We studied the morphology of the ovipositor of Platygaster diplosisae (Hymenoptera: Platygasteridae) and Aprostocetus procerae (= Tetrastichus pachydiplosisae) (Hymenoptera: Eulophidae), two parasitoids associated with the African rice gall midge (AFRGM), and Orseolia oryzivora (Diptera: Cecidomyiidae). Scanning electron microscope techniques were used for this study. The ovipositor of P. diplosisae was short (40 μm), and most of the sensillae found on it were mechanoreceptors and located on the distal portion of the 3rd valvulae. These sensillae may be involved in selection of an egg or larval host. The shortness of this ovipositor may be an adaptation to a host whose egg envelope thickness is not more than 0.7 μm. The ovipositor of A. procerae was 30 times (1.2 mm) the length of the P. diplosisae ovipositor. It was not only well equipped with mechanoreceptive sensillae, but these sensillae were very diverse and distributed along the length of the valvulae. The 10 denticulations of the lancet of this ovipositor allow this parasitoid to exploit hosts that are not otherwise readily accesible. These two parasitoids share the same resource by infesting different life stages of the host. The ovipositor of each species of parasitoid enhanced resource sharing, due to its length and its sensillae type and distribution.
1. Introduction
The African rice gall midge (AfRGM), Orseolia oryzivora Harris & Gagné (Diptera:
Cecidomyiidae), is an insect pest indigenous to Africa.
It was considered a minor pest prior to the 1970s but has since caused
increasingly severe damage to rice crops [1].
The young larva feeds on tillers at the growing point of the rice plant and induces the
plant to form an oval, hollow gall. Each gall prevents production of a panicle.
The amount of yield loss caused by the gall midge larva varies among rice
varieties. Nacro et al. [2], and Williams et al. [3] showed that an increase in 1% in the percentage of tillers with galls at the stem-elongation stage reduced
yield by 2 to 3%.
It has been reported that early and synchronized plantings of rice reduce
the damage by the AfRGM [1]. Unfortunately, these cultural control methods are
very often insufficient because of problems with water management and the
conflicting management of both upland cereal crops and irrigated rice. The use
of insecticides to control AfRGM is not ideal because of the cost, the risk to
human health and the environment, and the destruction of natural enemies [4]. Furthermore,
only systemic insecticides are likely to be effective in the control of the
midge because of its feeding habit inside plant tissue. The conservation of natural
enemies of the AfRGM may be a good alternative to insecticidal control.
So far, little is known about the predators of AfRGM. Some egg predators
have been reported [1]. These include tiny predatory mites (Neoseiulus sp., Phytoseiidae), the bug Cyrtorhinus viridis Linnavuori (Miridae),
and the sword-tailed crickets Anexipha longipennis Serville, and Trigonidium cicindeloides Rambur (Gryllidae). Ladybird beetles (Coccinellidae) and the long-horned grasshopper Conocephalus (Tettigoniidae) are also egg predators. Two common parasitoids are known to be associated with the AfRGM. These are Platygaster diplosisae Risbec (Hymenoptera: Platygastridae) and Aprostocetus procerae Risbec (=Tetrastichus pachydiplosisae) (Hymenoptera: Eulophidae). These two parasitoids are the primary biological
control agents. P. diplosisae is a gregarious larval parasitoid whereas A. procerae is a solitary pupal parasitoid of the AfRGM [5]. P. diplosisae oviposits inside the eggs or
the larvae of AfRGM. The parasitoid’s larvae hatch inside the young AfRGM
larva. They feed inside the larva and kill it when it is fully grown. They then
pupate inside the corpse, from which the adults emerge. The adults cut one or
more very small exit holes in the gall and disperse. The adult A. procerae lays its eggs onto AfRGM
pupae, or occasionally onto large larvae. It does this by piercing through the
wall of the gall with the tip of its abdomen. The host is stung and paralyzed
by the female parasitoid as the egg is laid. A. procerae feeds on, rather than inside, the host, and only one
larva develops on each host. After it has finished feeding, the parasitoid
larva changes into a pupa inside the gall. The adult that emerges cuts an exit
hole in the gall to escape. Cumulative parasitism due to these two hymenopterans
has been reported to reach 77% [6–9]. However, sometimes, such a high level of parasitism occurs too late to
prevent damage by the pest.
