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. 2023 Aug 8;23(4):15. doi: 10.1093/jisesa/iead066

Why fake death? Environmental and genetic control of tonic immobility in larval lacewings (Neuroptera: Chrysopidae)

Katherine L Taylor 1,2,✉, Charles S Henry 3, Timothy E Farkas 4,5
Editor: John Ewer
PMCID: PMC10407979  PMID: 37551937

Abstract

Tonic immobility is a passive antipredator strategy employed late in the predation sequence that may decrease individual mortality in prey animals. Here, we investigate how energetic state and genetic predisposition influence antipredator decision-making in green lacewing larvae, Chrysoperla plorabunda (Fitch), using simulated predatory encounters. We demonstrate that tonic immobility is a plastic response influenced by energetic resource limitation. Larvae exposed to 1 or 2 days of food deprivation initiate tonic immobility more often and with less physical provocation than individuals fed ad libitum. Recently molted individuals exposed to food deprivation, the individuals most energetically challenged, engage in tonic immobility at a higher rate than any other group. We also find that variation in antipredator strategy between individuals is partly the result of within-population genetic variation. We estimate the propensity to enter tonic immobility to have a broad-sense heritability of 0.502. Taken together our results suggest that larval lacewings under energetic stress are more likely to engage in tonic immobility. Yet, energetic state does not explain all within-population variation, as individuals can have a genetic predisposition for tonic immobility.

Keywords: death feigning, tonic immobility, thanatosis, antipredator behavior, lacewing

Introduction

Tonic immobility, also called thanatosis or death feigning, is a maintained motionless posture triggered by proximity of an antagonist (Humphreys and Ruxton 2018). In some taxa, this behavioral syndrome involves not only rigid stillness but also behavioral or even physiological changes associated with death. The archetypal example is the opossum (Didelphis virginiana), which not only maintains a motionless posture but decreases body temperature, respiratory rate, and heart rate, while also urinating, defecating, and salivating (Gabrielsen and Smith 1985). The occurrence of tonic immobility is widely distributed throughout the animal kingdom, yet is underreported and understudied (Rogers and Simpson 2014, Humphreys and Ruxton 2018). Despite widespread tonic immobility, variation in this behavior has mostly been studied in a small number of organisms.

Prey that feign death with tonic immobility experience lower rates of predation-associated mortality than active conspecifics (Miyatake et al. 2009, Krams et al. 2013). Indeed, predators attack immobilized prey less frequently (Gyssels and Stoks 2005, Skelhorn 2018). Experiments on multiple beetles and predator species have found that laboratory lines selected for more tonic immobility experienced lower predation rates and longer latency to predation (Miyatake et al. 2004, Konishi et al. 2020, Asakura et al. 2022). Insects also likely experience minimal energetic cost with tonic immobility, as metabolic rates in beetles are lower during tonic immobility than resting metabolic rates (Metspalu et al. 2013, Li and Wen 2021). Yet when prey engage in tonic immobility, they do incur an opportunity cost: the time spent remaining motionless cannot be invested in foraging or reproduction. When tonic immobility also results in dropping from a resting or foraging substrate, the opportunity cost is even greater, as the fallen prey may encounter a less hospitable environment and must spend time refinding resources (Humphreys and Ruxton 2019). As an alternative to tonic immobility, prey may attempt an active escape or direct engagement of the predator. These strategies result in higher predation rates and higher energetic costs, but potentially result in less lost foraging time.

Prey behavior depends on the threat type and intensity, the physiological status of the prey, and other aspects of the ecological context (Stephens 1981, Kacelnik and Bateson 1996, Lima 1998, Mishra et al. 2017) (Stephens). Previous experiments on a wide variety of insects have demonstrated that the frequency of tonic immobility is dependent on the condition of the individual. For example, tonic immobility is observed more at lower ambient temperatures (Miyatake et al. 2008a), in younger, newly emerged, or smaller insects (Hozumi and Miyatake 2005, Cassill et al. 2008, Farkas 2016), and in individuals with lower resting metabolic rates (Krams et al. 2013) or less locomotor activity (Miyatake et al. 2008b). These findings suggest that energetically challenged or poor-condition individuals, with less ability for rapid movement or other defenses, may be more likely to engage in tonic immobility. However, not all studies align with this trend. For example, starved adult beetles are less likely to engage in tonic immobility and recover more rapidly than well-fed individuals (Acheampong and Mitchell 1997, Miyatake 2001, Li et al. 2019).

