Sie können Operatoren mit Ihrer Suchanfrage kombinieren, um diese noch präziser einzugrenzen. Klicken Sie auf den Suchoperator, um eine Erklärung seiner Funktionsweise anzuzeigen.
Findet Dokumente, in denen beide Begriffe in beliebiger Reihenfolge innerhalb von maximal n Worten zueinander stehen. Empfehlung: Wählen Sie zwischen 15 und 30 als maximale Wortanzahl (z.B. NEAR(hybrid, antrieb, 20)).
Findet Dokumente, in denen der Begriff in Wortvarianten vorkommt, wobei diese VOR, HINTER oder VOR und HINTER dem Suchbegriff anschließen können (z.B., leichtbau*, *leichtbau, *leichtbau*).
Diese Studie untersucht die räuberische Dynamik zwischen Pterostichus melanarius, einem bodenfressenden Käfer, und der Sojabohnengallmücke Resseliella maxima. Die Forschung konzentriert sich auf die Fähigkeit des Käfers, Kokon-Larven und Puppen zu verzehren, ein bisher wenig untersuchter Aspekt ihrer Interaktion. Die Studie zeigt, dass Pterostichus melanarius durch Wahlfreiheit, Wahlfreiheit und Bodenuntersuchungen in der Lage ist, sich tatsächlich in versteckten Stadien zu verstecken, wenn auch in unterschiedlicher Geschwindigkeit. Die Ergebnisse deuten darauf hin, dass die Käfer, während sie zunächst freie Larven bevorzugen, lernen können, mit der Zeit gefräßige Beute zu verzehren. Das Vorhandensein von Böden beeinflusst die Raubtierraten erheblich, was die Bedeutung realistischer experimenteller Bedingungen unterstreicht. Diese Forschung bietet wertvolle Einblicke in das Potenzial von Pterostichus melanarius als biologisches Mittel zur Bekämpfung der Sojabohnengallmücke und trägt zur Entwicklung integrierter Schädlingsbekämpfungsstrategien bei.
KI-Generiert
Diese Zusammenfassung des Fachinhalts wurde mit Hilfe von KI generiert.
Abstract
The soybean gall midge, Resseliella maxima Gagné (Diptera: Cecidomyiidae), feeds on soybean, Glycine max (L.) Merrill (Fabales: Fabaceae), causing significant injury and yield losses. Pterostichus melanarius Illiger (Coleoptera: Carabidae), a generalist predator introduced to North America, has been reported to prey on R. maxima larvae under laboratory conditions. Understanding the feeding preference of P. melanarius on different prey life stages is important to evaluate its role in the biological control of R. maxima. Three laboratory experiments were conducted to assess predatory behaviors. In a no-choice test, P. melanarius adults fed on both R. maxima free (i.e., not cocooned) larvae and cocooned larvae, showing significant differences in prey consumption between R. maxima developmental stages over time. A choice test revealed a preference of P. melanarius adults for free larvae over cocooned larvae within the first hour, although this preference was not significant after 24 h. In an experiment examining the effect of soil on predation rates, P. melanarius adults consumed larvae and cocooned pupae placed either without soil, on the soil surface, or at a 1 cm depth, and predation rates were influenced by prey stage and the presence and depth of soil. These findings indicate that P. melanarius adults can feed on cocooned life stages, but that the presence of soil may hinder predation.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Introduction
Soybean gall midge, Resseliella maxima Gagné (Diptera: Cecidomyiidae) was described in 2019 in the Midwestern USA as a new species that feeds on stems of soybean, Glycine max (L.) Merrill (Fabales: Fabaceae) (Gagné et al. 2019). Infestation of soybean plants by this insect pest typically begins when soybean plants have 2–3 fully developed trifoliate leaves, when females oviposit at the base of the plants in natural cracks that occur during plant growth (McMechan et al. 2021a). After hatching, the larvae of R. maxima enter the stem and feed beneath the plant's epidermis, with larvae moving into the phloem, xylem, and pith as time passes (Gagné et al. 2019). Injury to these plant tissues can lead to wilting, plant death, and yield losses (McMechan et al. 2021a; Helton et al. 2022). Once mature, the larvae drop from the plants, burrow into the soil, build silken cocoons, and then either immediately pupate or overwinter as larvae before pupation in the spring (McMechan et al. 2021b). Adults eventually emerge out of the soil (McMechan et al. 2021b).
