-
sity category (continuous independent variable)
could not be analyzed by a two-way ANOVA due to
non-normality of data. One-way analysis of covariance
for the same response variable and using the number
of parasitoids found per leaf (P. dignus, D. phtori-
maeae, or both) as a categorical independent variable
and the host density as a covariate (more than one
larva per leaf) could not be used either because the
categorical variable slopes were heterogeneous
(Gotelli and Ellison 2004). Thus, we evaluated the
response variable for each host density group sepa-
rately, using one-way ANOVA (or KruskalÐWallis
when ANOVA assumptions could not be corrected
with transformations). Additionally, we examined the
relationship between mean total proportions of par-
asitism by each single species (occurring alone or
together with the other parasitoid in the same leaf) by
linear regressions. The null hypothesis was that the
proportion of parasitism by each species does not vary
with host density. Analyses were performed with Sta-
tistica 7.0 (StatSoft 2007), and a signiÞcance level of
P � 0.05 was chosen for all statistical analyses.

Results

Biology of D. phtorimaeae. Body size (length) was
2.28 � 0.09 mm (n � 47) for the pupal stage, 1.69 �
0.14 mm (n � 10) for the adult male, and 2.17 � 0.13

mm (n � 10) for females (Fig. 1). The latter value is
larger than that described previously (de Santis 1983).
Sexual dimorphism was noted at pupal stage: males can
be distinguished 24 h before adult emergence by the
translucent area on the gaster, a characteristic de-
scribed for the imago (de Santis 1983).

Preimaginal developmental time was 11 d for both
sexes (H � 0.31, df � 1, P � 0.57; n � 47) (Table 1).
Adult longevity differed signiÞcantly between sexes,
being longer for females(F�4.45;df�1, 34;P�0.04).

Fig. 1. D. phtorimaeae adult female (a) and male (b).

Table 1. Life history traits of D. phtorimaeae, a larval ecto-
parasitoid of T. absoluta

Trait Value

Preimaginal developmental time
(mean � SE, d)

Female 11.06 � 0.38
Male 11.29 � 0.81
Total 11.17 � 0.60

Adult longevity (mean � SE, d)
Female 11.73 � 0.92
Male 8.78 � 0.93

Sex ratio (no. males/no. males � no. females) � 0.51
(n � 48)

Reproductive behavior (mean � SE no.)
Paralyzed hosts/female (n � 13) 2.00 � 0.60
Parasitized hosts/female (n � 9) 1.61 � 0.60

Potential fecundity (eggs/female) (n � 9) 9.69 � 3.61

938 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 6



The proportion of sexes was equal under Þeld condi-
tions (n � 48).
D. phtorimaeae larval morphology was hymenop-

teriform. All parasitized host larvae collected in the
Þeld and brought to the laboratory were late larvae
(mainly third instar), and all had only a single para-
sitoid larva (n � 122).

Thirteen of 24 coupled D. phtorimaeae attacked
hosts, and nine of those 13 D. phtorimaeae effectively
parasitized T. absoluta larvae. All of them showed
symptoms of permanent paralysis and could be dis-
tinguished from active larvae by their yellowish col-
oration and lack of mobility. The host larvae died
within 24 h after the parasitoids began to feed. Some
paralyzed hosts lacked a D. phtorimaeae egg, an indi-
cation of nonconcurrent host feeding. On average, a
female attacked four hosts throughout her lifetime and
deposited eggs in �50% of the cases. The number of
hosts attacked by the most successful female was six,
yielding a potential fecundity of �10 eggs (Table 1).
Only one individual parasitoid per host developed
effectively, although up to two D. phtorimaeae eggs
were observed on some hosts. Females frequently
entered the mines to attack T. absoluta larvae and
failed to parasitize moth larvae outside tomato leaves.
Pleiotropism of hatched larvae on paralyzed hosts was
observed.

The Þrst oviposition event took place 4 d after the
Þrst batch of hosts was offered and the maximal daily
mean of oviposition rate was 1.2 hosts, at the Þfth day
of female life. The shape of the oviposition curve
showed a synovigenic-type parasitoid behavior (Fig.
2).
Evidence for Parasitoid Guild Interaction. In total,

160 leaves were observed, yielding 324 T. absoluta
larvae in 97 leaves. In total, both parasitoid species
attacked �45% ofT. absoluta larvae; 20% were affected
by the ectoparasitoid and 23.34% by the endoparasi-
toid. We recorded six groups of parasitized host den-
sities at leaf spatial scale (1, 2, 3, 4Ð6, 7Ð10, and 12Ð16
larvae per leaf). The range of host densities agreed
with those reported for organic tomato crops in the
region (Sánchez et al. 2009).