Individual condition does not explain all variation in tonic immobility. A genetic basis for duration of tonic immobility has been identified in several animals. In chickens, 78–91% of individual variance for death feigning can be explained by genetics, and several candidate genes have been identified that may underlie the behavior (Gallup 1974, Fogelholm et al. 2019). Heritability of tonic immobility duration has also been demonstrated in several flour beetle species (Miyatake et al. 2004, Nakayama et al. 2010). In flour beetle lines selected for long- and short-duration tonic immobility, several metabolic pathways and dopamine-associated candidate genes have been identified as potential genetic bases of tonic immobility (Uchiyama et al. 2019, Tanaka et al. 2021).

Here, we describe tonic immobility in larvae of the North American green lacewing, Chrysoperla plorabunda (Fitch) (Neuroptera: Chrysopidae), a generalist predator of arthropods. Individuals are well defended, having biting mandibles capable of injecting paralyzing and digestive venoms, are fast moving, and produce anal secretions that deter ant predation (Canard et al. 1984, Lamunyon and Adams 1987). Despite formidable weapons, these soft-bodied insects also engage in tonic immobility, previously described as “reflex curling and falling” (Canard et al. 1984), to escape natural enemies. Using simulated predatory encounters, we investigated the effects of energetic stress and within-population genetic variation on antipredator decision-making in larval lacewings.

Methods

The Insects

Chrysoperla plorabunda were purchased from Biobest Canada Insectary (Leamington, Ontario, Canada), identified to species by song phenotype, and reared in the laboratory. Lacewings were maintained under constant long day–light cycle (16L:8D) with white fluorescent lighting and at a temperature of 25 ± 1 °C. Larvae were reared individually in lidded 1-ounce clear plastic containers and fed Ephestia kuehniella moth eggs from Beneficial Insectary (Redding, CA, USA). Adults were group reared with up to 10 same-sex individuals in 8-ounce clear plastic cups stacked inside another 8-ounce clear plastic cup and covered with a petri dish lid. Holes were drilled in the bottom of the upper cup for a cotton wick to transfer water from a reserve in the plastic cup stacked below. Adults were provided shelter made of folded cardstock, ad libitum water, and ad libitum food consisting of a 3:2:1 mixture of Wheast:honey:water.

Experimental Feeding Treatment

Second-instar larvae, both male and female, which had previously been receiving E. kuehniella eggs ad libitum, were randomly assigned to one of 3 experimental groups. For the “fed” group, E. kuehniella eggs were provided for the duration of the experimental feeding period. For the “1-day starved” group, the E. kuehniella eggs were removed 1 day before behavioral tests. In the “2-day starved’ group, the E. kuehniella eggs were removed 2 days before behavioral tests. After exclusion of a small number of insects that we were unable to identify to instar due to accidental loss of photographs, the final sample size for the fed group was 55, 1-day starved group was 59, and 2-day starved group was 55.

Body Measurement

Larvae were photographed from above with a 6.35 mm (1/4 inch) scale bar on the day of the behavioral tests. Head and body-size measurements were made from the digital photographs using ImageJ 1.52a (Schneider et al. 2012). The length and width of the head and body (thorax and abdomen) were measured to assess the effects of the feeding treatments on body condition and development. The impact of treatment group on body length and width was analyzed with a multivariate analysis of variance (MANOVA). Measurements of the head capsule were used to determine developmental stage. Insects with both a head width above 0.7874 mm and a head length above 0.4572 mm were identified as likely third instar, and all others were classified as second instar.

