Reproductive Traits of Ontsira mellipes (Hymenoptera: Braconidae), a North American Parasitoid, as a Novel Biological Control Agent for Exotic ...
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Journal of Economic Entomology, XX(XX), 2020, 1–8
doi: 10.1093/jee/toaa160
Biological and Microbial Control Research
Reproductive Traits of Ontsira mellipes (Hymenoptera:
Braconidae), a North American Parasitoid, as a Novel
Biological Control Agent for Exotic Anoplophora
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glabripennis (Coleoptera: Cerambycidae)
Xingeng Wang1 and Ellen M. Aparicio
Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, 501 S. Chapel Street,
Newark, DE 19713 and 1Corresponding author; e-mail: xingeng.wang@usda.gov
Subject Editor: Julio Bernal
Received 13 April 2020; Editorial decision 30 June 2020
Abstract
Ontsira mellipes Ashmead is a gregarious larval ectoparasitoid of woodboring cerambycids that is native to North
America but can readily attack the exotic Asian longhorned beetle, Anoplophora glabripennis (Motschulsky).
To evaluate the potential of the parasitoid as a novel association control agent for the pest beetle, this study
investigated some key reproductive traits of the parasitoid, including egg maturation dynamics, and host size
preference and suitability in association with the beetle. Results showed that female wasps emerged with a
substantial portion (38%) of their lifetime complement of mature eggs and matured eggs rapidly, reaching a
peak 4–6 d post-eclosion. The number of mature eggs was positively related to the female wasp’s body size.
Oviposition prompted production of more mature eggs by young female wasps. The parasitoid did not show a
significant preference for large over small hosts in a choice test. Host size did not affect the parasitoid’s offspring
survival, developmental time, or sex ratio. However, clutch size increased with increasing host size. Female
wasps that developed from large hosts had larger body size and consequently a higher mature egg load than
those reared from small hosts. Neither longevity nor the total number of parasitized hosts over a female’s life-
time was affected by the female’s size, but the total number of offspring produced per female increased with
the female’s size. These results have important implications for improving rearing and field-release strategies
as well as understanding the ecological mechanisms underlying host size selection in gregarious parasitoids.
Key words: biological control, body size, clutch size, egg maturation, host size
A novel host–parasitoid association could occur from ecological and Native to China and the Korean peninsula, the Asian longhorned
physiological similarity between a parasitoid’s ancestral and novel beetle, Anoplophora glabripennis (Motschulsky), is a serious inva-
hosts in the aftermath of pest invasion or biological control intro- sive pest worldwide (Haack et al. 2010). Populations of the beetle
duction (Hokkanen and Pimentel 1989, Wiedenmann and Smith have been reported since 1996 in the United States, 2001 in Europe,
1997, Heimpel and Mills 2017). In the case of invasion of exotic and 2003 in Ontario, Canada (Haack et al. 2010, Meng et al. 2015).
pests, such novel host–parasitoid interactions may be considered as Although the beetle’s populations have been successively eradicated
options for biological control of the invasive pests (Symondson et al. in 10 European countries, two U.S. states (Illinois and New Jessy)
2002, Wang et al. 2012, Heimpel and Mills 2017). Although the em- and Canada, active invasive populations are still present across
phasis on biological control of exotic pests has focused toward the Europe (Javal et al. 2019), and in Massachusetts, Ohio, and New
introduction of coevolved and specialist parasitoids because they can York in the United States (APHIS 2020). Anoplophora glabripennis
more specifically and efficiently attack targeting hosts (Kimberling attacks various hardwood trees such as maples, poplars, willows and
2004, Heimpel and Mills 2017), parasitoids native to the introduced elms, and may threaten 30–35% of the trees in urban areas of the
ranges of exotic pests should also be explored for their potential to eastern United States (Haack et al. 2010, Meng et al. 2015). The
add to the management of exotic pests, especially when there may economic, ecological, and aesthetic impacts on the United States
be a lack of coevolved and specialist natural enemies in the pests’ would be devastating if the beetle continues to spread; potential
home range. losses have been estimated in the tens to hundreds of billions of
Published by Oxford University Press on behalf of Entomological Society of America 2020. This work is written by (a) US Government employee(s) and is in the 1
public domain in the US.2 Journal of Economic Entomology, 2020, Vol. XX, No. XX
U.S. dollars (Nowak et al. 2001). Considering the continuous threat over 20 native idiobiont North American parasitoids have been
of re-establishment of this exotic pest in North America, sustainable found to parasitize larvae of the exotic emerald ash borer Agrilus
and area-wide management strategies need to be developed should planipennis Fairmare throughout different geographical areas, with
eradication and containment measures fail. Biological control, es- reported level of parasitism up to 40% (Cappaert and McCullough
pecially using parasitoids, could be a valuable option for reducing 2009; Duan et al. 2012, 2013; Roscoe et al. 2016).