Resseliella maxima is present in seven soybean-producing states (i.e., Iowa, Kansas, Minnesota, Missouri, Nebraska, North Dakota, and South Dakota) (https://soybeangallmidge.org), which together account for more than 43% of the total soybean production in the USA (USDA 2024). Yield losses caused by infestations of R. maxima can exceed 92% within the first 30 m from the field edges and can reach up to 31% in the interior of the field (McMechan et al. 2021a). The expanding range of R. maxima and its potential to cause yield losses to soybean press for the identification of potential management methods for this pest. Foliar insecticides and granular at-plant insecticides have shown some suppression of the pest. However, their effects are inconsistent and likely not sufficient for effective control (Cooper and McMechan 2024; Hodgson and Helton 2021; McMechan 2021; Montenegro et al. 2022). Cultural control, such as hilling, can be highly effective at reducing R. maxima infestation and yield loss, but this practice requires specialized equipment and is not common in soybean production (McMechan et al. 2023; Gupta and McMechan 2025). Soybean genotypes are being screened for resistance to R. maxima to provide a foundation for development of host plant resistance (Sever 2021).
Anzeige
Biological control of R. maxima is also being assessed. A new species of wasp, Synopeas maximum Awad & Talamas (Hymenoptera: Platygastridae) was identified and described as a parasitoid of R. maxima (Melotto et al. 2023a), but its parasitism rate in the field is relatively low (Melotto et al. 2023b). A second wasp, Synopeas ruficoxum Buhl (Hymenoptera: Platygastridae) recently had its parasitoid-host association with R. maxima confirmed, although its distribution and parasitism rate remain unknown (von Gries et al. 2025a). The role of predators was investigated in soybean fields in southwest Minnesota, and Pterostichus melanarius (Illiger) (Coleoptera: Carabidae) was the most abundant among the ground-foraging predatory species found (Melotto et al. 2023c). Adults of P. melanarius feed on R. maxima larvae under laboratory conditions (Melotto et al. 2023c), and P. melanarius exhibits a preference for R. maxima larvae over an alternative prey species as well as a Type I (i.e., linear) functional response across R. maxima densities (von Gries et al. 2025b).
Pterostichus melanarius is an exotic, omnivorous generalist predator unintentionally introduced to North America that feeds on insects, nematodes, plant tissue, and spores (Pollet and Desender 1985; Busch et al. 2021). It is also an opportunist, feeding on the most abundant prey (Pollet and Desender 1985; Busch et al. 2021). In the field, when third instar larvae of R. maxima drop to the ground, they may become more vulnerable to attacks from ground-foraging predators such as P. melanarius. Given that R. maxima larvae burrow into the soil and form cocoons, it raises the question of whether P. melanarius adults can locate and open these cocoons to consume the larva or pupa inside. Thus, this study was conducted to evaluate: (1) the consumption rate of P. melanarius on cocooned R. maxima larvae (no-choice test), (2) the feeding preference of P. melanarius adults between free (i.e., not cocooned) R. maxima larvae and cocooned R. maxima larvae (choice test), and (3) the ability of P. melanarius adults to find and feed on buried cocooned R. maxima pupae (soil test). This information will provide insights on the role of P. melanarius as a biological control agent of R. maxima.
Material and methods
No-choice test
Pterostichus melanarius adults were collected as described in Melotto et al. (2023c), using dry pitfall traps (11.5 cm diameter × 14 cm length) in a soybean field near Luverne, Minnesota, USA in July and August of 2023. Pterostichus melanarius were separated from the by-catch, transported to the laboratory in coolers, then kept in an environmental growth chamber at 25 ± 2 ºC with a L:D 16:8 photoperiod. They were placed in clear round plastic containers (18.7 cm diameter × 7.62 cm height; Pioneer Plastics, Dixon, Kentucky, USA). Each container had a polystyrene plastic vial (33.7 ml) filled with deionized water and a small cotton ball at the tip as a water source, along with an ad libitum supply of dog food (Pro Plan Puppy Sensitive Skin & Stomach Salmon & Rice Formula Dry Dog Food; Purina, Nestlé Purina PetCare Company, St. Louis, Missouri, USA) and paper towels to create a sheltered environment. Beetles remained in the environmental growth chamber for 5–20 days prior to further processing, depending on collection timing and experimental scheduling. Before experiments, P. melanarius adults were subjected to a starvation period of 48 h to standardize hunger levels. This was done by placing individual P. melanarius in tight-fitted Petri dishes (50 mm diameter × 9 mm height) with small cotton balls moistened with deionized water, and maintained in an environmental growth chamber with the same conditions described above.
Resseliella maxima were obtained from soybean plants collected from commercial fields near Luverne, Minnesota, USA and Sioux Falls, South Dakota, USA. The soybean plants were brought back to the laboratory, and what are assumed to be the third instar larvae (orange-colored) of R. maxima were collected with the help of a soft-bristled brush after dissecting the soybean stems with a scalpel (von Gries et al. 2025b). For treatments involving free larvae, stems were collected five or six days before setting up the experiment, but larvae were only extracted from the stems on the same day the experiments were set up. For production of cocooned R. maxima, stems were collected from the field 12 days before setting up the experiment. The process for obtaining R. maxima cocoons was modified from the methods described by Košťál and Havelka (2000) and Des Marteaux et al. (2012) and optimized for R. maxima (P. Anderson, unpublished data) by placing the collected larvae in polystyrene plastic vials (33.7 ml) containing moistened sand and sealing them with a plastic cap. Vials containing R. maxima were kept in environmental chambers with a temperature of 20 ± 2 ºC and a L:D16:8 photoperiod. After ten days, cocoons containing R. maxima larvae were collected from the vial by emptying its contents into a clear round plastic container and using a plastic squeeze bottle filled with deionized water to wash and separate the sand particles. The cocoons were then removed with tweezers and placed on filter paper to dry.