Tonic Immobility Assay

Larvae were transferred to a paper-covered lab bench and gently prodded by the index finger of a researcher (Supplementary Video 1). The larvae were prodded until tonic immobility was observed or up to a maximum of 20 times. Experimenter prodding is frequently used to simulate predatory attacks and elicit tonic immobility in predation experiments. Other tonic immobility experiments have elicited this behavior with wooden sticks (Miyatake et al. 2004, Konishi et al. 2020), brushes (Nakayama et al. 2010), and soft forceps (Farkas 2016). These simulated encounters seem to be reasonable proxies for real predation, as in Miyatake et al. (2004), Konishi et al. (2020), and Asakura et al. (2022), insects selected for long- and short-duration tonic immobility responses to a wooden stick had differences in tonic immobility rates, predation latency, and survival in real predator encounters. Prodding with a finger was chosen over an array of other approaches, as it proved to consistently elicit tonic immobility and reduced injury to these small, soft-bodied insects. Tonic immobility was identified when an insect lay rigidly still on its side or back with legs pulled in toward its body, and only scored as such if it remained motionless for at least 3 s.

Three tonic immobility response variables were measured and analyzed. First, the propensity for tonic immobility was scored as a binary trait: the lacewings either did or did not initiate tonic immobility in response to up to 20 prods. Second, the number of prods before tonic immobility began was recorded. Third, whether the duration of immobility was long (≥2 min) or short (<2 min) was recorded. The relationship between predictor and response variables was analyzed using a general linear model comparison approach, starting with an intercept-only model, then adding feeding treatment, followed by developmental stage, and finally an interaction between feeding treatment and developmental stage. The nested models for each response variable were compared using a likelihood ratio chi-square test with an α of 0.05. Binomial GLM were selected for the two binary response variables (“yes” or “no” for engaging in tonic immobility and “long” or “short” duration tonic immobility), while quasi-Poisson GLM was used for the count of stimuli before response. Post hoc pairwise contrasts were calculated with the R package emmeans (v. 1.8.6), with an α of Bonferroni corrected 0.05.

Heritability Estimate

Larvae from the fed group that had completed the tonic immobility assay were reared to adulthood. To increase variance in offspring phenotype, adults were mated assortatively by tonic immobility propensity. Males and females were ranked by propensity for tonic immobility, with those that entered tonic immobility with the least stimulation on one extreme and those that never entered tonic immobility at the opposite extreme, and mating pairs were made of similarly ranked males and females. Nineteen crosses were produced: 6 pairs of half-sibling lines that shared fathers (12 total) and 7 lines without half-siblings. Ten offspring were reared from each cross with E. kuehniella eggs ad libitum and were tested for tonic immobility response as described above under “Tonic immobility assay.”

The propensity to engage in tonic immobility was scored as a binary trait. Heritability of this trait was estimated using an “animal model,” which incorporates all relatedness data available, including parent–offspring, full-sibling, and half-sibling information, to assess how well relatedness explains the distribution of phenotypes (Wilson et al. 2010). Heritability was assessed in a Bayesian framework using MCMCglmm (Hadfield 2010) with a χ2 prior, the most precise method typically used for calculating heritability estimates using binary data (de Villemereuil et al. 2013).

Results

Feeding Assay

Feeding condition had a considerable impact on body measurements. Body measurements were larger for the fed group than the 1- or 2-day starved groups with mean body lengths (±SE) of 5.1 ± 0.10, 4.2 ± 0.11, and 3.5 ± 0.11 and body widths of 1.3 ± 0.02, 1.1 ± 0.03, and 0.88 ± 0.03 mm, respectively (MANOVA, Pillari’s trace = 0.42, F4,334 = 21.97, P < .001). One or 2 days of starvation significantly changed body condition. However, food limitation did not halt development completely: between the start of the feeding experiment and the time of the behavioral tests, 16.3% of the fed, 8.4% of the 1-day starved, and 7.2% of the 2-day starved larvae molted into the third instar as determined by grouping within head-size clusters.