established A. glabripennis populations in natural forests because Ontsira mellipes is a predominant parasitoid collected from
the beetle’s immature stage is hidden deep in the wood where in- cerambycid-infested hardwood trees during a recent survey in
secticide sprays may not penetrate, while parasitoids have developed Mid-Atlantic forests, although the field survey was unable to de-
morphological and behavioral adaptations to better cope with con- termine parasitoid–host relationships due to the concealed nature
cealed hosts in the wood (Quicke et al. 1998). Also, intensive use of of woodborers and their associated parasitoids (Golec et al. 2020).
insecticides may be prohibitively expensive and/or environmentally Some aspects of the parasitoid’s biology, including life history, larval
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undesirable. development, and fecundity, have been investigated (Duan et al. 2015;
In the native range of A. glabripennis in China, surveys for its Golec et al. 2016, 2017). Like other typical larval ectoparasitoids
natural enemies have identified two parasitoids, including a para- of woodborers, a female O. mellipes paralyzes the host larva prior
sitic beetle, Dastarcus helophoroides (Fairmaire) (Coleoptera: to laying a clutch of eggs on the surface of the host. At 23°C, the
Bothrideridae), attacking A. glabripennis larvae and/or pupae and parasitoid eggs hatch in 2–3 d, larvae develop in about 8–10 d and
a bethylid wasp, Scleroderma guani (Hymenoptera: Bethylidae), at- pupate by the consumed host, and adults emerge in about 10–15
tacking the beetle’s larvae (Smith et al. 2009, Liu et al. 2016, Gould d. Offspring of the parasitoid are female biased (85% female), and
et al. 2018, Rim et al. 2018). Although both parasitoids are very each female wasp can produce up to a mean of 6.8 female progeny
effective and have been mass-reared and released extensively against per A. glabripennis larva. Recent evaluations also showed that the
A. glabripennis in China, they are generalist ectoparasitoids attacking parasitoid’s parasitism on A. glabripennis increased with later gen-
many other woodboring beetle species, and thus not recommended erations (Golec et al. 2019). Host specificity testing in laboratory
for the management of A. glabripennis outside of Asia because of showed that O. mellipes could attack four of the six tested North
potential nontarget risks to woodboring beetle communities in the American cerambycid species, Elaphidion mucronatum (Say),
targeted region (Gould et al. 2018, Rim et al. 2018). Although efforts Monochamus carolinensis Olivier, Monochamus notatus (Drury),
are continuing toward the discovery and introduction of specialized and Neoclytus scutellaris Olivier, but could not attack Xylotrechus
A. glabripennis parasitoids in Asia for biological control in North colonus (Fabricius) and Xylotrechus sagittatus Germar). It did not
America, five North American parasitoid species are found to be show a preference between A. glabripennis and the four attacked
capable of forming novelassociations with A. glabripennis in la- North American host species, regardless of the host species on which
boratory tests: Ontsira mellipes Ashmead, Rhoptrocentrus piceus the tested parasitoids were reared, and the development and body
Marsh, Spathius laflammei Provancher, and two unidentified spe- size of females and offspring survival were similar when reared from
cies of Hesterospilus and Atanycolus (all Hymenoptera:Braconidae) A. glabripennis and M. carolinensis (Wang et al. 2019). However,
(Duan et al. 2015). Similarly, three native European hymenop- some key reproductive traits of the parasitoid are still unknown. As
teran parasitoids of woodborers, including one braconid, Spathius a part of the efforts to utilize this parasitoid as a novel control agent
erythrocephalus Wesmael, one pteromalid, Trigonoderus princeps for A. glabripennis, this study reports some key reproductive traits
Westwood, and one bethylid, Sclerodermus brevicornis (Kieffer), of this parasitoid, including egg maturation dynamics, host size pref-
readily parasitize A. glabripennis in Europe (Brabbs et al. 2015, Lupi erence, and effect of host size on offspring fitness. Such informa-
et al. 2017). All of them are idiobiont larval ectoparasitoids. tion could help improve mass-rearing techniques and field-release
More interestingly, recent surveys in mid-Atlantic forests re- methods and increase understanding of the ecological mechanisms
vealed that the majority of parasitoids emerged from field-collected underlying host size selection in gregarious parasitoids.