Anzeige
The no-choice test was performed in 9 cm Petri dishes kept on a laboratory bench at room temperature (~ 25 °C) with constant lighting. One of two prey treatments was placed in each dish: five cocooned larvae or five free larvae of R. maxima. One starved P. melanarius adult was added to each dish (Fig. 1a). The experiment was conducted over two temporal blocks, with 4–6 replications of each treatment per block for a total of ten replications of each treatment. Within each treatment, five replicates were performed with female P. melanarius adults and five with male P. melanarius adults (Lindroth 1966; von Gries et al. 2025b). The overall feeding period lasted 24 h after the addition of P. melanarius adults to the dishes, with assessment of the number of remaining cocooned larvae or free larvae recorded at 1 and 24 h by visually inspecting the Petri dishes.
Fig. 1
Experimental setup for predation trials using Pterostichus melanarius and Resseliella maxima: a No-choice test: P. melanarius adults were placed in Petri dishes with either R. maxima free larvae or cocooned larvae. b Choice test: P. melanarius adults were placed in Petri dishes and given a simultaneous choice between R. maxima free larvae or cocooned larvae. c Soil test: P. melanarius adults were placed in cups, with and without soil, containing either R. maxima free larvae or cocooned pupae, covered with a plastic sheet and secured with a rubber band
Pterostichus melanarius adults were collected, maintained and starved as described above for the no-choice test. Resseliella maxima were obtained from soybean plants collected from a commercial field near Sioux Falls, South Dakota, USA. Resseliella maxima free larvae and cocooned larvae were obtained as described above for the no-choice test.
The choice test was performed using the same Petri dish and at the same conditions described above for the no-choice test. Five cocooned larvae and five free larvae of R. maxima were placed in each Petri dish, with each prey type positioned on opposite sides of the dish. One starved P. melanarius adult was added to each dish (Fig. 1b). The experiment was conducted with a total of ten repetitions, with five repetitions having female P. melanarius adults and five having male P. melanarius adults. The total feeding period lasted for 24 h after the addition of P. melanarius adults to the dishes, with assessment of the number of remaining cocooned larvae and free larvae recorded at 1 and 24 h by visually inspecting the Petri dishes.
Soil test
Pterostichus melanarius adults were collected from a commercial soybean field near Luverne, Minnesota, USA in June of 2024, and maintained and starved as described above for the no-choice test. Resseliella maxima were obtained from soybean plants from a laboratory colony of R. maxima maintained at the University of Minnesota, USA. Resseliella maxima larvae were collected from soybean stems on the same day the experiments were set up, following the methods described above for the no-choice test. For production of R. maxima cocoons, stems were obtained from the colony 12 days before setting up the experiment. The process for obtaining R. maxima cocoons was carried out as described previously in the no-choice test. The cocoons used in this study contained R. maxima pupae, likely because the larvae collected from the laboratory colony had not been exposed to overwintering cues and therefore continued development to the pupal stage (in contrast to the field-collected individuals which would have likely ceased development in the overwintering stage [cocooned larvae]).
The experiment was performed in 266.16 ml (88.9 mm top diameter × 57.15 mm bottom diameter × 101.6 mm height) clear plastic cups (Clear cups, Great Value, USA), closed on top using a 15 cm square clear plastic sheet, cut from a zip-top storage bag, secured with a rubber band. Soil used as substrate was collected from the same field from which P. melanarius were collected. The soil was dried for 48 h in a chamber at 60 °C and then sifted (sieve number 20, 0.84 mm) to remove any material larger than the prey. Before setting up the experiment, water was added to moisten the soil: 520 ml of water for every 2 kg of soil. In this experiment, five treatments were tested: (1) cocoons with no soil, (2) cocoons placed on the surface of the soil, (3) cocoons placed 1 cm deep in the soil, (4) free larvae with no soil, and (5) free larvae with soil. Five individual prey were used in each arena. In treatments with soil as substrate, a 3 cm deep layer of soil was used in each arena. For the treatment using free larvae with soil, larvae were placed on the surface of the soil because they typically burrow into the soil, and do not remain on the surface like the cocoons. For the treatment with cocoons 1 cm into the soil, a 2 cm deep layer of soil was initially added in the cup, the cocoons were placed on the surface of this layer, and the remaining 1 cm deep layer of soil was added after the cocoons were placed. One P. melanarius was placed into each arena and they were closed on top as described above (Fig. 1c). The experiment was performed with 20 arenas (i.e., repetitions) of each of the five treatments. To assess the effectiveness of recovering cocoons and free larvae from the soil, five additional predator-free replicates of cocoons (buried at 1 cm) and of free larvae were also conducted, but not included in statistical analyses. Five individuals were placed in each of these replicates, and all individuals were recovered after 24 h.
