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Predation Response of Macrolophus caliginosus Wagner (Hemiptera: Heteroptera: Miridae) Across Multiple Prey Density Levels of Aphis craccivora Under Fixed Temperature Conditions
This study investigates the predation response of Macrolophus caliginosus, a predatory insect crucial in biological pest control, to varying densities of Aphis craccivora under fixed temperature conditions. The research reveals that predation rates increase with prey density but are significantly influenced by temperature and the predator's developmental stage. At lower temperatures (20°C), predation rates consistently rise with increasing prey density, with early nymphal instars showing the highest consumption rates. However, at 25°C, predation rates become more irregular, indicating a potential reduction in efficiency. At higher temperatures (30°C), predation rates fluctuate more dynamically, with peak consumption observed in the fourth instar at the highest prey density. The study also examines functional response parameters, including handling time and search rate, which vary across temperatures and instars. These findings highlight the adaptability of M. caliginosus to environmental changes and underscore its potential as a reliable biological control agent. The research provides valuable insights into improving pest management strategies in dynamic climatic conditions, emphasizing the importance of considering prey availability and composition in biological control programs.
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Abstract
Macrolophus caliginosus Wagner (Hemiptera: Heteroptera: Miridae), a predatory bug widely used in biological control against whiteflies and spider mites, also shows strong efficiency on aphids, with females consuming on average ~43.2 first-instar Aphis gossypii nymphs per day under laboratory conditions. This study evaluates the predation capacity and functional response of M. caliginosus to varying densities of Aphis craccivora, aiming to assess its potential as a biological control agent against this significant agricultural pest. The research examines how each instar’s predation rate responds to three temperatures (20 °C, 25 °C, and 30 °C) and five prey density levels (5, 10, 15, 20, and 25). Predation rates were measured by exposing individual predators to different prey densities and recording the number of aphids consumed daily. Functional response parameters, including handling time (Th), search rate (α), and the average number of prey killed (Ha), were calculated using Holling’s disc equation. This study is a laboratory-based investigation conducted under controlled conditions. Macrolophus caliginosus nymphs showed a clear Type II functional response against Aphis craccivora, with first instars exhibiting the highest predation efficiency, consuming significantly more aphids than older instars, At 20 °C, predation capacity increased with prey density, peaking in the first instar and declining in later instars; at 25 °C, consumption patterns fluctuated, with reduced efficiency in higher instars; and at 30 °C, predation rates varied, with some instars showing improved efficiency. Functional response parameters revealed that the first instar had the shortest handling time at 20 °C, indicating high efficiency, while efficiency decreased at 25 °C and improved at 30 °C. The second instar showed enhanced predation at 25 °C but slightly reduced efficiency at 30 °C. The third instar exhibited high efficiency at 20 °C, declined at 25 °C, and partially recovered at 30 °C. The fourth instar consistently had the lowest predation rates and longest handling times across temperatures, improving efficiency at 30 °C; These findings underscore the interplay of temperature, prey density, and predator instars in determining predation rates. The data highlights the adaptability of M. caliginosus to environmental changes, providing critical insights for applications in biological pest control under varying climatic conditions.