The ovipositor of parasitic hymenopterans is primarily used to deposit an
egg into or onto a host [9]. The structure of the ovipositor in different
species of parasitic hymenoptera varies both in length and in its arrangement on
the terminal metasomal segments. The general organization of the ovipositor
includes 3-paired valvulae (1, 2, and 3), one paired valvifers. The paired 1st valvulae and the 2nd paired valvulae are fused in their distal portion
to form the lancet, which is the piercing organ.
This study compares the ovipositor of A. procerae and P. diplosisae in terms of
morphology and function of the associated sensillae. Furthermore, we hypothesize
about the possible effect of the sensillae richness and diversity on the
parasitism rate of A. procerae and P. diplosisae.
2. Material and Methods
Adult parasitoids were captured
from irrigated rice fields in Burkina Faso and kept in a 90% alcohol solution and sent to France
where all the laboratory
work was completed. The average age of the specimen was 7. We used about 100
individuals of each parasitoid species in 5 replicates. Unfortunately, due to
the smallness of the ovipositor of P.
diplosisae only a few samples were observed under electron microscope. Ovipositors
of A. procerae and P. diplosisae were dehydrated in
successive alcohol solutions (70%, 80%, 95%, and 100%) and acetone solutions
(50%, 70%, 90%, and 100%). Ovipositors were then mounted on a lead
object-holder. Samples were critical point dried in a Balzers CPD 010 apparatus
with liquid CO2 gas and then
gold palladium coated with a JEOL JFC-100 sputter. These samples were observed
under a JSM 6400 electron-scanning microscope (JEOL Ltd, Japan).
3. Results3.1. Description of the Ovipositor of Platygaster diplosisae
The ovipositor of P. diplosisae measures 40 μm in length (Figure 1(a)).
Ovipositor
of P. diplosisae. (a) View of the abdomen showing the ovipositor at its distal
end. abd: abdomen. (b) Front view of the ovipositor of P. diplosisae. Several sensillae are seen on the 3rd valvulae. a: trichoid sensillum of type
a; b: trichoid sensillum of type b; c: sensillum of type c; d: sensillum of
type d. (c) Valves 3 showing 2 types of trichoid sensillae. a:
sensillum of type a; b: sensillum of type b. (d) Distal end of the 3rd valvulae with 2 types of
trichoid sensillae. c: sensillae of type c; d: sensillae of type d. (e) Two campaniform sensillae located at the proximal portion
of the 3rd valvulae. v3: 3rd valvula; sc: campaniform
sensillum. (f) Sensillum of type d observed on the distal end of the 3rd valvula. d: sensillum of type d. (g) Distal end of the ventral part of a 2nd valvula viewed in profile. Five denticles are seen on this valvula. v2: 2nd valvula. (h) 1st valvula of the ovipositor. They appear
large in their proximal portion and more and more slender near their distal
end. v1: 1st valvula. (i) Two campaniform sensillae on the proximal portion of a 1st valvula. v1: 1st valvula.
3.1.1. 3rd Valvulae
The paired 3rd valvulae are 40 μm in length and protect the 1st and 2nd valvulae when the ovipositor is at rest (Figure 1(a); see
arrow). 3rd valvulae are connected distally, which causes a cone
that has a slightly flat peak (Figure 1(b)).
3.1.2. 1st and 2nd Valvulae
The two pairs of 1st and 2nd valvulae are fused and
form the ovipositor stylet (Figure 1(g)).
At rest, this ovipositor stylet is entirely embedded in the cavity of the
3rd valvulae (Figure 1(b)). The paired valvulae are larger in their
proximal portion and come to a sharp point distally (Figure 1(h)). The extremity
of the paired 2nd valvulae, also called the lancet, is equipped with
five denticles (Figure 1(g); see arrow).