Larvae that had been deprived of food for 1 or 2 days exhibited tonic immobility more often than the continuously fed larvae (Fig. 1). The model that best described the propensity to engage in tonic immobility had treatment as a predictor, and this model was a significantly better fit than an intercept-only model (D168,166 = 13.29, P = 0.001). Post hoc contrasts with a Bonferroni correction for multiple testing revealed that both 1 (estimate = −1.37, P = 0.003) and 2 days (estimate = −1.09, P = 0.02) of food deprivation significantly increased propensity for tonic immobility compared to the consistently fed group. There was no difference between the 2 food-deprived groups (estimate = 0.28, P = 1). The inclusion of developmental stage main effect did not further improve fit (D166,165 = 0.33, P = 0.57), but the inclusion of an interaction between developmental stage and feeding treatment did significantly improve model fit (D166,163 = 11.66, P = 0.009). Third-instar larvae in the fed group were unlikely to use tonic immobility, but 100% individuals recently molted into the third instar that were in the food-deprived groups did engage in tonic immobility (Fig. 1).

Fig. 1.

Fig. 1.

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Proportion of larvae of Chrysoperla plorabunda entering tonic immobility in response to prodding in 3 feeding conditions: fed, 1 day starved, and 2 days starved for both second and third instars. Starved individuals engaged in the behavior more often than fed individuals. Sample sizes for the fed, 1-day starved, and 2-day starved groups were 46, 54, and 51, respectively, for second-instar larvae and 9, 5, and 4, respectively, for third-instar larvae.

Congruent with the above findings, food-deprived larvae initiated tonic immobility with less provocation than continuously fed larvae (Fig. 2). The model that best described the amount of provocation required to initiate tonic immobility had treatment as the only predictor. This model was a better fit than an intercept-only model (D111,109 = 69.56, P < 0.001) and adding developmental stage (D109,108 = 12.96, P = 0.07) or an interaction between developmental stage and treatment (D109,106 = 24.17, P = 0.09) did not significantly improve fit. Post hoc contrasts with a Bonferroni correction showed that both 1 (estimate = 0.76, P < 0.001) and 2 (estimate = 0.78, P < 0.001) days of food deprivation decreased the provocation required for tonic immobility initiation compared with the fed group and that there was no difference between the food-deprived groups (estimate = 0.021, P = 1).

Fig. 2.

Fig. 2.

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The number of stimuli required to provoke tonic immobility in larvae of Chrysoperla plorabunda for those that did engage in the behavior. Starved individuals required less provocation to initiate the behavior. Results shown in three feeding conditions, sample sizes for the fed, 1-day starved, and 2-day starved groups were 26, 46, and 40, respectively.

Yet, the number of individuals remaining in long-duration (≥2 min) tonic immobility was not significantly different between well-fed and food-deprived larvae (Fig. 3). Models incorporating feeding treatment (D111,109 = 2.78, P = 0.25), instar (D111,110 = 0.27, P = 0.60), and the interaction of feeding treatment and instar (D111,106 = 4.33, P = 0.50) were not improvements over the intercept-only model.

Fig. 3.

Fig. 3.

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Proportion of larvae of Chrysoperla plorabunda remaining in a state of tonic immobility for 2 min or longer. A smaller proportion of starved lacewings engaged in long-duration tonic immobility, but this difference is not significant. Sample sizes for the fed, 1-day starved, and 2-day starved groups were 26, 46, and 40, respectively.

Heritability

According to the MCMCGLMM animal model, propensity for tonic immobility was heritable in the broad sense. The mean broad sense heritability was 0.502 (95% credible interval [0.251–0.753]). Dominance or maternal effects could not be separated from the additive genetic effects with these data, likely due to sample size limitations and the binary nature of the trait data. Parent and offspring phenotypes are visualized in Fig. 4.

Fig. 4.

Fig. 4.

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Mean parent and offspring tonic immobility response in larvae of Chrysoperla plorabunda, ranging between 1 (all engage in tonic immobility) and 0 (none engage in tonic immobility). Parent mean is the average of the mother and father of each line; offspring mean is the average response of offspring from each line. The relationship between offspring and parent mean supports the heritability of the behavior. Dot size indicates number of offspring tested for each line (between 10 and 3).