The arenas were kept in a controlled environment, with a temperature of 26 ± 2 ºC and a L:D16:8 photoperiod. After 24 h, P. melanarius were removed from each arena, and prey consumption was evaluated by quantifying the remaining R. maxima. Quantification was done by transferring the soil to a sieve (sieve number 20, 0.84 mm) and washing the soil with deionized water until only R. maxima remained in the sieve. All remaining R. maxima for each repetition were examined under a microscope to determine if the cocoons were open and/or if the larvae were partially consumed. Resseliella maxima that were missing or partially consumed were considered eaten.
Statistical analysis
For the no-choice test, the proportion of R. maxima consumed by P. melanarius adults was analyzed separately for 1- and 24-h time assessments with bias-reduced (package brglm2 version 0.9.2, method = brglmFit, Kosmidis 2023) generalized linear models with a Binomial distributions and a logit link function (package stats version 4.3.2, function glm; R Core Team 2025). The proportion of R. maxima consumed was used in the model as the response variable and stage (free larvae versus cocooned larvae) was included as a fixed factor. The significance of estimates was obtained with a Type II Wald χ2 test (package car version 3.1–2, function Anova; Fox and Weisberg 2019), and model fit and presence of influential observations (outliers) were verified visually with diagnostic plots (package performance version 0.10.9, function check_model; Lüdecke et al. 2021). The presence of one influential observation was detected for 24 h and therefore this replicate was removed from all analyses. Models followed assumptions after removal of the outlier.
For the choice test, the difference in consumption between the number of R. maxima free larvae and the number of cocooned larvae by P. melanarius adults was tested against 0 with a Wilcoxon signed rank test (package stats version 4.5.2, function wilcox.test: R Core Team 2025), because the assumption of normality was violated for the 24 h assessment. The assumption of normality was assessed with a Shapiro–Wilk normality test (package rstatix version 0.7.2, function shapiro_test; Kassambara 2023).
For the soil test, the proportion of R. maxima consumed by P. melanarius adults was analyzed with bias-reduced (package brglm2 version 0.9.2, method = brglmFit; Kosmidis 2023) generalized linear models with Bbinomial distributions and a logit link function (package stats version 4.3.2, function glm; R Core Team 2025). The proportion of R. maxima consumed was used in the model as the response variable and treatment was included as a fixed factor. The significance of estimates was obtained with a Type II Wald χ2 test (package car version 3.1–2, function Anova; Fox and Weisberg 2019) and model fit was verified visually with diagnostic plots (package performance version 0.10.9, function check_model; Lüdecke et al. 2021). Furthermore, pairwise comparisons of treatments were conducted using estimated marginal means with Tukey’s adjustment (p < 0.05) (package emmeans version 1.8.9; Lenth 2023).
Results
No-choice test
Pterostichus melanarius adults consumed both stages (i.e., free and cocooned larvae) of R. maxima. Under laboratory conditions, we observed P. melanarius adults detecting R. maxima cocoons, opening them, and feeding on the larvae. An observed P. melanarius adult grasped the cocoon with its mandibles and, using its anterior tarsi for support, opened the cocoon to feed on the larva inside. In some cases, parts of the cocoon remained intact, but the larva was fully consumed. Occasionally, P. melanarius bit into the cocoon, and consumed both the silk and the larva. In this case, the only material left behind was the sand from the cocoon’s exterior.
After one hour, P. melanarius adults ate significantly (χ2 = 5.77, df = 1, p = 0.016) more free larvae (40.00 ± 13.66%) than cocooned larvae (17.77 ± 11.76%) (Fig. 2a), with seven P. melanarius adults eating free larvae and two eating cocooned larvae. In contrast, after 24 h, P. melanarius adults ate significantly (χ2 = 5.65, df = 1, p = 0.017) more cocooned larvae (100.00 ± 0.00%) than free larvae (90.00 ± 5.37%) (Fig. 2b). All P. melanarius adults consumed at least one prey within 24 h.