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Introduction
Macrolophus caliginosus Wagner (Hemiptera: Heteroptera: Miridae), a predatory insect from the Miridae family, is a key agent in biological pest control due to its polyphagous nature. This species preys on a wide range of insect pests, making it a valuable component of integrated pest management (IPM) strategies (Embaby et al. 2024). M. caliginosus is an effective biological control agent against whiteflies, with a 27.6-day life cycle, a predation rate of 5.94 larvae per day, and the ability to produce 51 progeny in 30 days, while its effectiveness improves when combined with other control methods. Additionally, the predatory bug exhibited varying developmental times, adult longevity, and consumption rates depending on prey type, with silverleaf whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) eggs being the most favourable, highlighting its potential for biological pest control, particularly in tomato crops (Mohd et al. 2009; Embaby et al. 2024). The functional response of M. caliginosus to prey density has been extensively studied. It exhibits a Type II functional response when preying on Aphis craccivora, where predation rates increase with prey density but eventually plateau due to handling time constraints (Lenteren and Bakker 1975). In some cases, M. caliginosus exhibits a Type III functional response, characterised by an accelerating predation rate at low prey densities and stabilization at higher densities (Holling 1959a; Shah and Khan 2013). Studies have shown that M. caliginosus exhibits this type of response when preying on species like green peach aphid Myzus persicae (Sulzer)(Hemiptera: Aphididae) and spider mite Tetranychus urticae (Acari: Tetranychidae) (Hamdan 2006; El Kenway et al. 2022). Laboratory studies have revealed that M. caliginosus can consume an average of 5.94 prey items per day across various stages of whiteflies and aphids, with consumption rates reaching up to 75 first-instar whiteflies in 24 h under high prey densities (Sharifian et al. 2017). When presented with mixed prey, it preferentially targets older nymphs of B. tabaci and shows a preference for Trialeurodes vaporariorum over B. tabaci, unless the latter constitutes more than 75% of the available prey (Castañé and Zapata 2006). Such selective feeding behaviour can significantly impact pest population dynamics and the efficacy of other natural enemies, such as parasitoids, targeting the same pests. Additionally, laboratory studies have demonstrated that M. caliginosus effectively preys on A. raciborski, with optimal predation occurring at specific prey densities (Yiacoumi et al. 2024). These preferences highlight the importance of considering prey availability and composition when deploying M. caliginosus in biological control programs. The predation capacity of M. caliginosus is strongly influenced by prey density. Research has shown that females consume more prey at higher densities, with maximum consumption rates reaching approximately 166 whitefly eggs per day and 111 spider mite eggs per day under optimal conditions (Fauvel et al. 1987). High predator densities, however, can reduce per capita predation rates due to increased intraspecific interactions, which may interfere with foraging efficiency (Castañé and Zapata 2006). Optimal predation capacity is achieved at moderate temperatures, with peak performance at around 25 °C (Maselou et al. 2015). By reducing A. craccivora populations at higher densities, M. caliginous contributes to ecosystem stability and demonstrates its potential as a reliable biological control agent (Zhang et al. 2018; Enkegaard et al. 2001). Recently, Integrated Pest Management (IPM) strategies in tomato cultivation have gained attention, prompting researchers to investigate the use of Miridae bugs to enhance predator densities and suppress populations of tomato whitefly and other insect pests below economic thresholds (Mohd et al. 2009). The role of generalist natural enemies in biological control has also received increased focus (Symondson et al. 2002; Janssen and Sabelis 2015), leading to a preference for generalist predatory bugs over specialists in aphid management. Ongoing research has evaluated various predatory bugs for their effectiveness in aphid control in sweet pepper, with mirid bugs demonstrating superior performance compared to anthocorid bugs. Among these, Macrolophus pygmaeus Rambur (Heteroptera: Miridae) and Nesidiocoris tenuis have shown promising results. Macrolophus pygmaeus, particularly when supported with weekly supplemental food, was identified as the most effective mirid predator in reducing aphid populations in sweet pepper when released prior to infestation (Perdikis and Lykouressis 2004; Messelink et al. 2011, 2014). Nesidiocoris tenuis, Macrolophus pygmaeus, and Dicyphus maroccanus effectively located, preyed upon, and significantly reduced populations of M. persicae in sweet pepper, demonstrating their strong potential for biological control (Pérez-Hedo and Urbaneja 2015; Bouagga et al. 2018; Martínez-García et al. 2017). This study aims to evaluate the predation capacity and functional response of the predatory bug M. caliginosus when exposed to varying densities of A. craccivora under different temperature conditions. By examining the predation capacity and the functional response type, the research seeks to understand the predator’s potential as a biological control agent against A. craccivora, a significant agricultural pest.