3.2. Sensillae on the Ovipositor of P. diplosisae
The sensillae on the ovipositor are relatively simple.
3.2.1. 3rd Valvulae
Two-thirds of these sensillae are campaniform sensillae whose external process is a dome embedded in a cuticular
depression (Figure 1(e)). The distal 1/3 of the 3rd valvulae possesses
four types of sensillae (Figures 1(b), 1(f)). Following is a list and description of the four sensillae types:
3 trichoid sensillae of type a, nonaligned. They are
slightly curved and measure 12 μm in length.
1 trichoid sensillum of type b, slightly straighter
than the other three but as long as them (13 μm length) (Figures 1(b), 1(c)).
1 unique sensillum of type c, 3 μm in length, so 4
times shorter than the trichoid sensillae described early (Figures 1(b), 1(d)). Unlike
the trichoid sensillae, the base of the type c sensillum is not embedded
in a cuticular depression. Its diameter is more continuous and its
extremity is less sharp.
1 unique sensillum of type d, located near the
sensillum of the type c (Figures 1(b), 1(d), 1(f)). It measures 2.5 μm. The base is
embedded in a depression similar to the trichoid sensillum. It is grooved
and its extremity ends with a bludgeon.
It measures 2.5 μm in length. This type of sensillum resembles the
chaetica of type 1 observed by Van
Baaren [10], on the antenna of Epidinocarsis lopezi (de
Santis) (Hymenoptera: Encyrtidae) a solitary endoparasitoid of the cassava
mealybug, Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae). The extremity of this sensillum which
was not explored by scanning electron microscopy could bear a pore. The
trichoid sensillae, the campaniform sensillae and the sensillum of type c may
be mechanoreceptors.
3.2.2. 1st and 2nd Valvulae
The 1st paired valvulae
are equipped with campaniform sensillae aligned on a line that runs the length
of the valvulae (Figure 1(i)). These sensillae are the same type as those
observed on the distal two thirds of the 3rd valvulae. These are
mechanoreceptive sensillae similar to those described on the ovipositor
valvulae of several hymenopteran parasitoids [11].
The size and the low number of ovipositors examined
did not allow us to determine whether the 2nd valvulae are equipped
with sensillae.
Table 1 summarizes the different
types of sensillae and their possible function.
Distribution of the sensillae on the ovipositor of P. diplosisae.
Type
Localization
Number
Length(μm)
Existence of an apical pore
Possible function
Campaniform mechanoreceptors
2/3 proximal of 3rd valvulae
—
—
—
—
Mechanoreceptors
Entire length of 1st valvulae 3rd valvulae
—
—
—
—
Trichoid a
1/3 distal
3
12
No
Mechanoreceptors
Trichoid b
Distal extremity of 3rd valvulae
1
13
No
Mechanoreceptors
c
Distal extremity of 3rd valvulae
1
3
No
Mechanoreceptors
d
Distal extremity of 3rd valvulae
1
2.5
Not sure
Chemoreceptors
3.3. Description of the Ovipositor of A. procerae
The ovipositor of A. procerae consists of a stylet
surrounded by the paired 3rd valvulae (Figure 2(a)).
Ovipositor of A. procerae. (a) Extremity of the abdomen of A. procerae showing the valvulae at the distal end of the stylet.
ts1: trichoid sensillum of type 1. (b) External surface of the distal end of a 3rd valvula bearing several types of trichoid sensillae; ts2: trichoid sensillum of
type 2; ts3: trichoid sensillum of type 3. (c) Extremity of a 3rd valvula showing 3 sensillae
of type 3. a: sensillum of type a. (d) Internal surface of the distal end of a 3rd valvula, viewed in profile. The interior of the valvula is empty. A trichoid
sensillum of type 4 is seen. ts4: trichoid sensillum of type 4. (e) Distal extremity of the stylet of the ovipositor viewed
in profile. The 2nd valvulae are carried by the 1st valvulae. v2: 2nd valvula; cs: campaniform sensillum. (f) Distal end of the dorsal surface of a 2nd valvula showing 10 denticulations making a united lancet. d: denticulation. (g) Styloconic sensillum of type 3 on the external surface of
the proximal part of a valve 2. ss3: styloconic sensillum of type 3. (h) Distal extremity of the ventral part of the stylet of the
ovipositor viewed in front. v1: valve 1; a: campaniform sensillum of type a. (i) Sensillum of type b located on the half proximal part of
the external surface of a valve 1. b: sensillum of type b. (j) Sensillum of type c located on the half proximal part of
the external surface of a valve 1. c: sensillum of type c. (k) Sensillum of type d, observed on the external surface of
the proximal part of a valve 1. d: sensillum of type d. (l) Sensillum of type e, located at 120 μm of the distal
extremity of a valve 1. e: sensillum of type e. (m) External surface of the distal extremity of a valve 1.
