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Article

The Temperature-Dependent Functional Response and Mutual Interference of Cyanopterus ninghais (Hymenoptera: Braconidae) Parasitizing Monochamus alternatus (Coleoptera: Cerambycidae)

by
Shaobo Wang
,
Mengjiao Han
,
Ke Wei
and
Xiaoyi Wang
*
Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing 100091, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(10), 2024; https://doi.org/10.3390/f14102024
Submission received: 7 September 2023 / Revised: 28 September 2023 / Accepted: 3 October 2023 / Published: 9 October 2023
(This article belongs to the Section Forest Health)
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Abstract

:
Cyanopterus ninghais (Hymenoptera: Braconidae) is a newly discovered parasitoid on the 3rd-5th instar larvae of the Japanese pine sawyer, Monochamus alternatus (Coleoptera: Cerambycidae). We investigated the functional response of C. ninghais at three temperatures (20, 25, and 30 °C) and examined mutual interference. Results showed that C. ninghais had a Holling Type II functional response at all temperatures. By increasing the density of the M. alternatus larvae, the number of parasitized larvae increased until a maximum was reached. The parasitoid was most effective (a′/Th) at 30 °C (0.270) and an individual female wasp’s attack rate (a′) was 0.158, the handling time (Th) was 0.587, and the maximum theoretical parasitization rate per day (T/Th) was 11.927. However, the per capita parasitized level and per capita searching efficiency decreased significantly when the parasitoid density ranged from one to five. These findings suggest that intraspecific mutual interference and competition occur when multiple females search for a host in the same area. This study demonstrates that C. ninghais serves as an effective biocontrol agent, displaying strong control capabilities against M. alternatus larvae, with the potential for further development in the context of biological pest management targeting M. alternatus.