Materials and Methods
Aphid Rearing
The cowpea aphid (Aphis craccivora) was reared in the laboratory on Faba bean plants (Vicia faba) maintained in pots under controlled environmental conditions at 25 ± 2 °C, 60 ± 5% RH, and a 12:12 L:D photoperiod. Aphid colonies were established by collecting infested plants from the field located in Giza Governorate, Egypt (30°00′N, 31°12′E), during the spring growing season of 2024. and transferring aphids to healthy, pesticide-free cowpea plants. To maintain the colony, infested plants were kept in wooden cages (60 × 60 × 60 cm)covered with muslin cloth, allowing for ventilation and preventing contamination. nymphs of known age (0–12 h old) were obtained by confining adult aphids on fresh Faba bean leaf discs placed on moistened sponges inside Petri dishes (3 cm diameter) with perforated lids to allow gas exchange. Leaf discs (3 cm diameter) were replaced regularly every two days to ensure a fresh food supply and prevent wilting. Daily monitoring of aphid development, survival, and reproduction was conducted to maintain colony health and consistency across generations.
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Predator Rearing
Macrolophus caliginosus was reared in the Biological Control Research Department, Plant Protection Research Institute, Agricultural Research Center (ARC), Giza, Egypt.under controlled conditions at 25 ± 2 °C, 60 ± 5% RH, and a 12:12 L:D photoperiod. To determine the predator, sixteen walk-in cages measuring 7.5 m3 (2.5 m × 1.5 m × 2 m) were used, each containing four Faba bean plants(Vicia faba) . Flowers and buds were removed from the plants to prevent predators from accessing alternative food sources. The female of M. caliginosus oviposits in the tissue of the leaf, vein or stalk of Faba bean plants. For this reason, after 48 h, plants were cut into small parts, and the pieces were placed on acalypha plants Acalypha indica L. situated on saturated cotton pads inside Petri dishes (10 cm in diameter) for 5–6 days until the first newly hatched nymphs emerged.
Fresh nymphs aged 0–3 days were collected from the mass-rearing colony and maintained until adulthood. Predators were provided with suitable prey of A. craccivora to support development and reproduction. successive generations were maintained to ensure a stable laboratory population. Environmental conditions, including temperature, relative humidity, and photoperiod, were kept constant to minimize variability. Regular monitoring of developmental time, fecundity, and survival rates was performed over 3 generations to assess colony health and consistency across generations, thereby ensuring the reliability and reproducibility of experimental results.
Effect of Prey Density and Predation Rate
Prey was provided at densities of 5, 10, 15, 20, and 25 individuals per dish, with five replicates per density, each corresponding to a single predator. The experiment was conducted at three different temperatures (20 °C, 25 °C, and 30 °C) for all prey density levels. The selection of temperature points (20 °C, 25 °C, and 30 °C) was based on several considerations relevant to the biology and ecology of M. caliginosus (Hart et al. 2002). First, these temperatures represent a gradient commonly experienced by the insect in its natural environment, particularly in protected horticultural crops where it is frequently employed for pest control. The range is also relevant because the optimal temperatures for Macrolophus pygmaeus, a similar species, are above 20 °C, with lower temperatures significantly slowing down development (Perdikis and Lykouressis 2002). Moreover, 25 °C is commonly used in rearing Macrolophus caliginosus, and previous studies (Hart et al. 2002) maintained cultures at 25 °C as a standard condition, where development, survival, and predation rates are favorable.
Prey consumption was assessed using a binocular stereoscope on the first day of observation. Following data collection, consumed prey was removed, and prey density was maintained by replenishing the required number of individuals. Experiments were conducted using mixed nymphal instars of A. craccivora, with early instars predominating, to simulate natural prey availability in the field. Each replicate commenced with the first nymphal instar of the predator and continued until the fourth nymphal instar. Completely consumed aphids were identified by their shrivelled remains, with only the exoskeleton left after predation. Control groups without predators, consisting of ten replicates and were maintained under the same spatial and temporal conditions as the treatment groups to ensure consistency. The nymphal instars of M. caliginosus were identified based on body size and morphological characters under a stereomicroscope. First instars are the smallest, pale green, and lack wing pads; second instars are larger with slightly elongated bodies; third instars show visible wing pad initiation; fourth instars have clearly developed wing pads covering about half of the abdomen; and fifth instars possess large wing pads extending close to the abdominal apex (Hart et al. 2002; Alomar et al. 2006).Specifically, for each instar and temperature combination tested (20 °C, 25 °C, and 30 °C), corresponding control replicates were established simultaneously and under identical environmental parameters.
