Skip to main content
NCBI home page
Wiley Open Access Collection logoLink to Wiley Open Access Collection
. 2022 Apr 19;337(6):666–674. doi: 10.1002/jez.2598

Flight capacity drives circadian patterns of metabolic rate and alters resource dynamics

Zachary R Stahlschmidt 1,✉
PMCID: PMC9324922  PMID: 35438260

Abstract

Animals must acquire, use, and allocate resources, and this balancing act may be influenced by the circadian clock and life‐history strategy. Field (Gryllus) crickets exhibit two distinct life‐history strategies during early adulthood—flight‐capable females invest in flight muscle at a cost to ovary mass, whereas flight‐incapable females instead invest solely into ovaries. In female Gryllus lineaticeps, I investigated the role of life‐history strategy in resource (food) acquisition and allocation, and in circadian patterns of energy use. Flight capacity increased the standard metabolic rate (SMR) due to greater late‐day SMR and flight‐capable crickets exhibited greater circadian rhythmicity in SMR. Flight‐capable crickets also ate less food and were less efficient at converting ingested food into body or ovary mass. Thus, investment into flight capacity reduced fecundity and the amount of resources available for allocation to other life‐history traits. Given the increasing uncertainty of food availability in many global regions, work in Gryllus may clarify the important roles of food and circadian patterns in life‐history evolution in a changing world.

Keywords: cricket, food, Gryllus, life history, wing dimorphism

Wing‐dimorphic crickets offer unique insight into the costs and benefits of flight capacity. Here I show that flight capacity increases the circadian rhythmicity of metabolic rate, and I further show that flight‐capable crickets eat less food and are less efficient at converting ingested food into body or ovary mass. In sum, investment into flight capacity in a field cricket can represent a risky energetic strategy that reduces fecundity and the amount of resources available for allocation to other life‐history traits.

graphic file with name JEZ-337-666-g002.jpg

Research Highlights

In a field cricket, investment into flight capacity (1) increased the circadian rhythmicity of resource use (standard metabolic rate), (2) reduced resource acquisition (food intake), and (3) reduced the efficiency by which ingested food was converted to reproductive tissue.

1. INTRODUCTION

The circadian clock in animals dictates virtually all levels of organismal biology—from gene expression and cell division to growth, behavior, and reproduction (Hori et al., 1995; Jakobsen & Strom, 2004; Panda et al., 2002; Sen & Hoffmann, 2020; Xu et al., 2011; Yeung & Naef, 2018). Many animals exhibit circadian patterns of metabolic rate (reviewed in Ellis & Gabrielsen, 2019; Mortola & Lanthier, 2004) as endogenous daily rhythms are synchronized to match the energy needs of animals (reviewed in Riede et al., 2017). Variation in metabolic rate may also be linked to life history (Bronikowski & Vleck, 2010; Crnokrak & Roff, 2002; Ksia̧zek et al., 2004; but see Clark et al., 2016; Djawdan et al., 1996, 1997). In addition, the evolution of circadian clocks may be entwined with life‐history evolution—circadian clocks and life‐history traits respond to similar selective pressures and selection on life‐history traits influences the evolution of circadian clocks (reviewed in Abhilash & Sharma, 2016). However, the interplay between life history and circadian rhythm related to metabolic rate is not fully understood.

Field crickets (Gryllus spp.) may offer important insight into the roles of life history and circadian clocks in standard metabolic rate (SMR), which is the energy cost of self‐maintenance and key to animal energetics (Glazier, 2005; Lighton, 2008). Gryllus crickets exhibit a wing dimorphism mediating two distinct life‐history strategies during early adulthood—long‐winged, flight‐capable (LW[f]) females invest in flight muscle at a cost to ovary mass, whereas short‐winged (SW) females are flight‐incapable but invest more heavily into ovaries than LW(f) females (Roff, 1984; Zera & Mole, 1994; Zera et al., 1997; Zera, 2005). The role of life‐history strategy in SMR for Gryllus is equivocal. Some work indicates that flight capacity is particularly costly (i.e., flight‐capable females exhibit greater SMR than SW females; Nespolo et al., 2008; Sun et al., 2020; Zera & Mole, 1994; Zera et al., 1997). Yet, other work finds no effect of flight capacity on SMR in Gryllus (Clark et al., 2016), or an effect only in particular contexts (e.g., flight capacity interacts with immune challenge to influence SMR; Stahlschmidt & Glass, 2020). A deeper dive into Gryllus physiology may reconcile these contrasting results. For example, flight capacity influences circadian physiology where flight‐capable females tend to exhibit larger daily fluctuations (i.e., greater circadian rhythmicity) in juvenile hormone levels and global gene expression patterns characterized by relative peaks late in the photophase (Zera et al., 2018; Zhao & Zera, 2004), putatively in preparation for nocturnal flight activity. As juvenile hormone increases SMR in other insects (Shigler et al., 2021), flight‐capable Gryllus may exhibit greater SMR late in the photophase. However, the link between variation in gene expression and SMR due to life‐history strategy is not understood in Gryllus. In garter snakes, fast‐aging individuals exhibit higher metabolic rate than their slow‐living conspecifics, and they exhibit higher expression of some (but not all) mitochondrial genes (Schwartz et al., 2015). Thus, further investigation is required to determine whether flight‐capacity in Gryllus increases circadian rhythmicity in whole‐animal resource use (i.e., SMR) similar to its effects on levels of hormones and gene expression.