Fig. 2
Percentage of Resseliella maxima free larvae (“larvae”) and cocooned larvae (“cocoons”) consumed by Pterostichus melanarius adults in a no-choice test at 1 h (a) and 24 h (b). Boxplots show the median (horizontal line), interquartile range (box), and minimum and maximum values (whiskers). Individual points represent replicate observations. Different lowercase letters indicate significant differences between prey stages within each time period (p < 0.05)
When given the choice between free larvae and cocooned larvae of R. maxima as prey (Fig. 3), P. melanarius adults consumed both stages but ate significantly more free larvae (78.00 ± 7.57%) than cocooned larvae (34.00 ± 13.35%) after one hour (Wilcoxon signed rank test, W = 40, p = 0.043). Ten P. melanarius adults were used in the test, and all of them consumed free larvae, while only six ate cocooned larvae during the first hour. After 24 h, there was no significant difference in consumption between free larvae (98.00 ± 2.00%) and cocooned larvae (70.00 ± 13.08%) (Wilcoxon signed rank test, W = 15, p = 0.058). However, after 24 h, all P. melanarius adults consumed free larvae, and only eight of them consumed cocooned larvae, with the data indicating a trend towards a higher consumption of free larvae.
Fig. 3
Consumption of Resseliella maxima free larvae (“larvae”) and cocooned larvae (“cocoons”) by Pterostichus melanarius adults in a choice test at 1 h and 24 h. Boxplots show the median (horizontal line), interquartile range (box), and minimum and maximum values (whiskers). “ns” indicates a non-significant difference (p > 0.05), while an asterisk (*) indicates a significant difference (p < 0.05) when comparing the mean difference in consumption to zero within each assessment time (1 h and 24 h). Values above zero indicate that beetles consumed more larvae, values below zero indicate that more cocoons were consumed, and zero indicates no preference. The size of each point represents the total number of prey consumed by each beetle
Pterostichus melanarius adults consumed both life stages (i.e., free larvae and cocooned pupae) of R. maxima within 24 h in all the treatments tested (Fig. 4). Our results showed a significant difference in consumption among treatments (χ2 = 118.91, df = 4, p < 0.001). The highest consumption occurred for free larvae without soil (56.00 ± 7.20%). The second highest consumption occurred for cocooned pupae without soil (21.00 ± 8.27%), but this did not significantly differ from the consumption of cocooned pupae on the soil surface (7.00 ± 2.19%) or free larvae with soil (7.00 ± 2.63%). The lowest consumption occurred for cocooned pupae placed 1 cm deep in the soil (2.00 ± 1.38%), but this did not differ from the consumption of cocooned pupae on the soil surface or larvae with soil. The majority of the free larvae used as prey burrowed in the soil and formed cocoons during the 24 h duration of the experiment.
Fig. 4
Percentage of Resseliella maxima free larvae (‘larvae’) and cocooned pupae (‘cocoons’) consumed by Pterostichus melanarius adults with or without soil, and either on the soil surface or buried. Consumption was recorded after 24 h. Boxplots show the median (horizontal line), interquartile range (box), and minimum and maximum values (whiskers). Different lowercase letters indicate significant differences among treatments (p < 0.05)
Biological control is an important method in integrated pest management that utilizes natural enemies to control pest populations (van den Bosch et al. 1982; Waage and Greathead 1998). This method can be valuable in managing pests like R. maxima, where other effective practical methods for controlling the pest are limited. This study explored the potential of P. melanarius adults as a biological control agent for R. maxima by assessing their ability to prey on multiple life stages of the pest.
Previously, predation of R. maxima larvae by P. melanarius adults was examined (Melotto et al. 2023c; von Gries et al. 2025b), but it was unclear if they consumed other stages such as cocooned larvae or cocooned pupae. The results presented here confirm that P. melanarius adults can indeed prey on larval and cocooned stages (both larvae and pupae) of R. maxima, indicating a broader predatory scope. This finding aligns with the known behavior of the genus Pterostichus, which seems capable of consuming any prey of a size they could ingest (Hengeved 1980). The consumption of cocooned insects by Pterostichus spp. was previously observed by Epstein et al. (2001), where both P. melanarius and Pterostichus adstrictus E. fed on cocooned larvae of Cydia pomonella L. (Lepidoptera: Tortricidae).
While P. melanarius is capable of consuming cocooned prey, several factors may influence the likelihood and efficiency of predation. The ability of a generalist predator to attack its prey depends on multiple factors, including its capacity to detect and access the prey, and how easily the prey can be consumed (Guershon and Gerling 1999; Eubanks and Denno 2000; Desneux and O’Neil 2008). Cocoons often serve to protect larvae or pupae from predatory attacks (Censier et al. 2014). The lower consumption of cocooned larvae compared to free larvae of R. maxima suggests that cocoons may reduce prey accessibility or detectability. This likely explains why a significantly higher number of free larvae were consumed during the first hour in the no-choice test where beetles were offered only one prey type.
However, the significantly higher consumption of cocooned larvae after 24 h in the no-choice test may be related to learning abilities of insects (Alloway 1972; Dukas 2008; Giurfa 2015). Reznikova and Dorosheva (2013) described catalog learning in carabids, where beetles optimize existing behaviors based on past successes. In addition, Plotkin (1979) demonstrated that P. melanarius uses odor cues to guide their behavior, associating specific scents with prey or resources. Similarly, if larvae or pupae of R. maxima emit olfactory cues, it is possible that adults of P. melanarius could learn to associate these signals with the prey, increasing consumption of cocooned prey over time. Furthermore, in the context of cocoons, P. melanarius might initially engage in various exploratory behaviors and, upon success (i.e., breaking a cocoon and finding prey), select and repeat the successful pattern more consistently over time.