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Aphid mortality was assessed 24 h after predator introduction, categorizing killed individuals as either “partially consumed” or “killed but unconsumed.” Fully consumed aphids were distinguished from those showing minimal consumption (less than 1/10 of their body). Following (Samu and Biro 1993), prey with less than 1/3 of their body consumed were classified as partially consumed. Unconsumed but killed aphids were identified by slight body deformation, darkening, and the presence of exudate on the siphunculi, indicating predator attack. The duration of observations depended on the developmental stage and individual longevity of the predator, and continued until the death of all individuals, which in some cases extended for several weeks.The Direct Consumption Count method is one of the simplest ways to calculate predation rates, where the total number of preys consumed by a predator over a fixed period (e.g., 24 h) is recorded and used to determine predation capacity (Holling 1959b). This method provides a straightforward estimate of predation rates and has been widely applied in controlled laboratory experiments to assess predator-prey interactions (Murdoch and Oaten 1975).
Functional Response Tests
The functional response of predators to different prey densities was expressed by fitting the data to Holling’s equation (Holling 1959a; El Kenway et al. 2021)
Where: Na defines the number of prey attacked by a predator per time unit, α is the search rate of a predator, T is the total time of exposure (1 day in this experiment), N is the original number of prey items offered to each predator at the beginning of the experiment, and Th is handling time for each prey caught (proportion of the exposure time that a predator spends in identifying, pursuing, killing, consuming prey).
The attack rate (α) quantifies the efficiency of prey discovery and attack: higher values reflect more effective searching ability. The handling time (Th) sets the upper limit of consumption, calculated as 1/𝑇ℎ. Since experiments were run over a 24 h period, handling time was first estimated in days per prey item. For clarity and cross-study comparison, these values were also converted into hours per prey item by multiplying daily 𝑇ℎ by 24. For example, a handling time of 0.05 days corresponds to 1.2 h. Reporting both daily and hourly handling times allows direct comparison with short-term laboratory trials (hourly scale) and whole-day predation capacity (daily scale).
Parameter estimation (α and Th) and their standard errors were obtained using nonlinear least squares regression with bootstrap resampling to generate 95% confidence intervals, implemented in the R package frair (Pritchard et al. 2017). The maximum daily predation capacity was derived from the reciprocal of Th. The relationship between the mean number of consumed prey versus the original number of prey offered to each predator at the beginning of the experiment (prey consumed/prey density × 100) for all larval instars was estimated.
Data Analysis
Statistical analysis was performed using Python with the scipy, statsmodels, and seaborn libraries. First, the assumptions of normality and homogeneity of variance were tested using the Shapiro-Wilk test and Levene’s test, respectively. The results confirmed that the data met the assumptions for ANOVA (p > 0.05 for both tests) , two-way ANOVA was then conducted to determine if there were significant differences in predation rates across prey densities for each instar and temperature. Since the measurements were taken from different individuals at each temperature and prey density level, and each individual was used only once for a specific treatment combination, the observations were independent. If the ANOVA results indicated significant differences (p < 0.05), Tukey’s Honestly Significant Difference (HSD) Test was applied for pairwise comparisons between prey densities to identify specific differences.
Results
Figure 1 presents the predation rates of Macrolophus caliginosus at three temperatures (20, 25, and 30 °C) and five prey densities (5, 10, 15, 20, and 25 individuals), evaluated across the predator’s different nymphal instars.. By analyzing how each predator instar responds to changes in temperature and prey availability.
Fig. 1
Mean number of A.craccivora prey consumed by different nymphal instars of M.caliginosus at at 20 °C,25 °C and 30 °C. Box plots represent the median, interquartile range, and minimum–maximum values of prey consumption for first, second, third, and fourth instars
The total predation rate (i.e. the sum of the entirely consumed and unconsumed prey) of M. caliginosus increased with rising prey density. Analysis revealed a significant relationship between prey density and predation rate at 20 °C (F = 45.75, p = 0.006) and 30 °C (F = 10.80, p = 0.03), indicating that predation rate significantly increases with prey density at these temperatures. However, at 25 °C, no significant relationship was found (F = 2.50, p = 0.21), suggesting that predation rate remains relatively stable regardless of prey density.
