BioControl (2005) 50: 259–270
Springer 2005

Life history studies of Prorops nasuta, a parasitoid of the

coffee berry borer

Francisco INFANTE1*, John MUMFORD2 and Peter BAKER3

1
El Colegio de la Frontera Sur (ECOSUR), Departamento de Entomologia Tropical,
Carretera Antiguo Aeropuerto km 2.5, Tapachula, 30700 Chiapas, Mexico; 2Imperial
College at Silwood Park, Ascot Berkshire SL5 7PY, UK; 3CABI-Bioscience, Bakeham
Lane, Egham, Surrey TW20 9TY, UK
*Author for correspondence; e-mail: finfante@tap-ecosur.edu.mx

Received 12 August 2003; accepted in revised form 2 July 2004

Abstract. Life history studies were conducted in the laboratory on the African para-
sitoid Prorops nasuta Waterston (Hymenoptera: Bethylidae), a parasitoid of the coffee
berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). The female wasp
enters an infested coffee berry, kills the adult borer and seals the entrance of the berry
with the body of the borer, impeding the entry of other organisms into the berry. The
preoviposition period ranges from 3 to 14 days (mean 5.42 ± 0.37 SE). During this
time females feed on the immature stages and paralyse fully grown larvae and pupae of
the CBB. P. nasuta is an idiobiont solitary ectoparasitoid. Eggs are laid externally on the
last instar larvae and pupae. Mean development time (egg to adult) for males and
females was 27.7 (±0.37 SE) and 30 (±0.12 SE) days, respectively. Median survival for
wasps fed on final instar CBB larvae was 27.7 days, significantly longer than any other
treatment, while for females without food it was 2.5 days. In culture, females produced
an average of 4.3 (±0.39 SE) progeny during their lifetimes. Adults began emerging at
30.6 days (±0.28 SE) after cultures were started and peak production was reached at 36
days, declining thereafter. Males normally emerged from coffee beans 2–3 days before
females. Males usually emerged from 07:00 to 09:00 h and females from 10:00 to
14:00 h. The culture sex ratio (proportion of males) was 0.21. Virgin females produced
only male offspring.

Key words: Bethylidae, biological control, Hypothenemus, Mexico, Prorops

Introduction

The coffee berry borer (CBB), Hypothenemus hampei (Ferrari) (Coleoptera:

Scolytidae), was accidentally introduced into Mexico from Guatemala in the
late 1970s (Baker, 1984), and rapidly became an important pest of coffee. At
present, coffee production in this country depends largely on the adequate
management of H. hampei. As an attempt to control this pest by biological
means, the parasitoid Prorops nasuta Waterston (Hymenoptera: Bethylidae)
260 FRANCISCO INFANTE ET AL.

was introduced into Mexico at the end of 1992 from Brazil, where this wasp
was originally imported from Uganda in 1929 (Hempel, 1934; Le Pelley, 1968).
Efforts to introduce P. nasuta to Mexico directly from Africa (Kenya and
Togo) were unsuccessful in 1988, 1989 and early 1992, due to problems in the
rearing system, which led to the death of the colonies after a few generations,
before field releases could be made (Barrera et al., 1990; Infante, 1998).
P. nasuta is one of three African parasitoids introduced into Mexico and
other Latin American countries for the biological control of CBB (Murphy and
Moore, 1990; Baker, 1999). The results obtained with this parasitoid in most
countries have been very poor in terms of field establishment and control of the
pest (De Ingunza, 1964; Heinrich, 1965; Barrera et al., 1990; Ferreira and Paes,
1995; Ruales, 1997; Infante et al., 2001). In the case of Mexico, more than
156,000 individuals were released in coffee plantations of Chiapas from 1992 to
1996 in 22 colonization sites, but up to now there are no evidence of the
establishment of this parasitoid in the country (Infante et al., 2001). Appar-
ently this species is only able to maintain high populations in the field if there
are multiple releases through the coffee season, otherwise, parasitoid popula-
tions decreased impressively (Infante, 1998). Cephalonomia stephanoderis
(Bethylidae), another parasitoid introduced into the Americas, has been
extensively established in most countries were has been released (Barrera, 1994;
Baker, 1999). However, after its establishment, C. stephanoderis exhibited low
parasitism rates if there are no additional releases (Barrera, 1994). It is con-
sidered that C. stephanoderis alone is not able to control CBB below eco-
nomical thresholds and other control methods are needed (Damon, 1999). A
third parasitoid Phymastichus coffea (Eulophidae) has recently been imported
and its value as a biological control agent is currently under evaluation. A
simulation model developed by Gutierrez et al. (1998) to assess the efficacy of
natural enemies of CBB suggested that control of the pest could be improved
when using C. stephanoderis and/or P. nasuta in combination with P. coffea.
In the present paper, several studies derived from the importation of
P. nasuta into Mexico are reported. All trials were designed to obtain infor-
mation on aspects regarding to the life history (development time, survival,
fecundity, parthenogenesis, and sex ratio) of this parasitoid.