logs infested by cerambycids belonged to the subfamily Doryctinae
(Braconidae) (Golec et al. 2020), which consists predominately
of idiobiont and gregarious larval ectoparasitoids (Marsh 1997,
Materials and Methods
Belokobylskij et al. 2004, Kula and Marsh 2011, Golec et al. 2020).
The idiobiont and gregarious life-history strategy seems to evolve in Insects Culture
association with hosts that remain concealed during the immature All bioassays were conducted under controlled room conditions
stages and attack hosts such as A. glabripennis that are often much (23 ± 1.5°C, 45–60% RH, 16:8 [L:D] h) at the quarantine facility
larger than the parasitoids (Askew and Shaw 1986, Gauld 1988, of the USDA-ARS Beneficial Insects Introduction Research Unit in
Godfray 1994, Quicke 1997). Because idiobionts paralyze and ar- Newark, DE, where the laboratory colonies of A. glabripennis and
rest their hosts’ development after oviposition, the immature stages O. mellipes are also maintained and voucher specimens were depos-
of idiobionts would be vulnerable to attack by other competitors, ited. The A. glabripennis colony was established in 1999 from adults
predators, and hyperparasitoids, as well as to abiotic factors if they collected in Illinois, Massachusetts, New York, and New Jersey,
were in an exposed situation, and therefore, idiobionts are adapted United States. For the rearing of the beetle, branches of maple trees
to exploiting hosts in concealed environments such as woodborers (Acer spp.) were collected weekly from the Blackbird State Forest in
(Askew and Shaw 1986, Gauld 1988). The life-history characteris- Delaware and cut into 15- to 20-cm-long bolts. Adult females feed
tics of idiobiont ectoparasitoids may allow them to more successfully on bark and chew oviposition pits to insert their eggs between the
parasitize novel hosts because they typically do not need to circum- inner bark and the sap wood. The young larval beetles feed under the
vent internal host defenses (Askew and Shaw 1986, Quicke 1997, bark, and then bore into the wood with as they grow and develop
Mayhew and Blackburn 1999). Indeed, many woodboring insects (Meng et al. 2015). We used middle-sized bolts (2–5 cm diameter) as
are attacked by idiobiont ectoparasitoids (Hanks et al. 2001, Paine the oviposition medium and small twigs as food for the adult bee-
2017, Golec et al. 2020), and indigenous larval ectoparasitoids have tles. Each pair of adult beetles was fed weekly with 8–10 twigs and
been observed to adapt to novel exotic invasive hosts. For example, given one bolt for oviposition in a 3.47-liter glass jar. Exposed boltsJournal of Economic Entomology, 2020, Vol. XX, No. XX 3
were held until eggs had developed into larvae (≈ 4–8 wk). Bolts maximum extrusion were measured with an ocular micrometer
were then dissected, and the retrieved larvae were transferred into (nearest 0.001 mm) for each dissected female to serve as a proxy es-
28.3-ml plastic cups (SOLO Cup Co., Urbana, IL) for rearing indi- timate of their body size. After it was found that the mature egg load
vidually using a cellulose-based artificial diet as described by Dubois of female wasps could be related to the female’s body size, additional
et al. (2002). 2-d-old females with a range of different body sizes were dissected to
The O. mellipes colony was established in 2010 from wasps count mature egg load and their body sizes were measured. In total,
reared from red maple (Acer rubrum L.) logs naturally infested by 182 females at 2 d of age were dissected.