The natural mortality (mean ± SE) of aphids in petri dishes due to the experimental manipulations was negligible and found to be 2.0 ± 0.42, 2.5 ± 0.34, 2.5 ± 0.34, 2.4 ± 0.3, and 2.5 ± 0.25 for densities of 5, 10, 15, 20, and 25 prey individuals per dish, respectively.
Predation rates at different prey densities revealed varying effects of temperature and instar stage. At the lowest prey density of 5, neither temperature (p = 0.18) nor instar (p = 0.26) had a significant effect on predation rates, indicating that predation remained relatively stable across temperature variations and developmental stages. Similarly, at a prey density of 10, temperature showed no significant effect (p > 0.05), while instar approached borderline significance (p ≈ 0.06), suggesting a potential but inconclusive influence of developmental stage on predation. However, at a prey density of 15, both temperature and instar had a significant effect (p < 0.05), indicating that predation rates were influenced by both factors. This trend continued at prey densities of 20 and 25, where temperature and instar effects were consistently significant (p < 0.05), highlighting an increasing dependency of predation rates on both environmental conditions and predator developmental stage as prey availability increased.
At 20 °C, prey density had a strong statistical impact in all instars (p < 0.001), with consumption rates increasing consistently as prey density rose, peaking at 18.2 ± 0.66 in the first instar and decreasing to 12.2 ± 0.24 in the fourth instar at the highest density of 25.
At 25 °C, while prey density continued to have a significant effect (p < 0.001), consumption rates were generally lower, and variability in predation patterns emerged, with consumption peaking at 9.6 ± 0.24 in the third instar before declining at higher densities.
At 30 °C, significant differences were observed across all predator instars (p < 0.001), with consumption rates fluctuating more dynamically. The highest predation was recorded at the highest prey density (25), where consumption peaked at 16 ± 0.32 in the fourth instar, suggesting a temperature-dependent shift in predation capacity. Overall, the results show that predation increased as prey density increased, but the effect of temperature was different. At 20 °C and 30 °C, the predators consistently consumed more prey as density rose, indicating high feeding efficiency. At 25 °C, however, consumption was more irregular, and the number of prey eaten did not increase as clearly with density, suggesting reduced or unstable predation performance at this temperature.
Functional Response Parameters
Table 1 presents the type II functional response parameters of M. caliginosus preying on A. craccivora nymphs at different temperatures and nymphal instars. The parameters measured include the average number of preys killed (Ha), handling time (Th) expressed in days and hours, and the successful search rate (α).
Table 1
The rate of successful Searching efficiency (α) and handling time (Th), describing functional response parameters of M.caliginosus at different densities of A.craccivora nymph. A significant slope (p < 0.05) indicates that prey density has a statistically significant effect on prey consumption.