In addition to circadian patterns of resource use, variation in resource acquisition and/or allocation may characterize flight‐related metabolic strategies. For example, LW(f) Gryllus are less efficient at converting digested food into body mass, potentially indicating a metabolic cost of flight capacity (Mole & Zera, 1993, 1994). Yet, LW crickets may offset greater energy use by exhibiting higher rates of food consumption, which has been shown in Gryllus firmus (Mole & Zera, 1994; but see Clark et al., 2016) and Gryllus lineaticeps (Treidel et al., 2021), but not in Gryllus rubens or Gryllus assimilis (Mole & Zera, 1993; Zera et al., 1998). Less studied is whether SW crickets exhibit greater reproductive investment because they more efficiently allocate ingested resources to ovary mass, or because they simply ingest more food thereby facilitating increased allocation to reproductive tissue. Understanding resource dynamics in Gryllus crickets may inform the evolution of flightlessness, which is fairly common in some insect taxa due to the reproduction‐related costs associated with flight (Guerra, 2011; Roff, 1984; Roff & Fairbairn, 1991). The loss of flight capacity may be favored if flight‐capable crickets exhibit a more precarious resource strategy whereby high metabolic rate and reduced efficiency in allocation of ingested resources to reproduction is not offset by increased food consumption. Thus, I used the variable field cricket (G. lineaticeps) to examine the role of flight capacity in (1) circadian patterns of SMR, (2) food consumption, and (3) efficiency by which ingested food is converted to somatic and reproductive tissues. Careful examination of the role of life‐history strategy in circadian patterns of resource use, as well as in resource acquisition and allocation, may inform drivers of life‐history evolution given the increasing uncertainty of food availability in many global regions (Ciais et al., 2005; Currano et al., 2008; Masoero et al., 2020).

2. MATERIALS AND METHODS

2.1. Study species

The variable field cricket (G. lineaticeps) is native to the western United States and is found predominately in California, USA, and Baja, Mexico (Weissman & Gray, 2019). G. lineaticeps is wing‐dimorphic like other Gryllus crickets (Weissman & Gray, 2019). Both LW and SW wing morphs were used in the study, and they were acquired from a long‐term colony that was subsidized annually by progeny from females collected from a natural population (Sedgwick Reserve). Breeding individuals in the colony were maintained at even sex and morph ratios. Throughout ontogeny, crickets were reared in standard conditions: 28 ± 1°C and 14:10 light:dark cycle with ad libitum access to water (water‐filled shell vials plugged with cotton) and shelter (cardboard egg cartons). Crickets were also supplied with ad libitum access to high‐protein (33% crude protein) commercial dry cat food pellets, because SW and LW G. lineaticeps fed a high‐protein diet exhibit the same investment into flight muscle and ovary mass as SW and LW crickets fed a diet of their choice (i.e., when offered several diets ranging in protein‐to‐carbohydrate ratios; Treidel et al., 2021). Newly molted female adults (<1 day after final ecdysis; Day 1) were weighed and individually housed in standard conditions (see above) in small translucent deli cups (473 ml) containing shelter (overturned 30 ml opaque containers with access holes) and preweighed food (pellets of dry cat food).

2.2. Experimental design

A factorial design was used to determine the independent and interactive effects of flight capacity and time‐of‐day on SMR, as well as the role of flight capacity in investment into reproductive tissue (i.e., ovary mass), food consumption, and the efficiency by which ingested food was converted to body and ovary mass. Crickets (n = 162) were placed into incubators (Model I‐30, Percival Scientific, Inc.) maintaining 28°C and a 14:10 light:dark cycle for 4 days. On Day 5, each cricket and its food were reweighed. Crickets (but not their food) were returned to their individual containers for 24 h before respirometry trials (see below) to limit the confounding effect of feeding state on metabolic rate (Secor, 2009).

On Day 6, each cricket was reweighed before its respirometry trial, which occurred in the morning (within initial 2–3 h of photophase; “AM”) or the afternoon (within final 2 h of photophase; “PM”). To estimate circadian rhythmicity of SMR, trials were performed at these timepoints for two reasons. First, circadian patterns of hormone levels and gene expression vary between the wing morphs when tissue sampling occurs at these two timepoints in at least four other Gryllus species in the field and lab, including those that exhibit flight in the scotophase (Zera et al., 2007, 2018; Zhao & Zera, 2004). Second, some field crickets are diurnal and even nocturnal field crickets exhibit some degree of behavioral activity during the photophase—thus, circadian shifts in physiology may be captured during the photophase (Jacot et al., 2008; Levy et al., 2021; Loher, 1979; Rost & Honegger, 1987; Sokolove, 1975; Tomioka & Chiba, 1989; Zera et al., 2007, 2018; Zhao & Zera, 2004). The activity patterns of adult G. lineaticeps are less understood. In the field, some female G. lineaticeps can exhibit flight activity in the scotophase (Sun et al., 2020), but females in the lab spend an estimated >90% of the scotophase under shelter when housed in isolation (Stahlschmidt et al., in review).

2.3. SMR

On Day 6, SMR was determined using flow‐through respirometry (see Supporting Information) as described previously (Padda et al., 2021; Stahlschmidt & Glass, 2020). Carbon dioxide production rate (V̇ CO2) was measured as an indirect estimate of SMR (Clark et al., 2016; Lighton, 2008; Nespolo et al., 2005), because CO2 analyzers are typically more sensitive than O2 analyzers (Harrison et al., 2012), and V̇ CO2 and V̇ O2 data in this study strongly correlated with one another (R = 0.91; p < 0.001). Each cricket (n = 149) was placed into a small glass metabolic chamber (59 ml) in an incubator (I‐30, Percival Scientific, Inc.) maintaining a constant 28°C. To reduce movement or activity during trials, a strip of opaque tape (width: 2.5 cm) was wrapped around each metabolic chamber to create a darkened (but not light‐free) environment and crickets were acclimated to their chambers for 90 min before measurement.