The three sensillae of type f are distributed in triangle. f: sensillum of type
f. (n) Sensillum of type g located at the half proximal part on
the external surface of a valve 1. g: sensillum of type g. (o) Campaniform sensillum located at the 2/3 proximal of the
a valve 1. cs: campaniform sensillum. (p) Three rows of styloconic sensillae of type 1 and 2 on the
external surface of the distal extremity of a valve 3. ss1: styloconic sensillum
of type 1; ss2: styloconic sensillum of type 2.
3.3.1. 3rd Valvulae
These
valvulae are largest proximally, but slightly sharp distally (Figure 2(b)). The internal
surface of the 3rd valvulae has many cuticular spines (Figure 2(d);
see arrow).
3.3.2. 1st and 2nd Valvulae
The ovipositor stylet of A. procerae is 1.2 mm in length,
surrounded by the paired 3rd valvulae. The paired 2nd valvulae
are coupled by the 1st valvulae. A sliding system allows the lancet
formed by the fusion of the paired 2nd valvulae to move backward and
forward. The lancet bears a notch that limits the movements of the paired 2nd and 1st valvulae. This lancet is 92 μm long and bears 10 denticles on its external surface (Figures 2(e), 2(f)).
These denticles are increasingly smaller from proximal to distal, which gives the
perforating system of the ovipositor its sharp form.
3.4. Sensillae on the Ovipositor of A. procerae
The paired 3rd valvulae bear four
types of sensillae, three of which are trichoid sensillae.
Type 1: a long trichoid sensillum, 104 μm in length. It is located proximally
(Figure 2(a)).
Type 2: this type of trichoid sensillum is the most common on the paired
3rd valvulae. These sensillae are nearly straight, 51 μm in length and
distributed on the 3rd paired valvulae up to 58 μm from the base. They
appear smooth when observed under the scanning electron microscope (Figure 2(b)).
Type 3: these are trichoid sensillae, 38 μm in length, curved and
observed from 42 μm distally on the 3rd paired valvulae where 6
sensillae of this type are observed. They are channeled and slightly rounded distally
(Figures 2(b), 2(c)).
Type A: this unique sensillum is observed at the proximal end of the 3rd paired valvulae. It is 5.3 μm in length and originates from a depression. It is
slightly curved and half of its proximal part is sharper than its basal part. This
styloconic sensillum is the shortest sensillum of all sensillae observed on the
3rd paired valvulae (Figure 2(c)).
3.4.1. 1st Paired Valvulae
The 1st paired valvulae
are very rich in sensillae. Eight types of sensillae were observed on these
valvulae.
Type b: the external process is located in a large groove. This type of
sensillum is located in the proximal half of the 1st paired valvulae.
It is basiconic (Figure 2(i)).
Type c: basiconic sensillum has a large groove. The external process is prominent,
almost perpendicular to the axis of the valvula (Figure 2(j)).
Type d: styloconic
sensillum, unique, with an appearance similar to a trichoid sensillum. It is
located basally and is 4.7 μm in
length (Figure 2(k)).
Type e: a basiconic sensillum. Five sensillae of this type are arranged randomly,
and the last one is located at 120 μm distally from the base of the valvula
(Figure 2(l)).