Temperature
Predator Nymphal instar
Average no. prey killed [Ha]
Handling Time [Th]
Successful search [α]
95% CI
F-value
P value
Significant
Th/day
Th/hours
Th
[day/individuals]
Lower
Upper
20 °C
First nymphal
0.20 ± 0.04
0.301
7.22
3.32 ± 0.69
0.14 ± 0.14
0.476
0.980
62.06
0.0015*
Yes
25 °C
0.19 ± 0.04
1.29
30.96
0.78 ± 3.21
0.10 ± 0.07
0.320
0.968
29.34
0.0058*
Yes
30 °C
0.21 ± 0.04
0.911
21.86
1.10 ± 2.84
0.18 ± 0.06
0.412
0.900
53.60
0.0018*
Yes
20 °C
Second nymphal
0.18 ± 0.03
1.48
35.52
0.676 ± 0.69
0.17 ± 0.14
0.423
0.841
70.32
0.0012*
Yes
25 °C
0.19 ± 0.04
0.23
5.52
4.348 ± 3.21
0.12 ± 0.07
0.454
1.050
46.21
0.0024*
Yes
30 °C
0.21 ± 0.04
0.249
5.98
4.016 ± 2.84
0.14 ± 0.06
0.563
0.941
113.20
0.0004*
Yes
20 °C
Third nymphal
0.15 ± 0.03
0.0166
0.40
60.241 ± 0.69
0.11 ± 0.14
0.098
0.902
11.96
0.026*
Yes
25 °C
0.13 ± 0.02
0.827
19.85
1.209 ± 3.21
0.08 ± 0.07
0.043
0.725
9.96
0.0349*
Yes
30 °C
0.18 ± 0.03
0.737
17.69
1.357 ± 2.84
0.15 ± 0.06
0.319
0.849
36.78
0.0038*
Yes
20 °C
Fourth nymphal
0.13 ± 0.02
3.086
74.06
0.324 ± 0.69
0.15 ± 0.14
0.154
0.694
18.42
0.013*
No
25 °C
0.11 ± 0.01
2.679
64.30
0.373 ± 3.21
0.11 ± 0.07
0.051
0.517
11.41
0.0284*
No
30 °C
0.15 ± 0.02
0.287
6.89
3.484 ± 2.84
0.20 ± 0.06
0.187
0.613
25.00
0.0074*
Yes
Logistic (polynomial) regression of the proportion of prey eaten against initial prey density produced a significantly negative linear term for all instar × temperature combinations (P1 < 0.05), indicating a Type II functional response. Accordingly, Holling’s Type II (disc) model was fitted to each dataset to estimate α and h (Table 1). Bootstrap 95% confidence intervals for α and h are reported; parameters were robust to fitting with the Rogers random-predator model for treatments showing any notable prey depletion.
The Average Number of Prey Killed (Ha)
The effect of prey density on the predation rate (%) by different instar nymphs of M. caliginosus at 20 °C, 25 °C, and 30 °C. The first instar exhibited a significantly higher predation rate at 30 °C (0.21 ± 0.04) compared to 25 °C (0.19 ± 0.04). The third instar also showed a significant increase in predation at 30 °C (0.18 ± 0.03) compared to 25 °C (0.13 ± 0.02). Similarly, the fourth instar displayed a higher predation rate at 30 °C (0.15 ± 0.02) than at 25 °C (0.11 ± 0.01). No significant differences were observed between temperatures for the second instar Handling Time (Th) Expressed in Days and Hours.
For the first nymphal instar of M. caliginosus, handling time (Th) varied markedly with temperature. At 20 °C, Th was relatively short (0.301 days, equivalent to 7.22 h per prey), indicating high predation efficiency. At 25 °C, Th increased significantly to 1.29 days (30.96 h), reflecting a pronounced reduction in feeding capacity. At 30 °C, Th decreased again to 0.911 days (21.86 h), suggesting a partial recovery in predation efficiency compared to 25 °C. At 20 °C, the second nymphal instar had a longer handling time of 1.48 days (35.52 h), indicating slower prey processing. At 25 °C, the handling time significantly reduced to 0.23 days (5.52 h), suggesting enhanced predation capacity. At 30 °C, the handling time slightly increased to 0.249 days (5.98 h). The third nymphal instar at 20 °C had an exceptionally short handling time of 0.0166 days (0.40 h), indicating very high efficiency in processing prey. At 25 °C, the handling time increased significantly to 0.827 days (19.85 h), showing a decline in efficiency. At 30 °C, the handling time improved to 0.737 days (17.69 h), indicating better predation capacity than at 25 °C. At 20 °C, the fourth nymphal instar had the longest handling time at 3.086 days (74.06 h), indicating significantly reduced efficiency in processing prey. At 25 °C, the handling time decreased to 2.679 days (64.30 h), reflecting a slight improvement in predation capacity. At 30 °C, the handling time improved significantly to 0.287 days (6.89 h), indicating much better predation capacity.