1. Introduction

Pine wilt disease (PWD), caused by the pine wood nematode (PWN) Bursaphelenchus xylophilus Steiner and Buhrer, 1934 (Nematoda: Rhabditida: Aphelenchoididae), is a devastating disease of forests [1]. It was discovered in China in Hong Kong and Taiwan in the 1970s and subsequently on the mainland in 1982 at the Zhongshan Mausoleum in Nanjing [2,3,4]. PWD has led to the death of hundreds of millions of pine trees in China, resulting in annual economic losses amounting to billions of dollars [5,6]. The China State Forestry and Grassland Administration has announced that PWD has now spread to 701 administrative districts, comprising 19 provinces across China [7]. Managing PWD has become critical as its spread to the northeastern and northwestern regions of China has been remarkably swift [8]. Preventing the spread of this disease is one of the primary objectives for the sustainable development of China’s forestry. As a plant-parasitic nematode, the PWN lives in the xylem of trees and is limited to activity in the xylem, unable to spread from infected trees to healthy ones on its own. Its transmission and spread are closely associated with vector insects. Vector insects play a crucial role in spreading PWD, so vector control is a proactive and potentially effective management strategy that should be investigated [9].
The Japanese pine sawyer, Monochamus alternatus Hope, 1842 (Coleoptera: Cerambycidae) is the primary vector for PWD transmission in China [8]. The effective management of the population density of this beetle within forest ecosystems has the potential to mitigate or interrupt the propagation of PWD [10]. Presently, China employs several strategies for the control of M. alternatus: Firstly, chemical insecticide application during the adult stage is common, and it can rapidly reduce the population density of M. alternatus in forests [11]. Secondly, adult attractant traps are deployed to lure and kill M. alternatus in forest environments. Furthermore, they allow for the concurrent monitoring of the population density of M. alternatus in forests and the proportion of beetles carrying PWNs [12]. Thirdly, biological control using natural enemies mainly involves the release of Sclerodermus spp. During the larval stage of M. alternatus and Dastarcus helophoroides (Fairmaire, 1881) during the mature larval and pupal stages [9]. Notably, the use of dead wood covers alongside the release of D. helophoroides has facilitated the establishment of an arboreal ‘predator rearing ground’, resulting in effective control of M. alternatus during its mature larval and pupal phases [13,14]. In comparison to chemical insecticides, biological control methods offer the advantages of intervening during the larval stage of M. alternatus, thus mitigating the occurrence of insecticide resistance, inadvertent harm to non-target species, and environmental contamination. Consequently, these methods are preferred for the practical application of vector control [15].
While the prospect of using biocontrol in pest management holds considerable promise, the available natural enemy species for the biological control of M. alternatus remains notably deficient. In a previous investigation of PWD in the regions of Zunyi city, Guizhou Province, and Enshi city, Hubei Province, a gregarious ectoparasitoid targeting the 3rd-5th instar larvae of M. alternatus was discovered. Subsequent taxonomic analysis confirmed its identity as Cyanopterus (Bracomorpha) ninghais (Wang, Chen, Wu, and He, 2009) [16,17]. As an idiobiont ectoparasitoid, this parasitoid has a natural parasitic rate of up to 30%, and appears to be a specialist of M. alternatus larvae. A single host beetle can support the development of up to 25 parasitoid offspring, indicating significant potential for the development of this parasitoid as a biocontrol method for M. alternatus. To date, only the taxonomic delineation and biological characteristics have been determined for C. ninghais [16,17,18].
Functional response is a key metric for assessing the potential of natural enemies in pest control [19]. Functional response analysis of S. alternatusi against the 3rd instar larvae of M. alternatus showed that a single female killed up to 9.48 larvae, with a parasitoid–host ratio of 1:1 yielding the greatest control [20]. Furthermore, previous investigations have revealed that nearly all parasitoid functional response curves conform to the Holling Type II model, including cases such as the parasitism of Myzus persicae (Sulzer, 1776) by Aphidius gifuensis (Ashmead, 1906), and the control of Plutella xylostella (Linnaeus, 1758) larvae through parasitism by Oomyzus sokolowskii (Kurdjumov, 1912) [21,22]. However, most of these studies focus on exploring the impact of the host size (instar) on the functional response parameters. In general, the handling time of hosts by parasitoids increased as the host instar aged, mainly influenced by the size of the host. Temperature, a pivotal environmental factor affecting insect reproduction and development, also had a substantial influence on the parasitoid functional response parameters [23]. However, current research typically uses a single temperature that is conducive to parasitoid reproduction, leaving the efficacy of parasitism within other temperature ranges unexplored. In the context of biocontrol application, particularly in cases where the natural enemy is translocated, accounting for the temperature’s influence on control efficacy becomes imperative [24]. The objectives of this study were to establish a theoretical foundation for assessing the control capability of C. ninghais against M. alternatus larvae to inform the application of potential field releases. Therefore, we studied the parasitism performance of C. ninghais on different host densities under different temperatures, as well as the mutual interference of parasitoid density.

2. Materials and Methods

2.1. Insect Cultures

All insect rearing and experiments were conducted in the Laboratory of Natural Enemy Insects and Biological Control, Chinese Academy of Forestry, Beijing, China. Cyanopterus ninghais is a synorogenic parasitoid, and its pre-oviposition period gradually increases with decreasing temperatures. The pre-oviposition period at temperatures ranging from 20 to 30 °C was maintained for 4–10 days. To minimize this interference, we used 10-day-old gravid females of C. ninghais that were naïve (i.e., had no prior exposure to hosts) as parasitoids. Healthy 4th instar larvae (300–400 mg) of M. alternatus were used as hosts for rearing the parasitoids and conducting the experiments. Colonies were maintained at 25 °C ± 1 °C, 14:10 h (L: D), and 60% ± 10% RH.