In the choice test, when both stages of R. maxima were offered to the P. melanarius adults simultaneously, there was greater consumption of free larvae at both 1 and 24 h. However, the difference was not statistically significant at 24 h. In a previous food preference study, Pterostichus globosus F. tended to select prey items that offered higher energy intake relative to the handling time required (Dinis et al. 2016). Thus, comparing the time and effort required for P. melanarius to find and open a cocoon with the time needed to locate and consume free larvae, feeding on the larvae appears to be more cost-efficient which may explain why P. melanarius initially exhibited a preference for consuming the free larvae over the cocooned R. maxima.
For the soil test, P. melanarius consumed significantly more free larvae without soil compared to cocooned pupae without soil. When soil was present, the consumption rates were lower when compared with the treatments without soil, which suggests that P. melanarius could have difficulty locating or handling R. maxima when they are in contact with soil, even when the prey is on the soil surface. Lee and Edwards (2012) observed that carabid beetles, including P. melanarius, showed reduced predation when prey were buried at depths of 1.3 or 5 cm, or when the prey had burrowed into the soil of potted strawberry plants. Similarly, Kulkarni et al. (2015) demonstrated that P. melanarius consumed a higher number of weed seeds located on or close to the soil surface (0.5 cm deep) as compared to those located farther below the surface. These findings highlight how studies conducted without any soil or other substrate might overestimate a predator's potential for biological control. Therefore, the finding that P. melanarius adults can locate and consume cocooned R. maxima buried in soil, even at a low rate, is important, especially considering that the cocoon provides an additional layer of protection for the prey.
Although laboratory experiments do not fully replicate field conditions, the findings of this study indicate that predation by P. melanarius may occur on the soil surface, and, to a lesser extent, even after the larvae enter the soil and form a cocoon. Renkema et al. (2012) showed that ground predators, including P. melanarius, contributed to mortality of blueberry maggot, Rhagoletis mendax Curran (Diptera: Tephritidae), a pest of similar size to R. maxima, on bare soil in a blueberry (Vaccinium corymbosum L.; Ericales: Ericaceae) field. A previous study observed P. melanarius feeding on wandering C. pomonella larvae searching for pupation sites in an apple (Malus domestica Borkh; Rosales: Rosaceae) orchard in England (Glen and Milsom 1978). In the field, R. maxima larvae leave the plants once they reach maturity to pupate in the soil (McMechan et al. 2021b). This is likely an important moment where P. melanarius could consume R. maxima larvae, but R. maxima larval behavior after leaving the plant to pupate is still not well known. Based on the results of this study, if larvae burrow rapidly into the soil, they may potentially evade predation by P. melanarius adults. However, it remains unknown whether P. melanarius larvae prey on R. maxima larvae or cocoons in the soil.
When comparing the results of the no-choice test to those of the soil test treatments without soil, we observed higher levels of prey consumption in the no-choice test (100% of cocooned larvae and 90% of free larvae consumed) compared to the soil test (21% of cocooned pupae and 56% of free larvae consumed), despite these treatments being similar. This difference in consumption, whether for cocooned prey or free larvae, could be explained by potential prior exposure of the predators to the prey. For the no-choice test, P. melanarius adults were collected later in the 2023 season (July and August), while, for the soil test, they were collected earlier in the 2024 season (early June). It is possible that P. melanarius adults used in the no-choice test had prior (and/or greater) exposure to R. maxima in the field before collection. Furthermore, the cocoons contained different life stages in the two experiments. In the no-choice test, cocooned larvae were used, whereas cocooned pupae were used in the soil test. Behavioral variation or differences in predatory cues can occur due to different life stages of prey (Pote and Nielsen 2017), which may have influenced predation outcomes in the cocooned prey treatments across the two tests. Although the slightly higher temperature during the soil test could have influenced predation rates, beetle collection dates and the developmental stage of the prey likely had a stronger effect.
The ability of P. melanarius to prey on R. maxima cocooned larvae and pupae is a significant finding, as the cocoon stage remains exposed outside the plant and in the soil for an extended period of time, making it a potential target for biological control. However, further studies are needed to assess the duration of exposure for each R. maxima stage and the likelihood of P. melanarius adults preying on them in a more natural setting.
Acknowledgements
The authors thank Juliana Lopes dos Santos for help with evaluations.
Declarations
Conflict of interests
The authors have no competing interests to declare that are relevant to the content of this article.
Ethical approval
This work does not contain any studies with human participants or animals (vertebrates).