2.4. Resource acquisition and allocation

Food (dry cat food pellets) consumption was determined by subtracting final (Day 5) food mass from initial (Day 1) food mass. To determine the ability of crickets to convert ingested food into body tissue, food conversion efficiency for body mass was estimated (body mass gained [mg]/total food ingested [mg]). On Day 6, crickets were euthanized and stored at −20°C. After storage, crickets were dissected, and their ovaries were removed and dried at 55°C to a constant mass to estimate investment into reproduction (Crnokrak & Roff, 2002; Glass & Stahlschmidt, 2019; Roff & Fairbairn, 1991). Newly molted G. lineaticeps exhibit very little investment into reproduction—dry ovary mass is ~0.57% of Day 1 body mass (Stahlschmidt et al., in review). Thus, food conversion efficiency for ovary mass was estimated (estimated dry ovary mass gained between Day 1 and Day 6 [mg]/total food ingested [mg]). During dissections, flight musculature (dorso‐longitudinal muscle [DLM]) was also examined. In other Gryllus, LW crickets with histolyzed DLM (LW[h]) are more physiologically similar to SW crickets relative to LWs exhibiting functional DLM (LW[f]; Zera & Larsen, 2001; Zera et al., 1997; reviewed in Zera et al., 2018). Therefore, differences due to flight morphology (i.e., among LW[f], LW[h], and SW crickets) were analyzed for all dependent variables.

2.5. Statistical analyses

Data were tested for normality, natural logarithm‐transformed when necessary to achieve normally distributed residuals, and analyzed using SPSS (v.26 IBM Corp.). Two‐tailed significance was determined at α = 0.05. To examine the independent and interactive effects of time‐of‐day (morning or afternoon) and flight morphology (LW[f], LW[h], or SW) on metabolic rate, a linear model analysis was performed on body mass‐corrected V̇ CO2 (ml/h/g/Day 6 body mass). Several additional linear models were also performed to examine the effects of flight capacity on food consumption, dry ovary mass, and conversion rates for body mass and dry ovary mass. To account for body size, initial (Day 1) body mass was included as a covariate for the food consumption, final body mass, and ovary mass models.

3. RESULTS AND DISCUSSION

3.1. Results

Flight capacity increased energy use due to elevated SMR in the afternoon (i.e., significant effects of flight morphology and a flight morphology × time‐of‐day interaction), but time‐of‐day did not independently influence SMR (Figure 1 and Table S1). Flight capacity reduced reproductive investment and food ingestion (Figure 2 and Tables S2 and S3), as well as the efficiency by which ingested food was converted to body mass and reproductive tissue (Figure 3 and Tables S4 and S5).

Figure 1.

Figure 1

Open in a new tab

Effects of time‐of‐day (AM or PM) on standard metabolic rate in female G. lineaticeps exhibiting variation in flight morphology—short‐winged (SW, white symbols) and long‐winged with histolyzed flight muscle (LW[h], light gray symbols) crickets were flight‐incapable, whereas LW(f) (dark gray symbols) exhibited functional flight muscle (n = 149). Asterisk denotes significant difference (p < 0.05).

Figure 2.

Figure 2

Open in a new tab

Variation in (a) estimated ovary mass added and (b) food ingested during early adulthood in female G. lineaticeps exhibiting variation in flight morphology—short‐winged (SW) and long‐winged with histolyzed flight muscle (LW[h]) crickets were flight‐incapable, whereas LW(f) exhibited functional flight muscle (n = 162). Values are displayed as estimated marginal mean ± SEM, because initial (Day 1 of adulthood) body mass was used as a covariate to account for body size. Asterisks denote significant differences (p < 0.05).

Figure 3.

Figure 3

Open in a new tab

Variation in the efficiency by which ingested food was converted to (a) body mass and (b) dry ovary mass during early adulthood in female G. lineaticeps exhibiting variation in flight morphology—short‐winged (SW) and long‐winged with histolyzed flight muscle (LW[h]) crickets were flight‐incapable, whereas LW(f) exhibited functional flight muscle (n = 162). Asterisks denote significant differences (p < 0.05).

4. DISCUSSION

An animal must carefully acquire, use, and allocate resources, and this balancing act may be influenced by the animal's circadian clock and life‐history strategy. Here, the wing‐dimorphic G. lineaticeps was used to investigate the role of life‐history strategy (investment into flight capacity or reproduction during early adulthood) in resource (food) acquisition and allocation, as well as in circadian patterns of energy use. Flight capacity increased SMR, but this effect of life‐history strategy was due to greater SMR by flight‐capable crickets at the end of the photophase (Figure 1 and Table S1). Flight‐capable crickets did not offset their higher energy use by acquiring or more efficiently allocating food. Relative to flight‐incapable crickets, LW(f) crickets ate less food (Figure 2b and Table S3) and were less efficient at converting ingested food into body or ovary mass (Figure 3 and Tables S4 and S5). In sum, investment into flight capacity for G. lineaticeps may represent a risky strategy in some environments, because it reduces fecundity (Figure 2a and Table S2) and the amount of resources available for allocation to other life‐history traits.