2.2. Parasitoid and Host Rearing

The parasitoid colony was established from collections of parasitized M. alternatus larvae from the Masson’s pine (Pinus massoniana Lamb., 1803) forest in Gongqing Lake, Zunyi City, Guizhou Province (27.5977° N, 106.8391° E) in 2022, and maintained on M. alternatus in Masson’s pine logs. The M. alternatus colony was also established from the collections from the same Masson’s pine (P. massoniana) forest that was infested and maintained on an artificial diet, as described by Chen et al. (Composition: Self-made Masson’s pine sawdust; sucrose; soybean protein; Wesson’s salt mixture; cholesterol; Kretschmer wheat germ; sorbic acid and methyl paraben. All reagents were purchased from Sinopharm Chemical Reagent Co. Ltd. Shanghai, China) [25]. Fresh Masson’s pine wood was cut into logs (diameter 4 ± 1 cm, length 20 ± 1 cm) and a U-shaped cut (length 3.5 cm, width 1 cm) was made longitudinally into the bark of each log. The bark was pried open from the “U”-shaped cut but not removed, and a 1 cm deep groove was made into the wood partway along the edge of the cut. A larva of M. alternatus was placed in the groove, the bark was closed, and the cut end was sealed with Parafilm M® (Heathrow Scientific, Vernon Hills, IL, USA). A total of 2–10 grooves with M. alternatus larvae were made in each log. The F5 generation of this population was used for this study.

2.3. Functional Response

The experiments were performed in a controlled environmental chamber (Haishu Saifu Experimental Instrument Factory, Ningbo, China) at three temperatures: 20 ± 1 °C, 25 ± 1 °C, and 30 ± 1 °C (one above and one below the optimal survival temperature). Host densities of 2, 4, 6, 8, and 10 M. alternatus larvae were used. The host larvae were placed within logs of pine wood. A single wood log containing host larvae and a female C. ninghais was placed in a rearing container (Sutai Plastic Products Co., Ltd., Cangzhou, China) (base diameter of 8 cm and height of 22 cm). Ventilation was provided through a mesh window (6 cm × 5 cm) in the container’s wall. Honey (Baihua Bee Industry Technology Development Co., Ltd., Beijing, China) was applied to the mesh to provide a food source for the parasitoid adults. A 25 mL plastic cup (Sutai Plastic Products Co., Ltd., Cangzhou, China) (base diameter of 3.0 cm and height of 3.3 cm) containing a 5 cm cotton swab (Bstar Medical Device Co., Ltd., Shenzhen, China) and water was placed in the rearing container. After 7 d, the female parasitoid was removed. The wood logs were maintained under their initial conditions until the emergence of a wasp progeny. Upon completion of parasitoid emergence (no parasitoids emerging for a consecutive 5 d period), the wood logs were dissected and the number of parasitized hosts were recorded. Experiments at each temperature consisted of 15 replicates, with one female parasitoid per replicate.
The data were analyzed in two steps [26]. First, a logistic regression of the proportion of parasitized hosts at the initial host density at the three temperatures was used to determine the type of functional response of C. ninghais to the M. alternatus larvae, using the Proc CATMOD procedure in the SAS software.
N a N o = e x p P 0 + P 1 N 0 + P 2 N O 2 + P 3 N O 3 1 + e x p P 0 + P 1 N 0 + P 2 N O 2 + P 3 N O 3
where Na is the number of parasitized hosts, No is the initial host density, (Na/No) is the probability of hosts being parasitized, and P0, P1, P2, and P3 are the intercept, linear, quadratic, and cubic coefficients, respectively. Coefficients were estimated using the method of maximum likelihood. The type of functional response was deduced based on the positive or negative values of coefficients P1 and P2. A negative linear coefficient (P1 < 0) indicates a Type II functional response, wherein the proportion of parasitized hosts decreases consistently with the initial host’s density. Conversely, a positive linear coefficient (P1 > 0) coupled with a negative quadratic coefficient (P2 < 0) signifies a Type III functional response [26].
Secondly, the parameters of the searching efficiency and handling time were determined by fitting Holling’s disc equation [27], as below:
N a = a ′ T N o / ( 1 + a ′ T h N o )
where Na = number of parasitized hosts;
No = initial host density;
a′ = attack rate;
T = total time of the experiment’s duration (7 d);
Th = handling time, the duration of the parasitoid’s activities of pursuing, subduing, and parasitizing a host individual, plus preparing for the search for another host. The parasitoid attack rate per handling time (a′/Th) and maximum theoretical parasitization rate per day (T/Th) were also calculated. The equations were solved with non-linear least squares regression using the Proc NLIN procedure in the SAS software.