various cerambycids in the Blackbird State Forest and maintained To determine the possible effect of oviposition experience on egg
on A. glabripennis larvae (Duan et al. 2015). To maintain vigor, maturation in young females, each young (2 d old) female wasp was
additional wild O. mellipes were collected from the same forest in provided with one host bolt containing one A. glabripennis larva for
2011–2018 and added to the colony. For rearing of the parasitoid, 2 d. Following the 2-d exposure, each bolt was dissected to deter-
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middle-aged host larvae (500–800 mg, aged in 2–3 mo) were indi- mine whether the host larva was parasitized and the number of eggs
vidually inserted into maple bolts (1–2 cm diameter, 16 cm long) laid on the parasitized host. In total, 95 females with similar body
through a hole drilled in one end of the bolt. After insertion of the size were tested. Of them, 31 females laid eggs, whereas the other 64
larva, a layer of Parafilm (Bemis Co., Inc., Neenah, WI) was placed did not. All exposed females were dissected within 2 d to count the
over each end of the bolt to maintain wood moisture. Four bolts, number of residual mature eggs in their ovaries. The total number of
each containing a host larva, were exposed to 6–14 mated, 2- to eggs produced (i.e., laid plus residual mature eggs) was determined
3-d-old female wasps for 18–21 d in a 9-liter jar (Pioneer Plastics for each of the 31 females. The number of eggs produced by these
Inc., Dixon, KY) with a screen lid (8 cm diameter). Fine drops of females was compared with the females of equivalent age (i.e., 4 d
honey streaked on the screen top and water in a small vial (1.5 × old) from above test. The 64 females that did not lay eggs were ex-
5 cm) plugged with cotton were provided inside the jar as food ad cluded from the analysis because of possible confounding effects of
libitum for the parasitoids. After parasitoids had pupated (≈ 18 d), both oviposition and host plants or other host-associated stimuli on
each exposed bolt was dissected using a chisel and mallet to collect ovarian development in parasitoids (Wang and Messing 2003).
parasitoid cocoons. All cocoons were placed individually in gelatin During all above dissections, we noticed that a few females (7
capsules (Size 1, Herb Affair, Palatine, IL) until the emergence of of 553 dissected females) seemed to be abnormal as they contained
parasitoids. extremely low numbers of mature eggs, and their bodies were filled
with fat globules. Normal females had no such fat globules. These
Bioassays abnormal females were thus excluded from the analysis.
A series of three experiments was conducted. All bioassays were
conducted using the following methods which allowed easy access Host Size Selection and Suitability
to check for and see parasitoid development. After the host larvae Both choice and no-choice tests were conducted to determine
had developed into the sizes required for each bioassay (see below), whether adult female O. mellipes prefers to attack large over small
they were individually weighed on a Sartorius analytical balance host larvae and the consequences of host size selection in terms of
(Model 1801, ± 0.1 mg) and then placed underneath a flap of bark clutch size and offspring fitness (survival, developmental time, and
in the maple bolt (1–2 cm diameter, 16 cm long) as described by body size of emerged females). For this experiment, 3- to 6-d-old
Wang et al. (2019). The bark flap was attached at one end and a mated female wasps were used. In the choice test, one female wasp
narrow groove (6.5 × 0.5 × 0.3 cm) was created under using a #11 was exposed simultaneously to two maple bolts each containing
wood veneer chisel (Woodcraft Supply LLC, Parkersburg, WV) to either a large A. glabripennis larva (≈ fourth instar) or a small host
provide a space for the larva. The bark flap was then secured by a larva (≈ second instar). Because 7 d may pass before O. mellipes
layer of Parafilm after the larva was inserted into the groove. Tests parasitizes a host (Wang et al. 2019), the exposure time was set at
were carried out in plastic boxes (9.5 × 9.5 × 20.9 cm, Sistema 7 d. During the test, each bolt was checked carefully every 2 or 3
Plastics, New Zealand) that had four ventilation holes (3 cm diam- d under a microscope by opening the flap to determine which host
eter) covered with fine mesh, and the boxes were held inside a plant had been attacked, the order of attack, and the number of eggs laid
growth chamber. Honey and water were provided to the parasitoids on each parasitized host. In cases when both host larvae were found
throughout the experiments. parasitized, the order of attack was determined based on the devel-
opmental stages of the immature parasitoid eggs or young larvae,
Egg Maturation Dynamics of the Parasitoid as the parasitoid eggs develop rapidly in 1–2 d (Wang et al. 2019).