Many animals exhibit circadian patterns of energy use, but the degree of circadian rhythmicity in metabolic rate varies significantly across taxa. For example, mammals exhibit fairly consistent circadian patterns in basal metabolic rate (BMR; reviewed in Mortola & Lanthier, 2004). Yet, bird taxa vary in metabolic rhythmicity—passerine birds generally show circadian effects on BMR while many polar birds, sea birds, pigeons, and birds of paradise do not (reviewed in Ellis and Gabrielsen, 2019). Among ectotherms, circadian patterns in metabolic rate are displayed by aquatic invertebrates (Chacón et al., 2003; Rosas et al., 1992; but see Diawol et al., 2016), by fishes (Kim et al., 1997; Ross & McKinney, 1988; Svendsen et al., 2014), and by reptiles (Birchard et al., 2006; Blem & Killeen, 1993; da Cruz et al., 2008; Klein et al., 2006; Roe et al., 2004, 2005). In terrestrial arthropods, circadian rhythmicity in SMR has been exhibited by insects (Banks et al., 1975; Crozier, 1979; Shipp & Otton, 1976; Woodring & Clifford, 1986), spiders (Humphreys, 1977; but see Stoltey & Shillington, 2009), and crustaceans (Reddy & Bhagyalakshmi, 1994; Van Senus, 1985). In this study, flight‐capable (LW[f]), but not flight‐incapable (SW and LW[h]), G. lineaticeps exhibited circadian rhythmicity in SMR (Figure 1). Future work is required to determine if this discrepancy is (1) due to the sampling protocol used (e.g., SMR was only examined during the photophase and some field crickets are more active during the scotophase; Sokolove, 1975; Tomioka & Chiba, 1989), or (2) because the evolution of flightlessness may blunt circadian patterns of physiology (Zera et al., 2018; Zhao & Zera, 2004).

Flight capacity led to increased energy use in G. lineaticeps (Figure 1) as has been previously demonstrated in Gryllus (Nespolo et al., 2008; Sun et al., 2020; Zera & Mole, 1994; Zera et al., 1997; but see Clark et al., 2016). The metabolic cost of flight investment was due to elevated SMR late in the photophase, putatively to facilitate nocturnal flight behavior, which is very metabolically demanding (Roff, 1991). However, metabolic differences due to flight morphology alone (i.e., independent of flight behavior) may be exacerbated in nature where crickets can thermoregulate—in G. lineaticeps, LWs exhibit a preferred temperature of 36°C whereas SWs prefer 32.5°C (Sun et al., 2020). Metabolic rate is highly sensitive to temperature and the respiratory quotient for V̇ CO2 in G. lineaticeps is 2.4 (Sun et al., 2020). Therefore, differences in thermal preference (Sun et al., 2020) may result in flight‐capable G. lineaticeps exhibiting 50% higher SMR than their flight‐incapable counterparts based on SMR data from the current study. Similar to wing morphs, ecotypes (different populations that are genetically distinct) often differ in life‐history strategy and metabolic rate (Andere et al., 2002; Chung et al., 2021; Gangloff et al., 2015; Rouleau et al., 2010). Thus, variation in patterns of energy use may be a fundamental feature of life‐history evolution, although work across taxa paints a fuzzier picture (e.g., metabolic data do not appear to support the pace‐of‐life hypothesis: reviewed in Royauté et al., 2018). As metabolic rate is complex (Glazier, 2015), understanding SMR in the context of life‐history evolution may require incorporating circadian effects. I encourage others to similarly integrate the effects of life‐history strategy (e.g., morph or ecotype) and circadian patterns on SMR.

In Gryllus, divergent resource allocation strategies underlie the two life‐history strategies (i.e., the flight‐fecundity tradeoff). Flight‐capable crickets invest in lipogenesis to produce lipid flight fuel and allocate more to somatic stores, whereas flight‐incapable crickets conserve protein and allocate more to ovaries (reviewed in Zera, 2005). These allocation strategies are achieved through differential feeding strategies—flight‐incapable females preferentially feed on a more protein‐biased diet relative to flight‐capable females (Clark et al., 2013; Treidel et al., 2021). Feeding in house (Acheta) crickets largely occurs at night (Woodring & Clifford, 1986), but it is not known if flight capacity in Gryllus influences circadian patterns of resource acquisition similar to the flight‐dependent rhythmicity of energy use (Figure 1). Although my study used a protein‐biased diet and did not monitor the allocation of specific macronutrients, its results mirror those from a recent study in G. lineaticeps that focused on macronutrient acquisition and allocation. Despite burning more calories, flight‐capable G. lineaticeps in this study ate 45% less food than flight‐incapable crickets in agreement with Treidel et al., 2021, and they were less efficient at converting ingested food into body or ovary mass (Figures 2b and 3). Therefore, conventional studies using gravimetric data can complement experiments examining the role of macronutrient composition of food in feeding behavior and allocation.

Other Gryllus appear to exhibit somewhat different dynamics of resource acquisition and allocation. There is mixed support that LW G. firmus eat more than their SW counterparts (Clark et al., 2015; Mole & Zera, 1994) and there is no evidence of flight‐related differences in feeding in G. rubens (Mole & Zera, 1993) or G. assimilis (Zera et al., 1998). However, flight capacity in four Gryllus species, including G. lineaticeps, reduces the efficiency by which ingested food is converted into body mass (Figure 3a; Mole & Zera, 1993, 1994; Zera et al., 1998) and flight‐capable G. lineaticeps are >40% less efficient at converting ingested food into reproductive tissue (Figure 3b). Thus, flight capacity diverts resources from body stores and reproductive tissue while also increasing energy use, which appears to leave LW(f) crickets in a very precarious energetic state. However, recent work in G. lineaticeps indicates that LW(f) crickets eat more food before adulthood relative to flight‐incapable crickets (Treidel et al., 2021). This temporal pattern of feeding may facilitate flight capacity by (1) fueling an increase in body size and features of flight morphology, including wing length and flight muscle mass, before adulthood, because such traits are fixed in size during adulthood, and (2) reducing flight load (body mass) during the dispersal phase of adulthood. Given the mass devoted to reproductive tissue and to filling the gastrointestinal tract, limiting feeding and reproductive investment by LW(f) females significantly reduces overall body mass—flight capacity reduced body mass by nearly 20% in the present study after controlling for body size (femur length). This, in turn, would promote the ability of LW(f) females to disperse away from low‐resource habitats (e.g., patches characterized by suboptimal temperatures, or limited food or mates).