2.4. Intraspecific Mutual Interference

The experiments were carried out in a controlled environmental chamber at a constant temperature of 25 ± 1 °C, 60 ± 10% RH, and a 16:8 h L:D photoperiod. To study the mutual interference among C. ninghais adults, five wood logs containing thirty 4th instar M. alternatus larvae were exposed to either 1, 2, 3, 4, or 5 mated C. ninghais females in separate rearing cages (Chongyi Biological Technology Co., Ltd., Taiyuan, China) (20 cm × 20 cm × 20 cm). Cotton balls soaked (Bstar Medical Device Co., Ltd., Shenzhen, China) in a 20% honey solution were supplied to the parasitoids for nutritional supplementation and changed every 48 h. The females were removed after 7 d, and the wood logs containing larvae were maintained under the initial conditions until the emergence of a parasitoid progeny was completed, as described earlier. The number of parasitized hosts was recorded for each cage. Experiments at each treatment consisted of 5 replicates. Hassell and Varley’s model [28] was fitted to the data to calculate the parameters of mutual interference, as below:
E = Q × P − m
where E = area of discovery/searching efficiency;
Q = quest constant (value of E when P = 1);
m = mutual interference coefficient;
P = parasitoid density.
The searching efficiency (E) [29], a measure of per capita parasitization when there is mutual interference between individual parasitoids in the same searching arena, was calculated as below:
E = 1 P T ln N N − N a
where P is the parasitoid density, T is the total time of the experiment’s duration (7 d), N is the number of host larvae offered (density), and Na is the number of parasitized host larvae.
To simplify the analysis of variation in the mutual interference as a result of the increased parasitoid density, a formula for the intensity of the scrambling competition (I) was introduced [30]:
I = E 1 − E P / E 1
where I = the intensity of the scrambling competition;
E1 = the searching efficiency of a single parasitoid;
EP = the searching efficiency of P number of parasitoids.

2.5. Statistical Analysis

The functional response was estimated using logistic polynomial regression, and parameters (the attack rate (a′) and handling time (Th)) were estimated using nonlinear regression in Holling’s disc equation. All these analyses were conducted using SAS Version 9.4 (SAS Institute, Cary, NC, USA). A two-way analysis of variance (ANOVA) was used to ascertain significant differences between the treatments, followed by Tukey’s test for comparisons of the means (p < 0.05), using SPSS 26 for Windows (IBM SPSS Inc.®, Chicago, IL, USA). All figures were created using Origin 2021 (OriginLab Corporation, Northampton, MA, USA).

3. Results

3.1. Parasitism by Cyanopterus ninghais on Monochamus Alternatus at Three Temperatures

A two-way ANOVA of the number of parasitized hosts revealed a significant effect of both temperature and host density (temperature: F = 22.61, df = 2, 8, p < 0.001; host density: F = 99.41, df = 4, 8, p < 0.001), but not a significant difference for interaction (F = 0.63, df = 2, 4, p < 0.562). Under each temperature, the number of parasitized hosts increased with the increasing number of hosts offered (host density); however, the proportion of parasitized hosts declined as the host density increased. Significant differences were observed in the number of hosts that were parasitized under different host densities (20 °C: F = 21.31, df = 4, 70, p < 0.001; 25 °C: F = 45.77, df = 4, 70, p < 0.001; 30 °C: F = 38.63, df = 4, 70, p < 0.001). The maximum number of parasitized hosts occurred at a host density of 10 under 20 °C, 25 °C, and 30 °C, with 4.13 ± 0.27, 5.00 ± 0.29, and 5.67 ± 0.32, respectively. Conversely, the lowest number of parasitized hosts were observed at a host density of two under each temperature, with 1.20 ± 0.11, 1.47 ± 0.13, and 1.73 ± 0.12, respectively (Table 1). The number of parasitized hosts increased significantly when the host densities ranged from two to six across all temperatures, but as the host density reached and exceeded eight, the rate of increase in the number of parasitized hosts gradually slowed and plateaued (Figure 1).
The number of hosts that were parasitized by C. ninghais increased significantly with the increasing temperature at each host density (host density = 2: F = 4.94, df = 2, 42, p = 0.012; host density = 4: F = 5.89, df = 2, 42, p = 0.006; host density = 6: F = 4.42, df = 2, 42, p = 0.023; host density = 8: F = 3.71, df = 2, 42, p = 0.033; host density = 10: F = 6.76, df = 2, 42, p = 0.003) (Table 1). The number of parasitized hosts at the same host density varies greatly under different temperatures. Across host densities, the greatest parasitism rates were measured at 30 °C, with the least occurring at 20 °C. Both 30 °C and 25 °C resulted in significantly greater parasitism rates compared to at 20 °C.