Differences in percentages of parasitism among cat-
egories were found at a density of one host per leaf

(H � 7.70, df � 1, P � 0.005; n � 64), with P. dignus
parasitism higher than that ofD.phtorimaeae(Fig. 3a).
We also found that parasitism due to both species in
the same leaf, at a density of four to six larvae per leaf,
was signiÞcantly greater than those caused by each
parasitoid alone (F� 9.04, df � 2, P� 0.002) (Fig. 3d).
However, at most host densities there were no differ-
ences in percentages of parasitism among categories
(two hosts per leaf:H� 5.65, df � 2, P� 0.06 [n� 12];
three hosts per leaf: H � 3.01, df � 2, P � 0.22 [n �
11]; and 7Ð10 hosts per leaf:H� 1.97, df � 2, P� 0.37
[n� 8]) (Fig. 3b, c, and e). It also was observed that
at the host density category �10 hosts per leaf, par-
asitism always involved both species (Fig. 3f). When
the proportion of parasitism by each single species was
discriminated in the both species in the same leaf
category across the host densities (Fig. 3bÐf), we ob-
served that the ectoparasitoid increased its percentage
of parasitism of T. absoluta with respect to P. dignus,
as the host density increased, attaining values as high
as 85Ð95%.

Regression analyses revealed that total mean pro-
portion of parasitism by D. phtorimaeae increased
signiÞcantly with host density, whereas that caused
by P. dignus showed a decreasing pattern, although
the slope was not signiÞcant in the latter case
(Table 2).

Discussion

The preimaginal and imaginal morphological traits
of D. phtorimaeae reported in this article expand the
original descriptions made by Blanchard (1939) and
de Santis (1983).
D. phtorimaeae exhibits promising traits to be a

successful biocontrol agent. This study provides evi-
dence that it can immobilize hosts permanently, in the
presence or absence of oviposition. A relatively faster
preimaginal developmental time for both sexes and a
slightly longer adult life span confer a moderate short-
lived generation of �23 d, compared with P. dignus
(�36 d; Luna et al. 2007).

In the Þeld, D. phtorimaeae can be responsible for
�30% parasitism of its host, as demonstrated in this
study and reported previously (Larraṍn 1986, Colomo
et al. 2002), and its attack rates can increase with host
density increment. An extra beneÞt can be obtained
by host feeding, which causes additional host mortal-
ity and prevents consumption of foliage (Briggs 1993,
Jervis and Kidd 1999). However, the amount of T.
absolutamortality by host feeding in the Þeld was not
estimated in this study.

Relatively low D. phtorimaeae fecundity can be re-
lated to synovigeny, a predominant egg maturation
pattern among parasitoid wasps (Jervis et al. 2001),
because this results in energetically expensive pro-
duction of eggs with large quantities of yolk. Host
feeding can provide those nutrients but is another
costly and time-consuming process that can also limit
the number of progeny (Rivero and West 2005). Al-
though high fecundity is an expected positive life trait
for an efÞcient biological control agent, there are

Fig. 2. Daily number of eggs (mean � SE) oviposited
over the lifetime ofD. phtorimaeae females with a T. absoluta
larval density of Þve per day.

November 2010 LUNA ET AL: BIOLOGY OF D. phtorimaeae IN TOMATO 939



reports of successful agents with similar oviposition
rates to D. phtorimaeae, such as the bethylid Prorops
nasutaWaterston (Infante et al. 2005), with 4.3 prog-
eny per female; the eulophids Eulophus pennicornis
(Nees), Hyssopus pallidus (Askew), and Euplectrus
maternus Bhatnagar, with 1.5 and 14 hosts per female
and 22.2 eggs per female, respectively (Marris and
Edwards 1995, Zaviezo and Mills 1999, Muniappan et
al. 2004); and for the ichneumonidMastrus ridibundus
Gravenhorst, with 0.4Ð0.9 hosts per day (Bezemer and
Mills 2001).