Discussion

One or 2 days of food deprivation increases the frequency of tonic immobility and decreases the amount of stimulation required to initiate tonic immobility in lacewings. These results suggest that propensity for tonic immobility in larval lacewings is energetic-state dependent and that individuals with fewer energy reserves are more likely to enter tonic immobility. The lower propensity for tonic immobility by individuals in the fed group could be explained by a higher probability of successful fleeing or counterattack by well-fed individuals. Prior literature suggesting that colder, younger, smaller, or less-active individuals are more likely to engage in tonic immobility (Cassill et al. 2008, Miyatake et al. 2008a, Krams et al. 2013, Farkas 2016) aligns well with the results observed here in lacewing larvae. However, in adult beetle starvation experiments, the opposite response to energetic stress was reported (Acheampong and Mitchell 1997, Miyatake 2001, Li et al. 2019).

We did not find an effect of food deprivation on the length of tonic immobility. Our findings suggest that energetically stressed insects may modify their tonic immobility decision in response to the different risks and benefits during and in the minutes immediately following the encounter with a predator. While those individuals in poor condition due to low energetic reserves may be more likely to initiate tonic immobility, it seems that those same individuals are not more likely to engage in the behavior for extended periods of time. It is possible that the cost to poor-condition individuals of attempting an active escape during predation is greater than the cost to individuals in good condition because of differences in the probability of success. After escape from immediate danger, a long duration of tonic immobility may decrease the chance of the predator re-engaging in the attack, but the cost of long-duration immobility in lost foraging time may outweigh the benefit for individuals with fewer energetic reserves. We should note that the decision to record the length of tonic immobility in this study as long or short, a binary trait (<2 min or >2 min), may have limited our power to detect effects of food deprivation on this response.

Additionally, our results suggest that the relationship between developmental stage and tonic immobility is more complex than previously thought. Prior studies (Cassill et al. 2008, Farkas 2016) have found that younger insects are more likely to enter tonic immobility. In larval lacewings, it seems that the energetic burden of molting from second to third instar (Camp et al. 2014) combined with starvation induces an especially poor condition that increases the frequency of tonic immobility, as all individuals exposed to food deprivation that had also recently molted to the third instar entered tonic immobility. These results suggest that tonic immobility might be observed more frequently at multiple points in development where animals are energetically challenged. Future experiments monitoring tonic immobility through developmental stages and the molting process would help us better understand the relationships among energetic stress, development, and tonic immobility.

Although lacewings modify tonic immobility behavior in response to their energetic state, not all observed variance in the behavior is due to plasticity. We demonstrated that the propensity for tonic immobility is heritable in C. plorabunda. Although low sample size and use of binary trait data limited our ability to investigate dominance and maternal effects in this experiment, future studies may separate additive genetic variance to estimate narrow-sense heritability. Because artificial selection has resulted in tonic immobility trait evolution in other insects (Miyatake et al. 2004, Konishi et al. 2020, Asakura et al. 2022), additive genetic components seem likely to underlie some of the heritability of tonic immobility in C. plorabunda. If plasticity in tonic immobility is adaptive, a genetic basis of the trait might result in some individuals responding in suboptimal ways. Identification of genetic mechanisms underlying tonic immobility in lacewings could be a fruitful future direction, especially when compared with information about the genetic basis of death feigning duration in other animals (Uchiyama et al. 2019, Tanaka et al. 2021), to explore whether similar or different genetic mechanisms underly this widespread behavior.

Supplementary Material

iead066_suppl_Supplementary_Material
Click here for additional data file. (22.8MB, zip)

Contributor Information

Katherine L Taylor, Department of Entomology, University of Maryland, College Park, MD 20742, USA; Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA.

Charles S Henry, Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA.

Timothy E Farkas, Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA; Department of Biology, University of New Mexico, Albuquerque, NM 87101, USA.