The Successful Search Rate (α)
At 20 °C, the search rate (α) for the first nymphal instar was relatively high at 0.144 ± 0.14, indicating frequent encounters with prey. At 25 °C, the successful search rate dropped to 0.10 ± 0.07, indicating fewer successful predatory events. At 30 °C, the successful search rate improved to 0.18 ± 0.06, suggesting better prey encounter rates than at 25 °C. At 20 °C, the successful search rate for the second nymphal instar was relatively low at 0.17 ± 0.14, suggesting a moderate level of predation capacity at this temperature. At 25 °C, the successful search rate surged to 0.12 ± 0.07, indicating a substantial increase in successful prey encounters. At 30 °C, the successful search rate was 0.14 ± 0.06, slightly lower than at 25 °C, suggesting a slight reduction in efficiency. The third nymphal instar at 20 °C had an extremely high successful search rate of 0.11 ± 0.14, suggesting that prey was encountered and processed very rapidly. At 25 °C, the successful search rate fell to 0.08 ± 0.07, indicating fewer successful encounters with prey. At 30 °C, the successful search rate increased to 0.15 ± 0.06, showing a slight increase in predation capacity. At 20 °C, the fourth nymphal instar had a rate of successful search rate of 0.15 ± 0.14, suggesting infrequent successful predation events. At 25 °C, the successful search rate was 0.11 ± 0.07, lower than at 20 °C. At 30 °C, the successful search rate increased to 0.20 ± 0.06, showing a considerable improvement in successful prey encounters compared to lower temperatures.
Discussion
The findings are consistent with previous research on the influence of temperature and prey density on predator feeding behaviour. At 20 °C, consumption rates consistently increased with rising prey density across all predator instars. The highest consumption rate was recorded in the first instar, peaking at 18.2 ± 0.66 at a prey density of 25. This result aligns with Jeschke and Tollrian (2000), who reported that younger instars exhibit higher feeding rates due to greater energy demands during development. At 25 °C, consumption rates showed variation, with a decline across instars as prey density increased, which agrees with Angilletta et al. (2004). . The stable consumption rates observed at higher prey densities imply a saturation point, beyond which predators reach their maximum foraging efficiency. At 30 °C, fluctuations in consumption rates across prey densities indicate a more complex feeding pattern, with peak consumption observed in the fourth instar at a density of 25 (16 ± 0.32). Predation efficiency generally increases with rising temperature within the predator’s thermal optimum due to enhanced metabolic activity (Sih et al. 1998). However, at higher or stressful temperatures, foraging efficiency declines as physiological stress reduces predator performance, consistent with De Backer et al. (2015).. The predation capacity of M. caliginosus on A. craccivora varied across nymphal instars and temperatures, offering important insights into its thermal biology. At 20 °C, the first nymphal instar exhibited a high predation rate (0.20 ± 0.04) with a short handling time (0.301 days), supporting the findings of Foglar et al. (1990). M. caliginosus demonstrated a Holling’s type II functional response for both M. persicae and Tetranychus urticae, with a higher handling time and attack rate for aphids (Th = 0.055 day, a = 1.035) than for mites (Th = 0.025 day, a = 0.947). At 25 °C, the predation rate slightly decreased (0.19 ± 0.04), while handling time significantly increased to 1.29 days. This aligns with findings by Moerkens et al. (2016) and Apreutesei (2010), who suggested that elevated temperatures may increase metabolic rates but reduce predation capacity due to physiological stress. This was further supported by a decline in successful search rates at this temperature (Benjamin et al., 2024).