3.2. Functional Response

Logistic regression was used to model the proportion of parasitized hosts (Na/No) against the host density (Na). The models indicate that temperature had no influence on the functional response of C. ninghais towards the M. alternatus larvae, i.e., the functional responses were the same at different temperatures. The linear coefficient (P1) showed a consistently negative trend across all temperatures. The functional response curve was a Type II pattern for each temperature (Table 2).
Holling’s disc equation was used to fit the functional response of C. ninghais towards the larvae of M. alternatus at various temperatures. The attack rate (a′) increased with the increasing temperature, whereas the handling time (Th) decreased. The parasitoid attack rate per handling time (a′/Th) and the maximum theoretical rate of parasitism per day (T/Th) increased with the increasing temperature (Table 3). Specifically, at 30 °C, a′ peaked at 0.158/h, and Th was shortest at 0.587 h. Over the 7 days, T/Th was 11.927. The functional response data and the corresponding fitted equation curves for each temperature were illustrated in Figure 1.

3.3. Intraspecific Mutual Interference

When the density of host M. alternatus larvae was kept at 30, an increase in the parasitoid density (P) from one to five resulted in a significant increase in the number of parasitized hosts, from 5.20 ± 0.37 to 13.80 ± 0.67 (F = 24.71, df = 4, 20, p < 0.001). Conversely, the number of parasitized hosts per capital decreased significantly from 5.20 ± 0.37 to 2.76 ± 0.17 (F = 14.28, df = 4, 20, p < 0.001). The per capital searching efficiency (E) decreased from 1.34 ± 0.11 to 0.87 ± 0.07 (F = 4.88, df = 4, 20, p = 0.007) (Table 4). The relationship between P and the number of parasitized hosts was fitted using a parabolic pattern: Y = − 0.243 X 2 + 3.557 X + 1.960 (R2 = 0.829, F = 53.33, df = 2, 22, p < 0.001). The relationship between E and P was calculated by fitting the Hassell–Varley interference model to the data, yielding E = 1.346 × P − 0.272 (R2 = 0.992, F = 322.26, df = 1, 3, p < 0.001), with an interference coefficient of 0.272.
The linear regression analysis of log E and the log intensity of the scrambling competition against log P for C. ninghais parasitizing M. alternatus larvae was conducted in this study. The searching efficiency of C. ninghais decreased with an increase in the parasitoid density, whereas the intensity of the scrambling competition increased (Figure 2). The intensity of scrambling competition (I) formula was used to elucidate the competitive dynamics arising from the increased parasitoid density. Upon fitting to the data, the correlation between the intensity of the scrambling competition (I) and the log of the parasitoid density (P) was found to be I = 0.5093 L o g   P + 0.0019 (R2 = 0.994, F = 532.73, df = 1, 3, p < 0.001) (Figure 2). This relationship underscores a highly significant correlation between the two variables, signifying a notable elevation in the intensity of the scrambling competition alongside an increase in the parasitoid density. When the parasitoid density reaches five, the calculated intensity of the scrambling competition stands at 0.348.