To determine how female O. mellipes matures eggs over time, groups After the parasitoid larvae had developed into pupae (i.e., 15–18
of 19–28 adult females were dissected at seven different ages (4 Journal of Economic Entomology, 2020, Vol. XX, No. XX
checked every 2 or 3 d until the host was found parasitized, and the between the female wasps that had produced eggs and those that did
number of eggs laid was counted. Like other ectoparasitoids, female not produce any eggs. The effect of host size on offspring develop-
O. mellipes inject venom into a host’s hemolymph to incapacitate it mental time from egg to adult emergence, body size, and mature egg
prior to the oviposition on the host’s surface. Our preliminary ob- load of developed females (all based on the mean value per clutch
servations found that the parasitoid left visible black scars on the of offspring) were also analyzed using one-way ANOVA. Prior to
surface of each parasitized host. We assumed that each sting caused the ANOVA, all data were checked for normality of residuals and
a black scar (which was often a small and round spot). Therefore, homoscedasticity with Shapiro’s and Bartlett’s tests. When an overall
the number of black scars indicated the number of times a host was ANOVA indicated that there was a significant effect of the factor, the
stung and was also recorded for each attacked host larva. In total, 41 mean values were separated using Tukey’s honestly significant differ-
parasitized host larvae of varying sizes were obtained. ence (HSD) test at α = 0.05.
All analyses were performed using JMP, Pro 14 (SAS Institute
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Female Size-Dependent Lifetime Fecundity Inc., Cary, NC, 1989–2019).
To determine whether the body size of adult female O. mellipes
would affect its realized reproductive success, a set of 30 female
Results
wasps with varying body size (metatibia length ranged from 1.202 to
1.850 mm) were monitored for their longevity and lifetime fecundity. Egg Maturation Dynamics of Parasitoid
Newly hatched (Journal of Economic Entomology, 2020, Vol. XX, No. XX 5
or clutch size (χ 2 = 1.8, P = 0.179). Host size also did not affect female produced 21.9 ± 2.8 (range 3–61) offspring. However, the
the parasitoid’s developmental time (from egg to adult emergence; total number of offspring produced per female wasp increased with
F1,36 = 2.7, P = 0.104). Offspring sex ratio (percentage of female) the female’s body size (Fig. 4). Dissection of dead females revealed
was also independent of the host (χ 2 = 1.6, P = 0.204) or clutch no effect of the female’s body size on the number of residual mature
size (χ 2 = 0.6, P = 0.446). However, female offspring emerging from eggs after the lifetime fecundity test (F1,28 = 1.6, P = 0.207). Dead
large host larvae were larger body than those reared from the small females contained 3.43 ± 0.76 residual mature eggs.
host larvae (F1,28 = 15.1, P < 0.001), and consequently, the large fe-
male wasps had more mature eggs than the small ones (F1,28 = 8.6,
P = 0.006). In the no-choice test, clutch size (range 1–27) increased Discussion
with host size (Fig. 3a) and was positively related to the number of
stings per parasitized host (Fig. 3b). The number of stings per para- This study revealed the ovarian dynamics of O. mellipes and the
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sitized host (y) was also related positively to the size of host larva (x) effect of host size on the parasitoid’s fitness in a potential novel asso-
(y = 1.068 + 0.001x, R2 = 0.038, P < 0.001). ciation with A. glabripennis. Ovarian dynamics is central to under-
standing a parasitoid’s foraging behavior and efficiency because the
physiological status of ovaries may determine when the parasitoid
Female Size-Dependent Lifetime Fecundity
is ready to lay eggs and if it can adjust oviposition rate based on
Adult female O. mellipes lived 21.9 ± 2.8 d (ranged 10–49 d), and
the availability of mature eggs (Jervis et al. 2001). In insect para-
their longevity was not affected by their body sizes (F1,28 = 0.9,
sitoids, most species are synovigenic (Jervis et al. 2001), and they
P = 0.342). In total, 1,333 host larvae were used, of which the
rely primarily on nutrients derived from larval stages for the produc-
parasitoids attacked 3.4 ± 0.4 hosts (range 1–10) during their life-
tion of eggs (Visser et al. 2010). In general, the capacity of a female
time, i.e., about 13% of the provided host larvae were parasitized.