Our prediction stating that D. phtorimaeae would
succeed when competing for hosts with P. dignuswas
correct; indeed, we registered higher D. phtorimaeae
parasitism. Both parasitoids can coexist at the host

densities recorded in the Þeld and also produce higher
parasitism rates than those reported forP.dignuswhen
it occurred alone (Sánchez et al. 2009).

Modeling results of host-parasitoid interactions
(Lane et al. 2006) indicated that a limited fecundity of
one species does not inevitably reduce the potential
for coexistence, provided one is more efÞcient and the
other more fecund. Also, different host density levels
and host niche differentiation contribute to multiple
parasitoid species coexistence (Briggs 1993, Mills
2006). All these factors seem to occur in the P. dig-
nusÐD. phtorimaeaeÐT. absoluta system.

InterspeciÞc competition in primary parasitoids has
been explained by competitive exclusion and coexist-
ence (Briggs 1993, Ueno 1999, Collier and Hunter
2001, Collier et al. 2007, Mills 2006). Mechanisms in-
volved in competitive interaction of dual parasitoid
species at immature stages are as follows: 1) interfer-
ence, with both larvae in the same host, including
multiparasitism and intraguild predation via killing
competitors, ovicide, and host feeding; and 2) exploi-
tation, when earlier-attacking parasitoids reduce host
density for the second species. There is also the po-
tential for adult competition via mutual interference
by females searching for hosts and mechanisms deal-

Fig. 3. Mean (�SE) proportions of Þeld-parasitized T. absoluta larvae by two parasitoid species at six different host
densities (La Plata, Buenos Aires, Argentina). Pd, P. dignus alone in a leaf; Dp, D. phtorimaeae alone in a leaf; and Both, two
species in the same leaf. SigniÞcant differences are given by different letters. Parasitism ratios of P. dignus versus D.
phtorimaeae are indicated in the box.

Table 2. Regression analyses of total proportion of T. absoluta
parasitized by P. dignus and D. phtorimaeae, occurring alone or
both in the same leaf, on six host densities per leaf (1, 2, 3, 4–6,
7–10, and 12–16)

Species Slope � SE R2 F df P

D. phtorimaeae 0.32 � 0.10 0.10 10.74 1, 95 0.02*
P. dignus �0.13 � 0.10 0.02 1.67 1, 95 0.20

* SigniÞcant differences at P 	 0.05.

940 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 6



ing with spatial and temporal heterogeneity on host
resources (Hawkins 2000).

The mechanisms involved in the competence be-
tween P. dignus andD. phtorimaeae are thought to be
mainly via interference, although exploitation de-
serves to be further explored, because P. dignus needs
healthy hosts in which to oviposit (Larraṍn 1986, Luna
et al., 2007, Sánchez et al. 2009). According to Mills
(2006), despite theoretical predictions of competitive
exclusion, Þeld data indicate that multiple natural en-
emy coexist on shared hosts, at least on a seasonal
basis.

In the current study, two effective natural enemies
of T. absoluta, a key pest in South America, have been
identiÞed. This research documents the potential im-
portance of two native parasitoids for the develop-
ment of biological control programs for T. absoluta,
and demonstrates how two competing species with
complementary combinations of life history traits can
be compatible. This type of information is also criti-
cally important if these wasps are to be considered for
importation into Europe, where T. absoluta has re-
cently been introduced, or elsewhere.

Acknowledgments

We thank tomato growers I. Abán, P. Peralta, M. del Pino,
M. Maita, R. López, S. Parrillo, and M. E. Senattori for per-
mission to collect material from their farms and E. Nieves and
J. Rouaux (Centro de Estudios Parasitológicos y de Vectores
CCT CONICET-UNLP) for technical assistance. We thank J.
Capinera (University of Florida) for reviewing the manu-
script and for his helpful suggestions. M. C. Estivariz made
the illustrations. This research was supported by grants from
Consejo Nacional de Investigaciones CientṍÞcas y Técnicas
(PIP 2000), Universidad Nacional de La Plata (Projects 396,
01/01/2002, and 452, 01/01/2005), and ANPCyT (IM 40-
2000).

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Received 9 February 2010; accepted 29 June 2010.

942 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 6