Consent for publication
All authors gave consent to the publication of this work.
Informed consent
Informed consent was not applicable to this work.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Regina Stacke
is a researcher in the Department of Entomology at the University of Minnesota, USA. Her research focuses on integrated pest management, with an emphasis on biological and chemical control, and she has a special interest in insect colony development and maintenance.
Sarah von Gries
is a PhD candidate in Entomology at the University of Minnesota, USA. Her research focuses on the biological control of soybean gall midge, with an emphasis on parasitoid–host interactions, predator-prey interactions, and landscape ecology.
Arthur Vieira Ribeiro
is a researcher in the Department of Entomology at the University of Minnesota, USA. His research focuses on multiple aspects of applied ecology and integrated pest management.
Pheylan Anderson
is a PhD candidate in Entomology at the University of Minnesota, USA. He studies population ecology and basic biology of soybean gall midge, focusing on longevity and development, cold tolerance, and sampling methodology.
Amelia Lindsey
is an associate professor in the Entomology Department at the University of Minnesota, USA. Her research primarily focuses on symbiosis and reproduction in insects, and she collaborates on a suite of projects related to biological control.
Robert Koch
is a professor and extension specialist in the Department of Entomology at the University of Minnesota, USA. His research addresses various aspects of applied ecology and integrated pest management of soybean insects.
Alloway TM (1972) Learning and memory in insects. Annu Rev Entomol 17:43–56CrossRef
Busch AK, Wham BE, Tooker JF (2021) Life history, biology, and distribution of Pterostichus melanarius (Coleoptera: Carabidae) in North America. Environ Entomol 50:1257–1266CrossRefPubMed
Censier F, Chavalle S, Knor S, De Proft M, Bodson B, Skuhravá M (2014) Unusual occurrence of cocoons in population of Haplodiplosis marginata (Diptera: Cecidomyiidae) in Belgium. J Insect Sci 14:239CrossRefPubMedPubMedCentral
Cooper VM, McMechan AJ (2024) Evaluation of timed foliar insecticide applications against soybean gall midge, 2020. Arthropod Manag Tests 49:tsae114CrossRef
Desneux N, O’Neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res 98:631–639CrossRefPubMed
Dinis AM, Pereira JA, Benhadi-Marín J, Santos SAP (2016) Feeding preferences and functional responses of Calathus granatensis and Pterostichus globosus (Coleoptera: Carabidae) on pupae of Bactrocera oleae (Diptera: Tephritidae). Bull Entomol Res 106:701–709CrossRefPubMed
Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160CrossRefPubMed
Epstein DL, Zack RS, Brunner JF, Gut L, Brown JJ (2001) Ground beetle activity in apple orchards under reduced pesticide management regimes. Biol Control 21:97–104CrossRef
Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25:140–146CrossRef
Fox J, Weisberg S (2019) An R companion to applied regression, Third edition. Sage, Thousand Oaks CA. https://www.john-fox.ca/Companion/.
Gagné RJ, Yukawa J, Elsayed AK, McMechan AJ (2019) A new pest species of Resseliella (Diptera: Cecidomyiidae) on soybean (Fabaceae) in North America, with a description of the genus. Proc Entomol Soc Wash 121:168–177CrossRef
Giurfa M (2015) Learning and cognition in insects. Wires Cognit Sci 6:383–395CrossRef
Glen DM, Milsom NF (1978) Survival of mature larvae of codling moth (Cydia pomonella) on apple trees and ground. Ann Appl Biol 90:133–146CrossRef
Guershon M, Gerling D (1999) Predatory behavior of Delphastus pusillus in relation to the phenotypic plasticity of Bemisia tabaci nymphs. Entomol Exp Appl 92:239–248CrossRef
Gupta P, McMechan AJ (2025) Impact of hilling timing on soybean gall midge (Diptera: Cecidomyiidae) abundance, plant injury, and yield. J Econ Entomol 118:724–731CrossRefPubMedPubMedCentral
Helton ML, Tinsley NA, McMechan AJ, Hodgson EW (2022) Developing an injury severity to yield loss relationship for soybean gall midge (Diptera: Cecidomyiidae). J Econ Entomol 115:767–772CrossRefPubMed
Hengeveld R (1980) Polyphagy, oligophagy and food specialization in ground beetles (Coleoptera, Carabidae). Neth J Zool 30:564–584CrossRef
Hodgson EW, Helton M (2021) Soybean gall midge efficacy, 2020. Arthropod Manag Tests 46:tsab010CrossRef