Author Contributions

Katherine Taylor (Conceptualization [Equal], Formal analysis [Lead], Investigation [Equal], Visualization [Lead], Writing – original draft [Lead], Writing – review & editing [Equal]), Charles Henry (Conceptualization [Equal], Investigation [Supporting], Resources [Lead], Supervision [Supporting], Writing – review & editing [Equal]), and Timothy Farkas (Conceptualization [Equal], Formal analysis [Supporting], Investigation [Equal], Supervision [Lead], Writing – review & editing [Equal])

References

  1. Acheampong S, Mitchell B.. Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl. 1997:82(1):83–89. 10.1046/j.1570-7458.1997.00116.x [DOI] [Google Scholar]
  2. Asakura M, Matsumura K, Ishihara R, Miyatake T.. Freezing or death feigning? Beetles selected for long death feigning showed different tactics against different predators. Ecol Evol. 2022:12(2):e8533. 10.1002/ece3.8533 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Camp A, Funk D, Buchwalter D.. A stressful shortness of breath: molting disrupts breathing in the mayfly Cloeon dipterum. Freshw Sci. 2014:33:695–699. [Google Scholar]
  4. Canard M, Séméria Y, New T, editors. Biology of Chrysopidae. The Hague: Springer Netherlands; 1984. [Google Scholar]
  5. Cassill DL, Vo K, Becker B.. Young fire ant workers feign death and survive aggressive neighbors. Naturwissenschaften. 2008:95(7):617–624. 10.1007/s00114-008-0362-3 [DOI] [PubMed] [Google Scholar]
  6. de Villemereuil P, Gimenez O, Doligez B.. Comparing parent–offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol Evol. 2013:4:260–275. [Google Scholar]
  7. Farkas T. Body size, not maladaptive gene flow, explains death-feigning behaviour in Timema cristinae stick insects. Evol Ecol. 2016:30:623–634. [Google Scholar]
  8. Fogelholm J, Inkabi S, Höglund A, Abbey-Lee R, Johnsson M, Jensen P, Henriksen R, Wright D.. Genetical genomics of tonic immobility in the chicken. Genes. 2019:10(5):341. 10.3390/genes10050341 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gabrielsen G, Smith E.. Physiological responses associated with feigned death in the American opossum. Acta Physiol Scand. 1985:123:393–398. [DOI] [PubMed] [Google Scholar]
  10. Gallup GG. Genetic influence on tonic immobility in chickens. Anim Learn Behav. 1974:2(2):145–147. 10.3758/bf03199142 [DOI] [Google Scholar]
  11. Gyssels FG, Stoks R.. Threat-sensitive responses to predator attacks in a damselfly. Ethology. 2005:111:411–423. [Google Scholar]
  12. Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 2010:33(2):1–22.20808728 [Google Scholar]
  13. Hozumi N, Miyatake T.. Body-size dependent difference in death-feigning behavior of adult Callosobruchus chinensis. J Insect Behav. 2005:18(4):557–566. 10.1007/s10905-005-5612-z [DOI] [Google Scholar]
  14. Humphreys RK, Ruxton GD.. A review of thanatosis (death feigning) as an anti-predator behaviour. Behav Ecol Sociobiol. 2018:72(2):22. 10.1007/s00265-017-2436-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Humphreys RK, Ruxton GD.. Dropping to escape: a review of an under-appreciated antipredator defence. Biol Rev. 2019:94(2):575–589. 10.1111/brv.12466 [DOI] [PubMed] [Google Scholar]
  16. Kacelnik A, Bateson M.. Risky theories—the effects of variance on foraging decisions. Integr Comp Biol. 1996:36(4):402–434. 10.1093/icb/36.4.402 [DOI] [Google Scholar]
  17. Konishi K, Matsumura K, Sakuno W, Miyatake T.. Death feigning as an adaptive anti-predator behaviour: further evidence for its evolution from artificial selection and natural populations. J Evol Biol. 2020:33(8):1120–1128. 10.1111/jeb.13641 [DOI] [PubMed] [Google Scholar]
  18. Krams I, Kivleniece I, Kuusik A, Krama T, Freeberg TM, Mänd R, Vrublevska J, Rantala MJ, Mänd M.. Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle. Acta Ethol. 2013:16(3):163–172. 10.1007/s10211-013-0147-3 [DOI] [Google Scholar]