Materials and methods

Foreign exploration and quarantine

In the middle of 1992 the parasitoid P. nasuta was collected from the field in
several locations of Minas Gerais, Brazil. Specimens were quarantined at the
Instituto Agronómico do Paraná for at least one generation, reared on CBB
 LIFE HISTORY STUDIES OF PROROPS NASUTA 261

that had been reared on an artificial diet (Villacorta, 1985). Subsequently, adult
parasitoids were shipped to Tapachula, Chiapas, Mexico, in glass tubes with
CBB eggs and larvae as food. In total 191 live individuals were received in four
shipments. Experiments reported in this paper were carried out during 1996
and 1997.

Parasitoid cultures

In the laboratory at ECOSUR, Tapachula, P. nasuta was reared on CBB-

infested ripe coffee berries collected regularly from coffee plantations, where
the parasitoid has never been released. These fresh berries were kept in the
laboratory for 3 days on trays lined with tissue paper to reduce humidity.
Cultures of P. nasuta were then established at a ratio of one female parasitoid
per 1.5 berries using circular plastic jars (22 cm in diameter and 10 cm high)
with a ventilated mesh lid. To avoid proliferation of saprophytic fungi, only a
single layer of berries was placed in each jar (approximately 200 coffee berries).
Four weeks after the culture was started, frass and dust were removed and the
jars were placed under fluorescent lights where they were checked several times
per day to collect and record parasitoids emerging from the coffee berries. A
selection of 50 parasitoid culture containers was observed to determine the
number, sex ratio and emergence time of offspring. The laboratory culture was
maintained under cycling temperature regimes ranging from 18 to 30 C (16
and 8 h respectively), relative humidity ranging from 60% to 85% and a 12 h
light:dark photoperiod.

Life history

Parasitoids were observed in the laboratory. P. nasuta eggs were obtained by

inducing females to oviposit on CBB hosts (larvae and pupae) extracted from
infested coffee berries collected from the field. The eggs and their host were
placed individually in aluminium foil cups (1 cm in diameter) lined with a piece
of black drawing paper in the bottom of the cup to distinguish the white eggs of
the parasitoid. These cups were held inside glass tubes 7.5 cm long · 1.5 cm
diameter closed with fine mesh, to observe the parasitoid development daily.
To determine the preoviposition period and the behaviour of the wasp inside
the coffee fruit, five berries, chosen randomly, were dissected every second day
from the start of the cultures up to 15 days (eight sets in total).
To determine the sex ratio in the culture, 50 adults of P. nasuta were col-
lected from the culture each week during a period of 6 months. The parasitoids
were dissected under a stereomicroscope to determine the sex. In total, 1500
individuals were examined. The effect of parthenogenesis was examined in 81
virgin females taken from intact cocoons, which were cultured in 20 containers
262 FRANCISCO INFANTE ET AL.

holding field collected coffee berries infested with CBB. The sex of the offspring
of these females was recorded.

Survivorship of adult females

Longevity studies of P. nasuta females fed on several diets were conducted

individually in glass vials 7.5 cm long · 1.5 cm diameter closed with fine mesh
to prevent the female from escaping. There were seven treatments: CBB adults,
CBB pupae, CBB larvae, CBB eggs, distilled water, honey, and control (no
food). Each treatment consisted of 15 newly emerged females placed individ-
ually inside the tubes. In the treatments using different stages of the CBB, adult
and juvenile stages were obtained by dissections of field infested coffee berries.
Adults, pupae, larvae and eggs of CBB were placed in foil cups as described
above and exposed to the wasp inside the glass vials. In this way, the manip-
ulation of organisms was relatively easy and harmless. Honey and distilled
water treatments were offered on a piece of filter paper. In the control dry filter
paper was used. All treatments were replenished every day.

Statistical analysis

The F-test was used to check homogeneity of variance for data pertaining to
males and females in the life history studies. The data were compared through
a t-test analysis, assuming equal variances. Survivorship data were analysed
using the Kaplan Meier Survival Analysis with Log-Rank Comparisons (SPSS
for Windows 10.0, SPSS Inc., 1999). In all statistical analyses p-values < 0.05
were considered significant.