Interestingly, at 30 °C, predation capacity recovered, with an increased predation rate (0.21 ± 0.04) and reduced handling time (0.911 days), consistent with observations by Sharifian et al. (2015) and Pervez et al. (2018), who noted that optimal temperature ranges can enhance foraging behaviour by balancing metabolic demands and efficiency (Chan et al. 2017; Berardo et al. 2020). The second nymphal instar exhibited a lower prey kill rate at 20 °C (0.18 ± 0.03 prey per predator per day) and a longer handling time (1.48 days) compared to the first instar at the same temperature, which showed a higher kill rate (0.41 ± 0.05) and a shorter handling time (0.30 days).corroborating the findings of Sidhu et al. (2020) that younger instars tend to be more efficient predators than older ones. The third nymphal instar displayed a high successful search rate at 20 °C (8.70 ± 2.43) despite a lower prey kill rate (0.15 ± 0.03), supporting previous observations by Hossie and Murray (2016) and Hatherly et al. (2009), indicating rapid prey encounters but reduced processing efficiency. This phenomenon has also been described by Mutz et al. (2023) in predator-prey dynamics. The fourth instar recorded the lowest predation rate (0.13 ± 0.02) and the longest handling time (3.086 days) at 20 °C, reflecting a decline in efficiency. This is consistent with the findings of Clancy and Price (1987) and López et al. (2008), who reported that older nymphal instars show reduced predation capabilities due to increased energy demands and behavioural changes (Barnadas et al. 1998). Overall, temperature significantly influenced the predation capacity of M. caliginosus, with varying effects across instars, contributing to a broader understanding of predator-prey ecological dynamics under climate variability (Calvo et al. 2009, 2012).
Due to the limited availability of specific information on Macrolophus caliginosus, scientific evidence related to Macrolophus pygmaeus can be cited, given the similarities in their life cycles and behavioural patterns. Both species share comparable ecological roles and predatory functions, making studies on M. pygmaeus a valuable reference for understanding M. caliginosus. M. pygmaeus exhibits a preference for smaller M. persicae instars in mixed prey patches, even when the abundance of larger prey increases, indicating selective predation. Smaller prey may be easier to capture despite offering lower energy returns (Krebs and McCleery 1984; Stephens and Krebs 1986), whereas larger prey, although more nutritious, tend to possess stronger defences or better escape abilities (Pastorok 1981; Sabelis 1992; Provost et al. 2006).
Macrolophus pygmaeus demonstrated a type II functional response when exposed to single instars (Fantinou et al. 2008). However, the presence of alternative prey can shift this to a type III functional response, where predation preference increases with prey availability (Holling 1965; Colton 1987; Murdoch and Oaten, 1975; Akre and Johnson 1979). Type III responses contribute to the stabilization of prey populations (Oaten and Murdoch 1975; Comins and Hassell 1996), highlighting the importance of prey size structure in maintaining natural population dynamics. Superfluous killing, in which prey is killed but not consumed, was observed and associated with prey size, handling time, and defensive traits (Sandness and McMurtry 1970; Meyling et al. 2003). While the study observed minimal changes in predation rates (e.g., from 0.20 to 0.21 prey killed) under certain conditions, it is important to consider the biological relevance of such small differences. In ecological and biological control contexts, even minor variations in predation capacity can have cumulative effects over time, particularly in predator-prey population dynamics. For instance, a slight increase in daily predation rates (e.g., 0.01 prey per predator) could translate to significant reductions in pest populations across multiple generations or at larger spatial scales, where predators are deployed in high densities.
Conclusions
This study examines the impact of temperature and prey density on the predation capacity of M. caliginosus across its developmental stages. Predation rates increased with prey density but varied by temperature and predator nymphal ages, with early instars showing the highest consumption rates. Functional response parameters, including handling time and search rate, highlighted these variations. The adaptability of M. caliginosus to environmental changes underscores its potential as a biological control agent, with insights for improving pest management strategies in dynamic climatic conditions. Further research into additional environmental factors could enhance its application in agriculture.
Funding
The article processing charge was funded by Open Access Publication Fund of Humboldt-Universität zu Berlin.
Conflict of interest
A.H. E.L. Kenawy, R.M. Qaseem, M.M. M. Soliman, A. El-Harairy and W.E.A. El-Sheikh declare that they have no competing interests.
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Predation Response of Macrolophus caliginosus Wagner (Hemiptera: Heteroptera: Miridae) Across Multiple Prey Density Levels of Aphis craccivora Under Fixed Temperature Conditions
Authors
Ahmed H. EL Kenawy
Randa M. Qaseem
Mahmoud M. M. Soliman
Amged El-Harairy
Wael E. A. El-Sheikh
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