  19. Lamunyon CW, Adams PA.. Use and effect of an anal defensive secretion in larval Chrysopidae (Neuroptera). Ann Entomol Soc Am. 1987:80(6):804–808. 10.1093/aesa/80.6.804 [DOI] [Google Scholar]
  20. Li H, Wen J.. Behaviour and metabolism during tonic immobility (death-feigning) in Eucryptorrhynchus scrobiculatus and E. brandti (Coleoptera: Curculionidae). EJE. 2021:118:322–329. 10.14411/eje.2021.033 [DOI] [Google Scholar]
  21. Li H, Zhang G, Ji Y, Wen J.. Effects of starvation on death-feigning in adult Eucryptorrhynchus brandti (Coleoptera: Curculionidae). Ethology. 2019:125(9):645–651. 10.1111/eth.12917 [DOI] [Google Scholar]
  22. Lima SL. Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives.Advances in the study of behavior. 1998:27:215–290. [Google Scholar]
  23. Metspalu L, Kuusik A, Hiiesaar K, Tartes U.. Tonic immobility in adult Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), evoked by mechanical and optical stimuli. EJE. 2013:99(2):215–219. 10.14411/eje.2002.030 [DOI] [Google Scholar]
  24. Mishra S, Barclay P, Sparks A.. The relative state model: integrating need-based and ability-based pathways to risk-taking. Personal Soc Psychol Rev. 2017:21(2):176–198. 10.1177/1088868316644094 [DOI] [PubMed] [Google Scholar]
  25. Miyatake T. Effects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). Ann Entomol Soc Am. 2001:94:612–616. [Google Scholar]
  26. Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M.. Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc Biol Sci. 2004:271(1554):2293–2296. 10.1098/rspb.2004.2858 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miyatake T, Nakayama S, Nishi Y, Nakajima S.. Tonically immobilized selfish prey can survive by sacrificing others. Proc Biol Sci. 2009:276(1668):2763–2767. 10.1098/rspb.2009.0558 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Miyatake T, Okada K, Harano T.. Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis. Physiol Entomol. 2008a:33(1):83–88. 10.1111/j.1365-3032.2007.00607.x [DOI] [Google Scholar]
  29. Miyatake T, Tabuchi K, Sasaki K, Okada K, Katayama K, Moriya S.. Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum. Anim Behav. 2008b:75(1):113–121. 10.1016/j.anbehav.2007.04.019 [DOI] [Google Scholar]
  30. Nakayama S, Nishi Y, Miyatake T.. Genetic correlation between behavioural traits in relation to death-feigning behaviour. Popul Ecol. 2010:52:329–335. [Google Scholar]
  31. Rogers SM, Simpson SJ.. Thanatosis. Curr Biol. 2014:24(21):R1031–R1033. 10.1016/j.cub.2014.08.051 [DOI] [PubMed] [Google Scholar]
  32. Schneider CA, Rasband WS, Eliceiri KW.. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012:9(7):671–675. 10.1038/nmeth.2089 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Skelhorn J. Avoiding death by feigning death. Curr Biol. 2018:28(19):R1135–R1136. 10.1016/j.cub.2018.07.070 [DOI] [PubMed] [Google Scholar]
  34. Stephens DW. The logic of risk-sensitive foraging preferences. Anim Behav. 1981:29(2):628–629. 10.1016/s0003-3472(81)80128-5 [DOI] [Google Scholar]
  35. Tanaka K, Sasaki K, Matsumura K, Yajima S, Miyatake T.. Genomic characterization between strains selected for death-feigning duration for avoiding attack of a beetle. Sci Rep. 2021:11(1):21816. 10.1038/s41598-021-00987-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Uchiyama H, Sasaki K, Hinosawa S, Tanaka K, Matsumura K, Yajima S, Miyatake T.. Transcriptomic comparison between beetle strains selected for short and long durations of death feigning. Sci Rep. 2019:9(1):1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH.. An ecologist’s guide to the animal model. J Anim Ecol. 2010:79(1):13–26. 10.1111/j.1365-2656.2009.01639.x [DOI] [PubMed] [Google Scholar]

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