Košťál V, Havelka J (2000) Diapausing larvae of the midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae) survive at subzero temperatures in a supercooled state but tolerate freezing if inoculated by external ice. Eur J Entomol 97:433–436CrossRef
Kulkarni SS, Dosdall LM, Spence JR, Willenborg CJ (2015) Depth of seed burial and gender influence weed seed predation by three species of ground beetle (Coleoptera: Carabidae). Weed Sci 63:910–915CrossRef
Lee JC, Edwards DL (2012) Impact of predatory carabids on below- and above-ground pests and yield in strawberry. BioControl 57:515–522CrossRef
Lindroth CH (1966) The ground-beetles (Carabidae, excl. Cicindelinae) of Canada and Alaska, Part 4. Opusc Entomol, Supplementum 29:409–648
Lüdecke D, Ben-Shachar M, Patil I, Waggone P, Makowski D (2021) performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6:3139CrossRef
Marteaux LED, Habash MB, Schmidt JM, Hallett RH (2012) A method for induction and quantification of diapause entry in the swede midge (Diptera: Cecidomyiidae). Can Entomol 144:792–800CrossRef
McMechan AJ (2021) Evaluation of at-planting soil treatment Thimet against soybean gall midge, 2020. Arthropod Manag Tests 46:tsab062CrossRef
McMechan AJ, Hodgson EW, Varenhorst AJ, Hunt T, Wright R, Potter B (2021a) Soybean gall midge (Diptera: Cecidomyiidae), a new species causing injury to soybean in the United States. J Integr Pest Manag 12:8CrossRef
McMechan AJ, Schroeder de Souza J, Umezu N, Gupta P, Carmona GI (2023) Hilling as a cultural control strategy for soybean gall midge (Diptera: Cecidomyiidae). J Econ Entomol 116:2009–2013CrossRefPubMedPubMedCentral
McMechan AJ, Hunt T, Wright R (2021b) Soybean gall midge in Nebraska. Eastern Nebraska Research, Extension and Education Center. https://digitalcommons.unl.edu/enrec/2
Melotto G, Awad J, Talamas EJ, Koch RL, Lindsey ARI (2023a) Synopeas maximum Awad & Talamas (Hymenoptera, Platygastridae): a new species of parasitoid associated with soybean gall midge, Resseliella maxima Gagné (Diptera, Cecidomyiidae). J Hymenopt Res 96:181–205CrossRef
Melotto G, Potter BD, Koch RL, Lindsey ARI (2023b) Spatial and temporal dynamics of soybean gall midge (Resseliella maxima) parasitism by Synopeas maximum. Pest Manag Sci 79:5096–5105CrossRefPubMed
Melotto G, Potter BD, Lindsey ARI, Koch RL (2023c) Arthropod predator community associated with soybean gall midge, Resseliella maxima (Diptera: Cecidomyiidae), in Minnesotan soybean fields. Environ Entomol 52:990–997CrossRefPubMed
Montenegro VM, Jorgenson D, McMechan AJ (2022) Evaluation of foliar treatments against soybean gall midge, 2020. Arthropod Manag Tests 47:tsac080CrossRef
Plotkin HC (1979) Learning in a carabid beetle (Pterostichus melanarius). Anim Behav 27:567–575CrossRef
Pollet M, Desender K (1985) Adult and larval feeding ecology in Pterostichus melanarius Ill. (Coleoptera, Carabidae). Meded Fac Landbouwwet Rijksuniv Gent 50:581–594
Pote JM, Nielsen AL (2017) Life stage specific predation of Halyomorpha halys (Stål) by generalist predators. Biol Control 114:1–7CrossRef
R Core Team (2025) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Renkema JM, Lynch DH, Cutler GC, MacKenzie K, Walde SJ (2012) Predation by Pterostichus melanarius (Illiger) (Coleoptera: Carabidae) on immature Rhagoletis mendax Curran (Diptera: Tephritidae) in semi-field and field conditions. Biol Control 60:46–53CrossRef
Reznikova Z, Dorosheva E (2013) Catalog learning: carabid beetles learn to manipulate with innate coherent behavioral patterns. Evol Psychol 11:513–537CrossRefPubMedCentral
Sever M (2021) Soybean gall midge: how do you solve a problem you know little about? Crops Soils 54:38–43CrossRef
van den Bosch R, Messenger PS, Gutierrez AP (1982) The nature and scope of biological control. In: van den Bosch R, Messenger PS, Gutierrez AP (eds) An introduction to biological control. Springer, US, Boston, MA, pp 1–7CrossRef
von Gries SC, Awad J, Talamas EJ, McMechan AJ, Lindsey ARI, Koch RL (2025a) Synopeas ruficoxum Buhl (Hymenoptera, Platygastridae) is a natural enemy of soybean gall midge, Resseliella maxima Gagné (Diptera, Cecidomyiidae). J Hymenopt Res 98:721–742CrossRef
von Gries SC, Lindsey ARI, Koch RL (2025b) Predation behaviors of Pterostichus melanarius adults on larvae of the soybean gall midge, Resseliella maxima. Biol Control 200:105679CrossRef
Waage JK, Greathead DJ (1998) Biological control: challenges and opportunities. Philos Trans R Soc Lond B Biol Sci 318:111–128CrossRef