4. Discussion

Functional response analyses are used to assess the potential of predatory or parasitoid insects to control an insect pest [31]. This study found that the parasitic efficacy of C. ninghais against 4th instar M. alternatus larvae followed a specific pattern: as the host density increased, the efficacy of an individual parasitoid increased until reaching a host density of eight or more, whereabouts the rate of increase plateaued, indicating a saturation effect. Across the three temperature conditions, the functional response of this parasitoid followed the Holling Type II model, which is consistent with most observed parasitic functional responses [32,33,34]. The time allowed for parasitizing the host in this study was 7 d, differing from the more common 24 h interval used in other research studies [31,35]. This duration was chosen based on the unique biological characteristics of C. ninghais, which has a typical synorogenic parasitism strategy. Post-emergence, the parasitization process does not occur instantaneously but requires a waiting period for egg development within the ovaries. After parasitizing one host, another waiting period is required for egg maturation in the ovaries, enabling subsequent parasitic activity. Given that C. ninghais typically parasitizes a maximum of one host within 24 h, a too-short study duration fails to accurately reflect its true parasitic capacity. Therefore, the parasitic time for this parasitoid in this study was set at 7 d.
Temperature influences the growth, development, and lifespan of insects, and also directly impacts the foraging and parasitic behaviors of natural enemy insects [36]. The results unequivocally demonstrated that temperature significantly affected the parasitoid’s attack rate and handling time. As the temperature rises, the attack rate increases and the handling time decreases, a pattern that is consistent with other studies on parasitoids [37,38]. Furthermore, our study revealed that at 30 °C, the parasitoid attack rate per handling time and the maximum theoretical parasitization rate per day reached their peak. While the temperature did not affect the functional response type of the parasitoid, it did directly influence the parasitic activity. Under higher temperatures, the wasp’s parasitic behavior became more active, thus enhancing its pest control capacity. At the same time, more activity demands an increased energy expenditure and output, which might contribute to the relatively shorter lifespan of parasitoids under elevated temperatures. Hence, when using this parasitoid for indoor mass rearing and subsequent field release for pest management, striking a balance between the temperature’s impact on the parasitoid efficacy and lifespan becomes crucial to select the optimal rearing temperature and application timeframe. Besides the temperature, factors such as the host’s developmental stage, the habitat complexity, the search area size, and the availability of alternative food sources can also influence the functional response of natural enemy insects toward their hosts [39]. Consequently, the results from indoor bioassays, such as in this study, should be used only as reference indicators for practical applications. In real-world scenarios, a judicious integration of these findings into the specific environment is paramount.
Research has shown that parasitoids in confined spaces demonstrate varying levels of intraspecific interference and competition as their population density rises [35,40]. This study showed that the per capita searching efficiency of C. ninghais towards hosts decreased significantly with an increase in its density. The main factor contributing to this is closely associated with the dimensions of the enclosed experimental area. Within a confined area, greater parasitoid densities are associated with an increased probability of mutual interference. Furthermore, this may also be connected to the observed phenomenon of cooperative interactions among female wasps during the experimental process, wherein they collaborate to subdue the host. The intensity of the scrambling competition formula was used to determine the effects of an increased parasitoid density on intraspecific competition in this study. The intensity of the scrambling competition (I) reached only 0.348 when the parasitoid density reached five. This suggests that, while intraspecific interference existed, its effect was not strong. Increased parasitoid population densities could be considered in field applications and indoor rearing. Not only can parasitoids cooperate to reduce the energy expenditure and handling time that are required to subdue hosts, they can also handle larger hosts that a single female may struggle with. While indoor study data may not comprehensively elucidate the interactions among parasitoids in natural environments, this information aids in comprehending interactions within specific parasitoid populations that target specific host patches.
In comparison to other parasitoids that target larval-stage M. alternatus, C. ninghais demonstrates a significantly better control capability. Commonly applied in the biological control of early instar M. alternatus larvae, parasitoids such as Sclerodermus spp. express robust “maternal care” behaviors [41]. After laying their eggs on the host’s body, these parasitoids remain near to ensure the well-being of their progeny. In contrast, C. ninghais displays a remarkably efficient parasitization process, characterized by a relentless search for hosts and the successful completion of parasitism. Previous investigations have shown that an individual S. guani can cause the death of up to 9.48 3rd instar M. alternatus larvae within 21 d [20]. In contrast, our current study revealed that an individual C. ninghais can parasitize and lead to the death of 11.93 4th instar M. alternatus larvae within just 7 d, thus highlighting its remarkable and efficient control capability. Furthermore, C. ninghais has strong host specificity and reproductive potential, further underscoring its promise as a highly effective biological control agent against early instar larvae of M. alternatus. Subsequent research should focus on its role in strategies using this parasitoid for the biological control of M. alternatus.