Results

Life history

The parasitoid production in the 50 selected culture containers is shown in

Figure 1. On average each female in culture produced 4.3 (±0.39 SE) individual
offspring.
Before entering an infested fruit, the female wasp has to fight with the CBB
female who reacts to the wasp’s presence by blocking the entrance hole to its
gallery with her body. The female wasp tries to sting the borer with its ovi-
positor. Within 15 min, there is usually an outcome of this fighting with three
possibilities: (i) the borer escapes from the berry without being stung by the
wasp; (ii) The CBB female is stung and tries to escape from the berry, but the
venom paralyses her and dies outside the berry; and (iii) the CBB female stays
 LIFE HISTORY STUDIES OF PROROPS NASUTA 263

400

300
Offspring

200

100

y = 4.3659x + 0.5586
2
R = 0.5228
0
0 10 20 30 40 50 60 70 80

Number of Parasitoids in Culture

Figure 1. Relationship between the number of parasitoids in culture and production of

Prorops nasuta under fluctuating temperatures (18–30 C) in the laboratory.

in the berry trying to protect her progeny, and the wasp kills her inside the
berry. If there is more than one CBB adult inside the berry, all may be killed.
The P. nasuta female kills adult CBB by severing the thorax and head from the
abdomen. Subsequently, the abdomen of the borer is placed in the entrance
hole, presumably to impede the entrance of predators, hyperparasitoids or
competitors. Once the female parasitoid has entered an infested berry, it usu-
ally spends the remainder of its life inside it. The preoviposition period ranges
from 3 to 14 days (mean 5.42 ± 0.37 SE; n ¼ 40 individuals). During this time
the wasp feeds on the immature stages and paralyses the full-grown larvae and
pupae. The female parasitoid is able to feed on all the juvenile stages of the
CBB, but not on adults.
P. nasuta is an idiobiont solitary parasitoid. Eggs are usually deposited
externally on the last instar larvae and pupae. Although the preference to
oviposit for each stage was not formally recorded, it was noted that most eggs
were laid on the final instar larvae, rather than on pupae. Oviposition must be
precise to achieve successful development of the larvae. If the anterior pole of
the egg is not in close contact with its host, the larvae will hatch but cannot
feed on the host and soon will die from lack of nourishment. If eggs oviposited
on pupae are laid on hard regions such as the thorax, head or proto-wings, the
larvae will also starve. It was observed (n ¼ 54 individuals) that when the
parasitoid egg did not develop successfully the paralysed host failed to continue
development and after several weeks the paralysed and mummified immature
borers had died.
264 FRANCISCO INFANTE ET AL.

In Table 1, developmental times for the different biological stages are

presented for both sexes. After the incubation period, larvae feed immediately
on hatching. They only feed on a single host, which is sufficient for their
development. P. nasuta larvae die if detached from their host, even if other
hosts were close by. When wasps are ready to emerge from the pupal case they
remain inside the cocoon for about a day, after which they chew one end off the
silk cocoon to emerge. Females emerged approximately 2.5 days after males.
Superparasitism is rare and cannibalism was never observed.
The male proportion in the population ranged from 0.40 to 0.04. Overall,
the mean sex ratio (male proportion) for all wasps emerging in the cultures
observed during 6 months was calculated as 0.21. Cultures with virgin females
produce male offspring. Virgin females produced an average number of
progeny ranging from 1 to 8 per wasp (overall average 3.6).

Survivorship of adult females

The median survivorship of P. nasuta females on the different diets was 6.7,
27.7, 8.7, 2.2, 2.1, 4.0 and 2.5 days; when exposed to eggs, larvae, pupae,
adults, honey, water and control, respectively (Figure 2). In the last four
treatments no wasps lived beyond 6 days. The maximum longevity was re-
corded at 57 days when the wasp fed on the CBB larvae. Nourishment had a
significant effect on the survival of P. nasuta. Female wasps fed on CBB larvae
had significantly greater survivorship ( p < 0.0001) than in all other conditions
tested (Table 2). There was no significant difference ( p > 0.05) in the longevity
of wasps in treatments with pupae and eggs, or for the three treatments of
honey, CBB adults and control. P. nasuta was observed to feed on all immature
stages of the borer. After feeding on eggs, only the chorion can be seen.
Feeding on pupae occurs mainly in the dorso-abdominal region and on larvae
in any region, except the head. Most adult borers exposed to the wasp were
killed but feeding on them was not observed.