The costs and benefits of flight investment vary across taxa (reviewed in Dingle, 2014). In Gryllus, the relative advantages of flight capacity are environment‐dependent (e.g., Glass & Stahlschmidt, 2019; Padda et al., 2021) and stable environments are predicted to favor the evolution of flightlessness in insects (Roff & Fairbairn, 1991; Roff, 1984). However, periods of food insecurity are expected to change in frequency and duration with global climate change (Ciais et al., 2005; Currano et al., 2008), and food may play an important role in the evolution of flightlessness in Gryllus. For example, a stable, constant supply of food during development reduces flight capacity in G. firmus (Glass & Stahlschmidt, 2019), and a greater intake of food and protein, in particular, is associated with reduced flight capacity in G. lineaticeps (Treidel et al., 2021). Flight capacity in G. firmus and G. lineaticeps also affects protein and carbohydrate regulation strategies (Clark et al., 2013, 2015, 2016; Treidel et al., 2021), and the effect of climate change on the quality or macronutrient composition of food may alter the relative advantages of different life history strategies (Lenhart, 2017). Ongoing climate change may also affect the evolution flightlessness in Gryllus via shifts in temperature. Warmer temperatures facilitate flying behavior (Sun et al., 2020) and the expression of the LW morph (Roff & Fairbairn, 2007), and flight capacity is also favored by a stable developmental temperature (Glass & Stahlschmidt, 2019). Therefore, wing‐dimorphic crickets may prove to be a valuable system to examine the roles of food, temperature, and circadian patterns in life‐history evolution in a changing world.

CONFLICT OF INTEREST

The author declares no conflict of interest.

Supporting information

Supplementary information.

Click here for additional data file. (16.7KB, docx)

ACKNOWLEDGMENT

I thank Alyssa Bonfoey for help with animal care.

Stahlschmidt, Z. R. (2022). Flight capacity drives circadian patterns of metabolic rate and alters resource dynamics. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 666–674. 10.1002/jez.2598

DATA AVAILABILITY STATEMENT

All data are available upon request.