5. Conclusions

This study delves into the control effect of C. ninghais on the larval stage of M. alternatus from the perspectives of functional response and mutual interference. The findings reveal the following outcomes: (1) Temperature had no influence on the functional response of C. ninghais towards M. alternatus larvae, as it consistently exhibited a Holling Type II functional response at three temperatures (20, 25, and 30 °C). (2) With the increasing temperature, the attack rate (a′) increased, while the handling time (Th) decreased. (3) C. ninghais exhibited its highest effectiveness (a′/Th) at 30 °C, where the maximum theoretical parasitization rate per day (T/Th) was 11.927. (4) With the increasing parasitoid density, the mutual interference among C. ninghais gradually reduced the search efficiency and simultaneously intensified the scrambling competition. In summary, C. ninghais effectively regulates M. alternatus larvae across a range of suitable temperatures. Furthermore, C. ninghais shows superior efficiency when compared to other natural enemies during the larval stage of M. alternatus.

Author Contributions

Conceptualization, S.W., M.H., K.W. and X.W.; methodology, S.W., M.H. and X.W.; formal analysis, S.W., K.W. and X.W.; investigation, S.W., M.H., K.W. and X.W.; data curation, S.W. and X.W.; writing—original draft preparation, S.W.; writing—review and editing, S.W., M.H., K.W. and X.W.; visualization, S.W. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Key R&D Program of China (2021YFD1400900) and the Fundamental Research Funds of Chinese Academy of Forestry (CAFYBB2021ZG001).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to administrative restrictions.