Table 1. Development in days (mean ± SE) for males and females of the parasitoid
Prorops nasuta under alternating temperatures
Stage Males (n = 14) Females (n = 102)
Eggs incubation 2.4 ± 0.14a 2.80 ± 05b
Larvae feeding on its host 4.3 ± 0.16a 4.6 ± 0.07a
Larvae constructing cocoon 4.1 ± 0.26a 3.8 ± 0.11a
Cocoon 16.9 ± 0.46a 18.7 ± 0.15b
Total 27.7 ± 0.37a 30 ± 0.12b
Means for males and females followed by the same letter within a row are not
significantly different (t-test; p < 0.05).
 LIFE HISTORY STUDIES OF PROROPS NASUTA 265

0.9

0.8

0.7

Eggs
Survivorship

0.6
Larvae
Pupae
0.5
Adults
Honey
0.4
Water
Control
0.3

0.2

0.1

0
0 5 10 15 20 25 30 35 40 45 50 55
Days

Figure 2. Survivorship of adult females of Prorops nasuta under different diets as food.

Discussion

Since the introduction of P. nasuta to Mexico several thousand batches of wasp

cultures have been made and this parasitoid has been reared uninterruptedly in
this country since the end of 1992. The culturing practices developed for
P. nasuta have been successful and in 10 years, more than 3 million individuals
were produced in the laboratory. The wasps’ production depends largely on the

Table 2. Log-Rank Statistics and (significance) for the survival data illustrated in
Figure 2, determined by Kaplan Meier Survival Analysis with Log-Rank Comparisons
(SPSS for Windows 10.0, SPPS Inc., 1999)
Factor Adults Control Eggs Honey Larvae Pupae
Control 0.44
(0.508)
Eggs 19.29 18.41
(0.000) (0.000)
Honey 0.04 1.10 20.67
(0.848) (0.293) (0.000)
Larvae 33.34 33.76 24.56 30.87
(0.000) (0.000) (0.000) (0.000)
Pupae 12.70 11.37 0.15 14.32 12.87
(0.000) (0.000) (0.700) (0.000) (0.000)
Water 11.20 10.08 9.34 18.26 32.53 3.94
(0.000) (0.001) (0.002) (0.000) (0.000) (0.047)
266 FRANCISCO INFANTE ET AL.

availability of infested coffee berries in the field, and the greatest levels are
typically reached from January to April each year. Adult parasitoids began
emerging 30.6 days (±0.28 SE) after the culture was established and reached
peak production at 36 days, after which production declined. Males normally
emerged from coffee berries 2–3 days before females. Males emerged in the
mornings, usually from 07:00 to 09:00 h and females from 10:00 to 14:00 h. De
Toledo (1942) observed that parasitoid emergence was rare on cloudy days,
which was confirmed in this study, even in the presence of intensive artificial
light.
Under this rearing system the offspring production of P. nasuta was higher
than those obtained by Portilla and Bustillo (1995) who reported 3.7 offspring
per wasp. In Ecuador, Klein-Koch et al. (1988) reported an initial yield of 3.2
wasps per coffee berry, which was improved months later up to 15.9 parasi-
toids, when wasps were offered highly infested coffee berries. With some var-
iation the rearing system used for P. nasuta is similar to those used by
Abraham et al. (1990) and Barrera et al. (1991).
Hempel (1934) was the first to note that adult females of P. nasuta place the
dead borers in the hole of the coffee berry to block the entrance, and that
behaviour was confirmed in this study. Remaining with its brood inside the
berry is a sub-social behaviour and occurs in other species of Bethylidae
(Evans, 1964). Hardy and Blackburn (1991) indicated that the cost of
remaining inside seemed at least partially offset by the prevention of oviposi-
tion by competing parasitoids.
It was observed that P. nasuta females gradually lose the ability to oviposit
precisely. Old females (over 20 days) often placed eggs in a poor position on
both larval and pupal hosts, where the future larva could not feed (head,
thorax, etc.), and consequently they died. In some cases eggs were laid that
were not in contact with hosts, and these were unable to parasitize a host
successfully. At more advanced ages, ovipositing females were observed to miss
the host altogether.
Waterhouse and Norris (1989) and Murphy and Rangi (1991) stated that
P. nasuta larvae usually feed on more than one host larva. In this study, several
hundred larval developments were observed, and none of them was found
consuming more than one host. On the contrary, it was found that if the larvae
became detached from its host it died from starvation, because its limited
movements prevented it from reaching another host. Fully developed larvae
are more capable of motion but despite this, they did not feed on a second host.
There are some differences between our data and previous studies of
development and preoviposition times for P. nasuta. However, these figures
cannot be compared directly, as the studies were carried out under different
conditions. For instance, in the field, Hargreaves (1926) found a 17 day pre-
oviposition period, while De Toledo (1942) reported a range of 8–24 days
 LIFE HISTORY STUDIES OF PROROPS NASUTA 267