parasitoid’s mature egg load is inversely correlated with its egg size
Thus, tested females had been provided with unlimited access to
(Jervis et al. 2001). Like many typical ectoparasitoids (Quicke 1997),
hosts during their lifetime. Host sizes were similar across repli-
an O. mellipes female produces relatively large and anhydropic eggs
cates, so mean sizes of host larvae attacked by the small (685.0 ±
as mentioned previously, and may not be able to hold a high number
23.9 mg) and large (697.3 ± 25.0) female wasps were not different
of mature eggs at any time possibly due to limited egg storage cap-
(F1,106 = 0.1, P = 0.749). The mean number of parasitized hosts was
acity. Under presumably suitable laboratory conditions, female
also not related to the female’s body size (F1,28 = 1.4, P = 0.245). Each
O. mellipes emerged with approximately 38.1 % of their lifetime
complement of eggs, and matured eggs rapidly, reaching a peak
within 4–6 d. Afterward, females seem to shut down egg production
50
b when deprived of hosts. The mature egg load of female O. mellipes
was affected by not only female age and body size, but also the inter-
Total number of eggs produced
40 a action of these two factors. These results suggest that young female
parasitoids are ready to oviposit at emergence, and large females not
30 only produce more eggs than smaller females but also seem to be
more capable of dynamically adjusting the rate of maturation egg
production in response to age.
20
Interestingly, we found that the act of oviposition triggered the
production of more mature eggs in young O. mellipes females. This
10 phenomenon is also reported in other parasitoids (e.g., Wang and
Messing 2003). Such a mechanism would maximize a parasitoid’s
0 fitness by producing more eggs in response to host availability.
No Yes Except direct host stimuli (oviposition), Papaj (2000) also proposed
Female's oviposition experience that indirect host stimuli, defined as stimuli from host resources such
as host plants or other host-associated cues, might promote ovarian
Fig. 2. Effect of oviposition experience on egg maturation of young female development in insects. We also compared the numbers of mature
Ontsira mellipes. Values are mean ± SE, and bars bearing different letters are eggs of the females that did not lay eggs in the presence of hosts
significantly different (Tukey’s HSD, P < 0.05). in bolts (36.2 ± 0.9, n = 64) with those females of equivalent age
Table 1. Ontsira mellipes preference for two size classes of Anoplophora glabripennis larvae in a choice test and the fitness consequences
of host size selection on the parasitoid’s offspring
Parameters n Small host larvaa n Large host larvaa
Fresh body mass of host (mg) 21 66.1 ± 5.1 a 26 775.5 ± 26.1 b
No. of eggs per parasitized host 21 6.1 ± 0.5 a 26 12.1 ± 1.3 b
Offspring survival of parasitoid (%) 21 92.1 ± 3.3 a 26 86.4 ± 4.1 a
Offspring developmental time (d)b 18 18.4 ± 0.8 a 20 20.1 ± 0.6 a
Female offspring (%) 18 61.8 ± 7.6 a 20 66.5 ± 9.0 a
Metatibia length of female (mm)b 15 1.53 ± 0.05 a 15 1.74 ± 0.02 b
Mature egg load of femaleb 15 21.5 ± 2.7 a 15 30.1 ± 1.1 b
a
Values (mean ± SE) followed by different letters within the row are significantly different (Tukey’s HSD, P < 0.05).
b
Values were calculated based on the mean size of all wasps from each clutch.6 Journal of Economic Entomology, 2020, Vol. XX, No. XX
(a) y = 0.008 x + 9.455 completely depleted of eggs. This suggests that despite the ovipos-
ition stimulus, the parasitoid may not be able to substantially in-
30 R² = 0.135, P = 0.018 crease egg production due to a limitation of larval-derived storage
reserves. Still, an inherent physiological mechanism seems to largely
25 determine the ovarian development in O. mellipes as it does in most
Clutch size
20 parasitoid species (Jervis et al. 2001, Visser et al. 2010).
For idiobiont, gregarious ectoparasitoids such as O. mellipes,
15 the quantity of resources (i.e., host size) available for the develop-
10 ment of progeny is fixed at the time of parasitism. Therefore, host
size selection by a female wasp can affect its offspring fitness attrib-
5 utes such as survival, developmental time, and sex ratio, as well as
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body size (Godfray 1994, Roitberg et al. 2001, Wang and Messing
0
2004). Therefore, many parasitoids have developed the adaptation
0 300 600 900 1200 1500 of assessing host size and adjusting their oviposition responses to
Host fresh weight (mg) maximize offspring fitness. In this study, we did not find a significant
preference for large over small hosts by O. mellipes, and a lack of
(b) host size preference suggests that this parasitoid may be unable to
30 directly assess host size before contact with the host (i.e., ovipositor
probing). Many parasitoids of larval woodborers employ host-
25 generated physical cues such as substrate vibrations caused by host
Clutch size
20 feeding or movement to locate the host in the wood (Hanks et al.