REFERENCES

  1. Abhilash, L. , & Sharma, V. K. (2016). On the relevance of using laboratory selection to study the adaptive value of circadian clocks. Physiological Entomology, 41(4), 293–306. 10.1111/phen.12158 [DOI] [Google Scholar]
  2. Andere, C. , Palacio, M. A. , Rodriguez, E. M. , Figini, E. , Dominguez, M. T. , & Bedascarrasbure, E. (2002). Evaluation of the defensive behavior of two honeybee ecotypes using a laboratory test. Genetics and Molecular Biology, 25(1), 57–60. 10.1590/S1415-47572002000100011 [DOI] [Google Scholar]
  3. Banks, W. M. , Bruce, A. S. , & Peart, H. T. (1975). The effects of temperature, sex and circadian rhythm on oxygen consumption in two species of cockroaches. Comparative Biochemistry and Physiology–Part A: Physiology, 52(1), 223–227. 10.1016/S0300-9629(75)80157-5 [DOI] [PubMed] [Google Scholar]
  4. Birchard, G. F. , Nelson, N. J. , & Daugherty, C. H. (2006). A circadian rhythm in oxygen consumption rate in juvenile tuatara (Sphenodon punctatus). New Zealand Journal of Zoology, 33(3), 185–188. 10.1080/03014223.2006.9518443 [DOI] [Google Scholar]
  5. Blem, C. R. , & Killeen, K. B. (1993). Circadian metabolic cycles in eastern cottonmouths and brown water snakes. Journal of Herpetology, 27, 341–344. [Google Scholar]
  6. Bronikowski, A. , & Vleck, D. (2010). Metabolism, body size and life span: A case study in evolutionarily divergent populations of the garter snake (Thamnophis elegans). Integrative and Comparative Biology, 50(5), 880–887. 10.1093/icb/icq132 [DOI] [PubMed] [Google Scholar]
  7. Chacón, O. , Viana, M. T. , Farías, A. , Vazquez, C. , & García‐Esquivel, Z. (2003). Circadian metabolic rate and short‐term response of juvenile green abalone (Haliotis fulgens philippi) to three anesthetics. Journal of Shellfish Research, 22(2), 415–421. Retrieved from www.scopus.com [Google Scholar]
  8. Chung, M.‐T. , Jørgensen, K.‐M. , Trueman, C. N. , Knutsen, H. , Jorde, P. E. , & Grønkjær, P. (2021). First measurements of field metabolic rate in wild juvenile fishes show strong thermal sensitivity but variations between sympatric ecotypes. Oikos, 130(2), 287–299. 10.1111/oik.07647 [DOI] [Google Scholar]
  9. Ciais, P. , Reichstein, M. , Viovy, N. , Granier, A. , Ogée, J. , Allard, V. , Aubinet, M. , Buchmann, N. , Bernhofer, C. , Carrara, A. , Chevallier, F. , De Noblet, N. , Friend, A. D. , Friedlingstein, P. , Grünwald, T. , Heinesch, B. , Keronen, P. , Knohl, A. , Krinner, G. ,… Valentini, R. (2005). Europe‐wide reduction in primary productivity caused by the heat and drought in 2003. Nature, 437(7058), 529–533. 10.1038/nature03972 [DOI] [PubMed] [Google Scholar]
  10. Clark, R. M. , Zera, A. J. , & Behmer, S. T. (2015). Nutritional physiology of life‐history trade‐offs: How food protein‐carbohydrate content influences life‐history traits in the wing‐polymorphic cricket Gryllus firmus . Journal of Experimental Biology, 218(2), 298–308. 10.1242/jeb.112888 [DOI] [PubMed] [Google Scholar]
  11. Clark, R. M. , Zera, A. J. , & Behmer, S. T. (2016). Metabolic rate is canalized in the face of variable life history and nutritional environment. Functional Ecology, 30(6), 922–931. 10.1111/1365-2435.12574 [DOI] [Google Scholar]
  12. Clark, R. M. , McConnell, A. , Zera, A. J. , & Behmer, S. T. (2013). Nutrient regulation strategies differ between cricket morphs that trade‐off dispersal and reproduction. Functional Ecology, 27(5), 1126–1133. [Google Scholar]
  13. Crnokrak, P. , & Roff, D. A. (2002). Trade‐offs to flight capability in Gryllus firmus: The influence of whole‐organism respiration rate on fitness. Journal of Evolutionary Biology, 15(3), 388–398. 10.1046/j.1420-9101.2002.00401.x [DOI] [Google Scholar]
  14. Crozier, A. J. G. (1979). Diel oxygen uptake rhythms in diapausing pupae of Pieris brassicae and Papilio machaon . Journal of Insect Physiology, 25(8), 647–652. 10.1016/0022-1910(79)90114-8 [DOI] [Google Scholar]
  15. Currano, E. D. , Wilf, P. , Wing, S. L. , Labandeira, C. C. , Lovelock, E. C. , & Royer, D. L. (2008). Sharply increased insect herbivory during the Paleocene‐Eocene thermal maximum. Proceedings of the National Academy of Sciences of the United States of America, 105(6), 1960–1964. 10.1073/pnas.0708646105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. da Cruz, J. G. P. , Grimes, C. , Ronchi, D. L. , & da Cunha, V. P. (2008). The influence of circadian rhythms on the metabolism of the snake Bothrops jararaca (Serpentes, Viperidae). Acta Scientiarum–Biological Sciences, 30(3), 327–331. 10.4025/actascibiolsci.v30i3.5030 [DOI] [Google Scholar]
  17. Diawol, V. P. , Torres, M. V. , & Collins, P. A. (2016). Field evaluation of oxygen consumption by two freshwater decapod morphotypes (Trichodactylidae and Aeglidae); the effect of different times of the day, body weight and sex. Marine and Freshwater Behaviour and Physiology, 49(4), 251–263. 10.1080/10236244.2016.1190521 [DOI] [Google Scholar]
  18. Dingle, H. (2014). Migration: The biology of life on the move. Oxford University Press. [Google Scholar]
  19. Djawdan, M. , Rose, M. R. , & Bradley, T. J. (1997). Does selection for stress resistance lower metabolic rate? Ecology, 78(3), 828–837. 10.1890/0012-9658(1997)078[0828:DSFSRL]2.0.CO;2 [DOI] [Google Scholar]
  20. Djawdan, M. , Sugiyama, T. T. , Schlaeger, L. K. , Bradley, T. J. , & Rose, M. R. (1996). Metabolic aspects of the trade‐off between fecundity and longevity in Drosophila melanogaster . Physiological Zoology, 69(5), 1176–1195. 10.1086/physzool.69.5.30164252 [DOI] [Google Scholar]
  21. Ellis, H. I. , & Gabrielsen, G. W. (2019). Reassessing the definition of basal metabolic rate: Circadian considerations in avian studies. Comparative Biochemistry and Physiology–Part A: Molecular and Integrative Physiology, 237, 237. 10.1016/j.cbpa.2019.110541 [DOI] [PubMed] [Google Scholar]