(average 18 days) when females are fertilised, and 8–39 days for virgins.
Abraham et al. (1990) reported 13.8 days under laboratory conditions. Harg-
reaves (1926) recorded an average of 27.0 days for egg to adult development
time in field conditions. De Toledo (1942) reported 23.0 days for egg to adult
development at 24 C and Abraham et al. (1990) observed 22.4 days at 25 C.
In other observations Infante (1998) observed that egg to adult development
took 18 days at a constant 27 C and 16 at a constant 30 C, although survival
was lower at the higher temperature.
The results obtained on the sex-ratio of P. nasuta are similar to those of De
Toledo (1942) and Klein-Koch et al. (1988) who reported a male proportion of
0.25 and 0.17, respectively. The wasp apparently has the ability to regulate the
sex of its progeny, but it is not yet understood how this species determines the
proportion of the sexes. According to Mayhew and Godfray (1997) and Hardy
and Mayhew (1998) the sex allocation of Bethylids is related to the clutch size
(higher proportion of males in smaller clutches, reducing mate competition in
larger clutches while ensuring male occurrence within smaller clutches) and
host quality (larger hosts have a lower proportion of males; they may also, of
course, support larger clutches of eggs). In H. hampei the sex ratio (male
proportion) is 0.09, and female larvae are almost double the length of male
larvae (Bergamin, 1943). As the sex-ratio of P. nasuta found in this study was
0.21, most parasitoid male eggs should have been laid on female hosts. If so,
that would mean that the host size in this species is not important for the sex
allocation. On the other hand, it will be important to determine the primary
sex-ratio, because it is possible that mortality rates in immature males and
females parasitoid might be different. The reproduction of virgin females ob-
served is consistent with the reports in earlier studies in which this species is
mentioned to have arrhenotokous parthenogenesis (Hargreaves, 1926; Hempel,
1934; De Toledo, 1942).
During this study feeding by the adult females of P. nasuta on honey or
CBB adults was not seen. It cannot be stated that this does not occur, as
individuals were only observed for a short time (1 h approximately) daily.
Nevertheless, as there was no difference between these treatments and the
control, we assumed that females do not feed on these diets, or if they do, they
do not benefit from it. These results thus agree with those of Murphy and
Rangi (1991) who gave figures of wasp survival of 2, 2 and 3 days in treatments
with no food, CBB adults + pupae, and honey, respectively. According to
Damon et al. (1999) the survival of P. nasuta females neither showed a positive
effect when individuals were feeding on honey. To our knowledge this is the
second case of a bethylid parasitoid not benefiting from honey feeding, in
addition to Goniozus nephantidis (Hardy et al., 1992). It seems that other kind
of sugars promote the longevity in this species, since P. nasuta adults lived
significantly longer if they fed on saccharose and nectar of the plant Euphorbia
268 FRANCISCO INFANTE ET AL.

hirta L. [(Euphorbiacea), which contained saccharose, glucose and dextrose], a

common weed growing in coffee plantations (Damon et al., 1999).
Although nutrients gained from host feeding are converted into oocytes in
many species of parasiotids (Heimpel and Collier, 1996), the increased lon-
gevity of P. nasuta females fed on immature stages of CBB revealed that
nutrients obtained by host feeding are also used for somatic maintenance
(Jervis and Kidd, 1986; Collier, 1995). Parasitoids that were given immature
stages of CBB as a food lived from two to ten times longer with respect to the
control, especially when feeding was on CBB larvae. It is well known that host
feeding alone can promote the survival of many species of parasitoids (Heimpel
and Collier, 1996; Jervis et al., 1996; Jervis and Kidd, 1999), but in other
species the interaction between host feeding and honey feeding, it is crucial to
increase the fecundity and longevity of parasitoid females (Heimpel et al.,
1997). Further experiments involving combinations of sugar rich foods and
immature stages of the CBB are necessarily to understand the feeding behav-
iour and nutritional ecology of P. nasuta females.
The studies on the life history of P. nasuta presented in this paper provide
valuable information, which can help to achieve more efficient use of this
parasitoid for the biological control of CBB. P. nasuta has a record of poor
field establishment that may be helped by releasing larger numbers from
rearing facilities with conditions optimised on the basis of these observations.

Acknowledgements

We express our sincere thanks to J.L. Barrera and Giber Gonzalez for technical
assistance and Tilly Collins, Sam Elliot and Ian Hardy for comments on an earlier
draft of this paper.

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