Type f: 3 sensillae arranged
in a triangle at the distal portion of the valvulae (Figure 2(m)). The external process is short. In
their morphology and distribution, these sensillae look like the sensilla
observed by Le Ralec [11] on the 1st paired valvulae of Encarsia
formosa Gahen (Hymenoptera: Aphilinidae), larval parasitoid of the greenhouse
Aleyrodid Trialeurodes vaporariorum Westwood (Homoptera:
Aleyrididae).
Type g: the process
is stretched and embedded in a depression (Figure 2(n)).
Campaniform sensillum: the external process is a dome. This
sensillum is located on the basal 2/3 of the valvulae. Its diameter is 2 μm (Figure 2(o)).
Styloconic sensillae of type 1 and type 2: one row of type 2 is enclosed
by two rows of type 1. Type one has an external process that is entirely
embedded in a depression. Three rows of styloconic sensillae are distributed on
the external surface of the basic portion of the valvulae. They are 0.7 μm in
length (Figure 2(p)).
3.4.2. 2nd Paired Valvulae
The sensillae on the paired 2nd valvulae are less abundant than those of the paired 1st valvulae.
They include
styloconic sensillae of type 3. Three of these
sensillae are observed on the basal external surface of the valvulae. Their
external process is more developed than that observed on the other types of
styloconic sensillae. This
process appears erect and oblique as compared to the axis of the valvula. The
sensillum is embedded in a narrow depression. Its external process is 0.7 μm in
length (Figure 2(g));
sensillae of type g:
they are located on the distal half of the valvula but are not illustrated.
The distribution of the sensillae
on the valvulae of the ovipositor of A.procerae and their possible
functions are summarized in the Table 2. The sensillae of the
ovipositor of this eulophid are as abundant as diverse and probably mainly function
as mechanoreceptors. The main biological features of the host (O. oryzivora) and its two parasitoids
are presented in Table 3.
Distribution of the sensillae on the ovipositor of A. procerae.
Type
Localization (μm)
Number
Extremity
Length
Existence of an apical pore
Probable function
Trichoid 1
Proximal portion of 3rd valvula
1
Sharp
104
No
Mechanoreceptor
Trichoid 2
58 μm from distal extremity of 3rd valvula
The most common of the trichoid type
Slightly sharp
51
No
Mechanoreceptor
Trichoid 3
42 μm from the distal extremity of 3rd valvula
—
Slightly rounded
38
No
Mechanoreceptor
Type a
Distal extremity of 3rd valvula
1
Rounded
5.3
No
Mechanoreceptor
Type b
Distal of 1st valvula
Few
Rounded
0.9
No
Mechanoreceptor
Type c
Half proximal of 1st valvula
Few
Rounded
0.8
No
Mechanoreceptor
Type d
Proximal portion of 1st valvula
1
Rounded
0.47
No
Mechanoreceptor
Type e
120 μm from the distal extrimity
of 1st valvula
Type f
5 μm from the distal extremity of 1st valvula 3
3
Slightly rounded
0.4
Probable
Chemoreceptor
Type
g
Half proximal of 1st valvula
—
—
—
—
—
Campaniform
2/3 proximal of 1st valvula
—
Rounded
2
—
Mechanoreceptor
Styloconic
1
Proximal portion of 1st valvula
—
Rounded
0.7
No
Mechanoreceptor
Styloconic 2
Proximal portion of 1st valvula
—
Rounded
0.7
No
Mechanoreceptor
Styloconic
3
Proximal part, interior surface of 2nd valvulae
3
Slightly sharp
0.7
No
Mechanoreceptor
Main biological features of O. oryzivora (host), Platygaster diplosisae, and Aprostocetus procerae (parasitoids). (According to Nacro and Nénon, 2006.)