  22. Gangloff, E. J. , Vleck, D. , & Bronikowski, A. M. (2015). Developmental and immediate thermal environments shape energetic trade‐offs, growth efficiency, and metabolic rate in divergent life‐history ecotypes of the garter snake Thamnophis elegans . Physiological and Biochemical Zoology, 88(5), 550–563. 10.1086/682239 [DOI] [PubMed] [Google Scholar]
  23. Glass, J. R. , & Stahlschmidt, Z. R. (2019). Should I stay or should I go? Complex environments influence the developmental plasticity of flight capacity and flight‐related trade‐offs. Biological Journal of the Linnean Society, 128(1), 59–69. 10.1093/biolinnean/blz073 [DOI] [Google Scholar]
  24. Glazier, D. S. (2005). Beyond the ‘3/4‐power law’: Variation in the intra‐ and interspecific scaling of metabolic rate in animals. Biological Reviews of the Cambridge Philosophical Society, 80(4), 611–662. [DOI] [PubMed] [Google Scholar]
  25. Glazier, D. S. (2015). Is metabolic rate a universal ‘pacemaker’ for biological processes? Biological Reviews, 90(2), 377–407. 10.1111/brv.12115 [DOI] [PubMed] [Google Scholar]
  26. Guerra, P. A. (2011). Evaluating the life‐history trade‐off between dispersal capability and reproduction in wing dimorphic insects: A meta‐analysis. Biological Reviews, 86(4), 813–835. 10.1111/j.1469-185X.2010.00172.x [DOI] [PubMed] [Google Scholar]
  27. Harrison, J. F. , Woods, H. A. , & Roberts, S. P. (2012). Ecological and environmental physiology of insects (Vol. 3). Oxford University Press. [Google Scholar]
  28. Hori, K. , Zhang, Q.‐H. , Li, H.‐C. , & Saito, S. (1995). Variation of growth rate of a rat tumour during a light‐dark cycle: Correlation with circadian fluctuations in tumour blood flow. British Journal of Cancer, 71(6), 1163–1168. 10.1038/bjc.1995.227 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Humphreys, W. F. (1977). Respiration studies on Geolycosa godeffroyi (Araneae: Lycosidae) and their relationship to field estimates of metabolic heat loss. Comparative Biochemistry and Physiology–Part A: Physiology, 57(2), 255–263. 10.1016/0300-9629(77)90468-6 [DOI] [Google Scholar]
  30. Jacot, A. , Scheuber, H. , Holzer, B. , Otti, O. , & Brinkhof, M. W. G. (2008). Diel variation in a dynamic sexual display and its association with female mate‐searching behaviour. Proceedings of the Royal Society B: Biological Sciences, 275(1634), 579–585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jakobsen, H. H. , & Strom, S. L. (2004). Circadian cycles in growth and feeding rates of heterotrophic protist plankton. Limnology and Oceanography, 49(6), 1915–1922. 10.4319/lo.2004.49.6.1915 [DOI] [Google Scholar]
  32. Kim, W. S. , Kim, J. M. , Yi, S. K. , & Huh, H. T. (1997). Endogenous circadian rhythm in the river puffer fish Takifugu obscurus . Marine Ecology Progress Series, 153(1‐3), 293–298. 10.3354/meps153293 [DOI] [Google Scholar]
  33. Klein, W. , Perry, S. F. , Abe, A. S. , & Andrade, D. V. (2006). Metabolic response to feeding in Tupinambis merianae: Circadian rhythm and a possible respiratory constraint. Physiological and Biochemical Zoology, 79(3), 593–601. 10.1086/502818 [DOI] [PubMed] [Google Scholar]
  34. Ksia̧zek, A. , Konarzewski, M. , & Łapo, I. B. (2004). Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiological and Biochemical Zoology, 77(6), 890–899. 10.1086/425190 [DOI] [PubMed] [Google Scholar]
  35. Lenhart, P. A. (2017). Using plant nutrient landscapes to assess Anthropocene effects on insect herbivores. Current Opinion in Insect Science, 23, 51–58. [DOI] [PubMed] [Google Scholar]
  36. Levy, K. , Wegrzyn, Y. , Efronny, R. , Barnea, A. , & Ayali, A. (2021). Lifelong exposure to artificial light at night impacts stridulation and locomotion activity patterns in the cricket Gryllus bimaculatus . Proceedings of the Royal Society B: Biological Sciences, 288(1959), 20211626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lighton, J. R. B. (2008). Measuring metabolic rates: A manual for scientists (pp. 1–216). Oxford University Press. 10.1093/acprof:oso/9780195310610.001.0001 [DOI] [Google Scholar]
  38. Loher, W. (1979). Circadian rhythmicity of locomotor behavior and oviposition in female Teleogryllus commodus . Behavioral Ecology and Sociobiology, 5(3), 253–262. [Google Scholar]
  39. Masoero, G. , Laaksonen, T. , Morosinotto, C. , & Korpimäki, E. (2020). Climate change and perishable food hoards of an avian predator: Is the freezer still working? Global Change Biology, 26(10), 5414–5430. 10.1111/gcb.15250 [DOI] [PubMed] [Google Scholar]
  40. Mole, S. , & Zera, A. J. (1993). Differential allocation of resources underlies the dispersal‐reproduction trade‐off in the wing‐dimorphic cricket, Gryllus rubens . Oecologia, 93(1), 121–127. 10.1007/BF00321201 [DOI] [PubMed] [Google Scholar]
  41. Mole, S. , & Zera, A. J. (1994). Differential resource consumption obviates a potential flight‐fecundity trade‐off in the sand cricket (Gryllus firmus). Functional Ecology, 8(5), 573–580. 10.2307/2389917 [DOI] [Google Scholar]
  42. Mortola, J. P. , & Lanthier, C. (2004). Scaling the amplitudes of the circadian pattern of resting oxygen consumption, body temperature and heart rate in mammals. Comparative Biochemistry and Physiology–A Molecular and Integrative Physiology, 139(1), 83–95. 10.1016/j.cbpb.2004.07.007 [DOI] [PubMed] [Google Scholar]
  43. Nespolo, R. F. , Castañeda, L. E. , & Roff, D. A. (2005). The effect of fasting on activity and resting metabolism in the sand cricket, Gryllus firmus: A multivariate approach. Journal of Insect Physiology, 51(1), 61–66. 10.1016/j.jinsphys.2004.11.005 [DOI] [PubMed] [Google Scholar]
  44. Nespolo, R. F. , Roff, D. A. , & Fairbairn, D. J. (2008). Energetic trade‐off between maintenance costs and flight capacity in the sand cricket (Gryllus firmus). Functional Ecology, 22(4), 624–631. 10.1111/j.1365-2435.2008.01394.x [DOI] [Google Scholar]
  45. Padda, S. S. , Glass, J. R. , & Stahlschmidt, Z. R. (2021). When it's hot and dry: Life‐history strategy influences the effects of heat waves and water limitation. Journal of Experimental Biology, 224(7)​. 10.1242/jeb.236398 [DOI] [PubMed] [Google Scholar]