2001, Wang et al. 2010, Ulyshen et al. 2011, Paine 2017). Likely,
15 O. mellipes also detects host larvae using vibrations caused by their
feeding and such cues would provide the parasitoid with reliable in-
10
y = 3.045 x + 8.257 formation on the location and viability of the host. The frequencies
5 R² = 0.369, P = 0.038 or intensities of vibration signals from host larvae could be positively
related to host size. For example, Mankin et al. (2008) found that
0 young A. glabripennis larvae produce weaker vibrational signals
0 2 4 6 8 than mature larvae. However, this form of host location can be indis-
criminate in terms of host species and the absolute size of individual
No. of stings / parasitized host
hosts (Meyhofer and Casas 1999). Parasitoids may also use other
Fig. 3. Relationships (a) between Ontsira mellipes clutch size per parasitized
cues that are correlated with host size when making oviposition deci-
host and the size of the host Anoplophora glabripennis larva and (b) between sions. We found that both the number of sting marks by O. mellipes
the clutch size and number of stings per parasitized host. on each parasitized host was related positively to the clutch size or
host size, suggesting that the parasitoid may be able to assess host
size and adjust the clutch size decision accordingly after stinging the
70 y = 29.166 x - 23.640 host. It is likely that large larvae are more defensive physically and/
R² = 0.133, P = 0.048 or more resistant to envenomation than small larvae. The parasitoid
60
may be able to estimate host size indirectly based on the intensity of
Number of offspring produced
50 host resistance (i.e., number of stings needed to paralyze the host)
against the attack by O. mellipes.
40 We found that some offspring fitness parameters of O. mellipes,
such as offspring survival, developmental time, and sex ratio,
30 were independent of clutch or host size. The reported sex ratio of
O. mellipes in this study was low (around 60–65% of females) when
20
compared with several previous studies (around 80–85% of females;
10 Duan et al. 2015, Golec et al. 2016, Wang et al. 2019). Among the
parasitized hosts that produced adult wasps, 5 of 20 large hosts and
0 3 of 18 small hosts produced only adult males. We suspected that
1.0 1.2 1.4 1.6 1.8 2.0 tested parental females from these replicates did not mate success-
Female hind tibia length (mm) fully and this might have underestimated the sex ratio in this study.
As expected, clutch size increased positively with increasing host
Fig. 4. Realized lifetime reproductive success of female Ontsira mellipes on size and female wasps were larger when developed on large hosts
Anoplophora glabripennis larvae as affected by the female’s body size. versus small hosts. A lack of dependence of offspring survival or
developmental time on host size suggests that competition among
that were not given access to host or host bolts (35.1 ± 1.5, n = 24) siblings could be mediated through body size rather than survival of
and found that there was no difference between these two groups the offspring in O. mellipes. This mechanism (i.e., scramble compe-
(F1,86 = 0.4, P = 0.511). Thus, indirect host stimuli unlikely affect tition among offspring) can be expected for a gregarious parasitoid
egg maturation of O. mellipes. However, each female O. mellipes such as O. mellipes (i.e., a scramble competition among siblings;
attacked only a few hosts even when provided with unlimited ac- Godfray 1994). This also seems to indicate that O. mellipes grows
cess to hosts, and dissection of dead females at the end of the life- faster on the larger host larvae than the smaller, which reflects the
time fecundity test showed that most tested parasitoids were almost plasticity of body growth of this ectoparasitoid (Wang and MessingJournal of Economic Entomology, 2020, Vol. XX, No. XX 7
2004). It seems plausible for O. mellipes that this apparent lack of of Agriculture (USDA). USDA is an equal opportunity provider and
costs to offspring survival and developmental time in achieving a employer.
large body on the large host and the fitness advantage of being large
should favor selection by the parasitoid for large hosts. Then, why References Cited
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