Nature
Average
potential fecundity
Average fertility
Eggs’ envelopes thickness
Length of the ovipositor
Distribution
of the sensorial organs on the ovipositor
Nature of the parasitism
O. oryzivora
host
High (300 eggs)
Medium (35.6)
Thin (0.7 μm)
—
—
—
P.
diplosisae
parasitoid
Very high
Not assessed
Very thin
40 μm
Mainly distributed on the
distal portion of valve 3 Mechanoreceptors and chemioreceptors
Gregarious endoparasitism of the egg or L1 of the host
A. procerae
parasitoid
Low
Not assessed
Thin
1.2 μm
well distributed on the different parts of the ovipositor Mechanoreceptors and chemioreceptors
Solitary ectoparasitism of the pupae of the host
4. Discussion
Table 3 explains the main biological features of
the host and its associated parasitoids. The reproductive biology of hymenopterans
has been used to explain the nature of their parasitism. Price [12]
showed that larval parasitoids of the wood fly, Neodiprion swainei, had a high fecundity and were gregarious. Their
hosts were relatively abundant and easy to find. In contrast, the pupal
parasitoids of the fly were ectoparasitoids with low fecundity. We are in a
similar situation, where P. diplosisae and A. procerae share the same
host at its different developmental stages due to the adaptations of their
reproductive biology.
The ovipositor plays an
essential role in the success of parasitism in Hymenoptera. Le Ralec [11], showed adaptive
morphological features, according to the type of hosts, in 22 parasitoid hymenopteran
species. These features are related
not only to the morphology of the ovipositor (length and width of the diameter)
but also to the quantity, the quality, and the way the sensillae are distributed
on it. Thus, the species that easily access their hosts have ovipositors well
equipped with mechanoreceptive sensillae spread along the length of the valvulae.
The species that have difficulty accessing their hosts have poorly equipped
ovipositors with mechanoreceptive sensillae that are generally grouped at the distal
end of the valvulae. The case of these two parasitoid species associated with O.
oryzivora is consistent with what was stated above.
Indeed, we have already observed
that most of the sensillae found on the ovipositor of P. diplosisae are
mechanoreceptors located essentially at the extremity of the 3rd valvulae.
These sensillae may be important for host selection, which for this parasitoid is
either an egg or a larva. So, these sensillae could “inform” the parasitoid on
the status of the surface of the host. The sensillae of type B, observed at the
extremity of the 3rd valvulae, probably of chemoreceptor type, could
“inform” the parasitoid on the interior status (parasitized or unparasitized)
of the host. Lastly, the short length of the ovipositor (40 μm) seems an
adaptation to this type of host where the thickness of the egg envelope is not
more than 0.7 μm.
The ovipositor of A. procerae is not only well equipped with
mechanoreceptive sensillae, but these sensillae are diverse and distributed
along the length of the valvulae. In addition to these features, the length of
the stylet of the ovipositor (1.2 mm) is 30 times the length of the ovipositor
of P. diplosisae, and the 10 denticulations of the lancet meet the conditions
of a parasitoid that exploits a host that is less accessible. As for P. diplosisae,
the very abundant mechanoreceptive sensillae observed at the distal end of the paired
3rd valvulae could be used by A. procerae to detect the substrate within which the host is located and to determine
the depth at which it is located. The three chemoreceptive sensillae of type F observed
at the distal end of the paired 1st valvulae could “inform” the
parasitoid on the depth and the condition of the host. The length of the
ovipositor has already been recognized as an adaptive feature for several
parasitoids that exploit the same host, Tryporyza incertulas Walker,
a lepidoperan rice stemborer whose egg masses have different layers [13]. The
two parasitoid species examined share the same resource by infesting different
stages of the host and by the ovipositor of each species differing in length and
associated sensillae. In fact, the parasitic action of the two parasitoids may be
complimentary.
The role of the two examined parasitoids
in the natural regulation of the AfRGM has already been investigated by several
authors [1, 4–7]. These parasitoids parasitize the midge
simultaneously, and they can find and kill up to 70% of the immature
populations of the pest. However, sometimes, such a high level of parasitism
occurs too late in the season to prevent large AfRGM populations from building
up and causing serious yield losses. The role of these parasitoids could be
integrated into an Integrated Pest Management (IPM) strategy that could include
also cultural control (early and synchronized planting, management of
alternative hosts and fertilizer), host plant resistance, and chemical control.
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