Acknowledgments

We sincerely thank Yanlong Tang from Zunyi Normal University for help with the parasitoid colony collection.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 02024 g001
Figure 1. Parasitism of M. alternatus larvae by C. ninghais at three temperatures and five host densities (A–C). Dots represent the number of parasitized hosts at each initial host density, and black lines were predicted using Holling’s disc equation.
Figure 1. Parasitism of M. alternatus larvae by C. ninghais at three temperatures and five host densities (A–C). Dots represent the number of parasitized hosts at each initial host density, and black lines were predicted using Holling’s disc equation.
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Forests 14 02024 g002
Figure 2. Regression lines indicate that mutual interference and scrambling competition increased as the density of C. ninghais increased.
Figure 2. Regression lines indicate that mutual interference and scrambling competition increased as the density of C. ninghais increased.
Forests 14 02024 g002
Table 1. The functional response of C. ninghais females to the 4th instar larvae of M. alternatus at different host densities and temperatures. Number of replications (N) = 15.
Table 1. The functional response of C. ninghais females to the 4th instar larvae of M. alternatus at different host densities and temperatures. Number of replications (N) = 15.
Host Density (No)20 °C25 °C30 °C
Number of
Parasitized Hosts (Na)		Proportion of
Parasitized Hosts (Na/No)		Number of
Parasitized Hosts (Na)		Proportion of
Parasitized Hosts (Na/No)		Number of
Parasitized Hosts (Na)		Proportion of
Parasitized Hosts (Na/No)
21.20 ± 0.11 Cb0.60 ± 0.051.47 ± 0.13 Dab0.73 ± 0.071.73 ± 0.12 Da0.87 ± 0.06
42.33 ± 0.21 Bb0.58 ± 0.052.80 ± 0.15 Cab0.70 ± 0.043.20 ± 0.18 Ca0.80 ± 0.04
63.27 ± 0.33 ABb0.54 ± 0.063.73 ± 0.23 Bab0.62 ± 0.044.47 ± 0.32 Ba0.74 ± 0.05
84.00 ± 0.34 Ab0.50 ± 0.044.60 ± 0.21 Aab0.58 ± 0.035.07 ± 0.27 ABa0.63 ± 0.03
104.13 ± 0.27 Ab0.41 ± 0.035.00 ± 0.29 Aab0.50 ± 0.035.67 ± 0.32 Aa0.57 ± 0.03
Note: data in the table are mean ± SE. Different uppercase letters indicate a significant difference (Tukey test, p < 0.05) between host densities, and different lowercase letters indicate significant differences (Tukey test, p < 0.05) among temperatures.
Table 2. Results of polynomial logistic regression analyses, indicating the estimated and standard errors of the linear coefficients for the proportion of M. alternatus larvae parasitized by C. ninghais.
Table 2. Results of polynomial logistic regression analyses, indicating the estimated and standard errors of the linear coefficients for the proportion of M. alternatus larvae parasitized by C. ninghais.
TemperatureParameterEstimateSEχ2p
20 °CP1−2.2781.7151.7670.184
P20.1490.3060.2380.626
P3−0.0020.0170.0130.908
25 °CP1−5.5873.2153.0190.082
P20.6110.5061.4580.227
P3−0.0250.0250.9590.328
30 °CP1−8.8194.2344.3390.037
P2−0.0500.0312.6170.106
P31.1360.6443.1180.078
Table 3. Parameters estimated using Holling’s equation for C. ninghais parasitizing M. alternatus larvae at three temperatures.
Table 3. Parameters estimated using Holling’s equation for C. ninghais parasitizing M. alternatus larvae at three temperatures.
TemperatureHolling Disc EquationAttack Rate (a′)Handling Time (Th)T/Tha′/Th
20 °CNa = 0.788No/(1 + 0.082No)0.113 ± 0.0200.732 ± 0.2129.5660.154
25 °CNa = 0.925No/(1 + 0.083No)0.132 ± 0.0160.628 ± 0.120311.1520.211
30 °CNa = 1.107No/(1 + 0.093No)0.158 ± 0.0200.587 ± 0.11011.9270.270
Note: data in the table are mean ± SE.
Table 4. Mutual interference within C. ninghais parasitizing the 4th instar larvae of M. alternatus at different parasitoid densities. Number of replications (N) = 5.
Table 4. Mutual interference within C. ninghais parasitizing the 4th instar larvae of M. alternatus at different parasitoid densities. Number of replications (N) = 5.
Parasitoid Density
(Females) (P)		Number of
Parasitized Hosts		Per Capital
Parasitized		Per Capital Searching
Efficiency (E)
15.20 ± 0.37 d5.20 ± 0.37 a1.34 ± 0.11 a
28.20 ± 0.58 c4.10 ± 0.29 b1.12 ± 0.09 ab
310.60 ± 0.51 bc3.53 ± 0.17 bc1.02 ± 0.06 ab
412.00 ± 0.86 ab3.00 ± 0.22 c0.90 ± 0.08 b
513.80 ± 0.67 a2.76 ± 0.17 c0.87 ± 0.07 b
Note: data in the table are mean ± SE. Different lowercase letters in each column indicate significant difference (Tukey test, p < 0.05) among parasitoid densities.
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Wang, S.; Han, M.; Wei, K.; Wang, X. The Temperature-Dependent Functional Response and Mutual Interference of Cyanopterus ninghais (Hymenoptera: Braconidae) Parasitizing Monochamus alternatus (Coleoptera: Cerambycidae). Forests 2023, 14, 2024. https://doi.org/10.3390/f14102024

AMA Style

Wang S, Han M, Wei K, Wang X. The Temperature-Dependent Functional Response and Mutual Interference of Cyanopterus ninghais (Hymenoptera: Braconidae) Parasitizing Monochamus alternatus (Coleoptera: Cerambycidae). Forests. 2023; 14(10):2024. https://doi.org/10.3390/f14102024

Chicago/Turabian Style

Wang, Shaobo, Mengjiao Han, Ke Wei, and Xiaoyi Wang. 2023. "The Temperature-Dependent Functional Response and Mutual Interference of Cyanopterus ninghais (Hymenoptera: Braconidae) Parasitizing Monochamus alternatus (Coleoptera: Cerambycidae)" Forests 14, no. 10: 2024. https://doi.org/10.3390/f14102024

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