  46. Panda, S. , Antoch, M. P. , Miller, B. H. , Su, A. I. , Schook, A. B. , Straume, M. , & Hogenesch, J. B. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell, 109(3), 307–320. 10.1016/S0092-8674(02)00722-5 [DOI] [PubMed] [Google Scholar]
  47. Reddy, P. S. , & Bhagyalakshmi, A. (1994). Elimination of diurnal rhythm of respiration by methyl parathion in the crab, Oziotelphusa senex senex fabricius . Bulletin of Environmental Contamination and Toxicology, 53(2), 192–197. 10.1007/BF00192032 [DOI] [PubMed] [Google Scholar]
  48. Riede, S. J. , Van Der Vinne, V. , & Hut, R. A. (2017). The flexible clock: Predictive and reactive homeostasis, energy balance and the circadian regulation of sleep‐wake timing. Journal of Experimental Biology, 220(5), 738–749. 10.1242/jeb.130757 [DOI] [PubMed] [Google Scholar]
  49. Roe, J. H. , Hopkins, W. A. , & Talent, L. G. (2005). Effects of body mass, feeding, and circadian cycles on metabolism in the lizard Sceloporus occidentalis . Journal of Herpetology, 39(4), 595–603. 10.1670/75-05A.1 [DOI] [Google Scholar]
  50. Roe, J. H. , Hopkins, W. A. , Snodgrass, J. W. , & Congdon, J. D. (2004). The influence of circadian rhythms on pre‐ and post‐prandial metabolism in the snake Lamprophis fuliginosus . Comparative Biochemistry and Physiology–A Molecular and Integrative Physiology, 139(2), 159–168. 10.1016/j.cbpb.2004.08.005 [DOI] [PubMed] [Google Scholar]
  51. Roff, D. A. (1984). The cost of being able to fly: A study of wing polymorphism in two species of crickets. Oecologia, 63(1), 30–37. 10.1007/BF00379781 [DOI] [PubMed] [Google Scholar]
  52. Roff, D. A. (1991). Life history consequences of bioenergetic and biomechanical constraints on migration. American Zoologist, 31(1), 205–215. Retrieved from www.scopus.com [Google Scholar]
  53. Roff, D. A. , & Fairbairn, D. J. (1991). Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. American Zoologist, 31(1), 243–251. 10.1093/icb/31.1.243 [DOI] [Google Scholar]
  54. Roff, D. A. , & Fairbairn, D. J. (2007). Laboratory evolution of the migratory polymorphism in the sand cricket: Combining physiology with quantitative genetics. Physiological and Biochemical Zoology, 80(4), 358–369. 10.1086/518012 [DOI] [PubMed] [Google Scholar]
  55. Rosas, C. , Sanchez, A. , Escobar, E. , Soto, L. , & Bolongaro‐Crevenna, A. (1992). Daily variations of oxygen consumption and glucose hemolymph level related to morphophysiological and ecological adaptations of crustacea. Comparative Biochemistry and Physiology–Part A: Physiology, 101(2), 323–328. 10.1016/0300-9629(92)90540-7 [DOI] [Google Scholar]
  56. Ross, L. G. , & McKinney, R. W. (1988). Respiratory cycles in Oreochromis niloticus (L.), measured using a six‐channel microcomputer‐operated respirometer. Comparative Biochemistry and Physiology–Part A: Physiology, 89(4), 637–643. 10.1016/0300-9629(88)90846-8 [DOI] [Google Scholar]
  57. Rost, R. , & Honegger, H. W. (1987). The timing of premating and mating behavior in a field population of the cricket Gryllus campestris L . Behavioral Ecology and Sociobiology, 21(5), 279–289. [Google Scholar]
  58. Rouleau, S. , Glémet, H. , & Magnan, P. (2010). Effects of morphology on swimming performance in wild and laboratory crosses of brook trout ecotypes. Functional Ecology, 24(2), 310–321. 10.1111/j.1365-2435.2009.01636.x [DOI] [Google Scholar]
  59. Royauté, R. , Berdal, M. A. , Garrison, C. R. , & Dochtermann, N. A. (2018). Paceless life? A meta‐analysis of the pace‐of‐life syndrome hypothesis. Behavioral Ecology and Sociobiology, 72(3), 64. 10.1007/s00265-018-2472-z [DOI] [Google Scholar]
  60. Schwartz, T. S. , Arendsee, Z. W. , & Bronikowski, A. M. (2015). Mitochondrial divergence between slow‐ and fast‐aging garter snakes. Experimental Gerontology, 71, 135–146. [DOI] [PubMed] [Google Scholar]
  61. Secor, S. M. (2009). Specific dynamic action: A review of the postprandial metabolic response. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 179(1), 1–56. 10.1007/s00360-008-0283-7 [DOI] [PubMed] [Google Scholar]
  62. Sen, A. , & Hoffmann, H. M. (2020). Role of core circadian clock genes in hormone release and target tissue sensitivity in the reproductive axis. Molecular and Cellular Endocrinology, 501, 501. 10.1016/j.mce.2019.110655 [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Shigler, H. Y. , Magory Cohen, T. , Ben‐Shimol, E. , Ben‐Betzalel, R. , & Levin, E. (2021). Juvenile hormone functions as a metabolic rate accelerator in bumble bees (Bombus terrestris). Hormones and Behavior, 136, 105073. [DOI] [PubMed] [Google Scholar]
  64. Shipp, E. , & Otton, J. (1976). Irradiation induced changes in circadian DDT susceptibility and metabolic rhythms in the housefly. International Journal of Chronobiology, 4(2), 71–81. www.scopus.com [PubMed] [Google Scholar]
  65. Sokolove, P. G. (1975). Locomotory and stridulatory circadian rhythms in the cricket, Teleogryllus commodus . Journal of Insect Physiology, 21(3), 537–558. [DOI] [PubMed] [Google Scholar]
  66. Stahlschmidt, Z. R. , & Glass, J. R. (2020). Life history and immune challenge influence metabolic plasticity to food availability and acclimation temperature. Physiological and Biochemical Zoology, PBZ, 93(4), 271–281. 10.1086/709587 [DOI] [PubMed] [Google Scholar]
  67. Stoltey, T. , & Shillington, C. (2009). Metabolic rates and movements of the male tarantula Aphonopelma anax during the mating season. Canadian Journal of Zoology, 87(12), 1210–1220. 10.1139/Z09-111 [DOI] [Google Scholar]
  68. Sun, B. , Huebner, C. , Treidel, L. A. , Clark, R. M. , Roberts, K. T. , Kenagy, G. J. , & Williams, C. M. (2020). Nocturnal dispersal flight of crickets: Behavioural and physiological responses to cool environmental temperatures. Functional Ecology, 34(9), 1907–1920. 10.1111/1365-2435.13615 [DOI] [Google Scholar]
  69. Svendsen, J. C. , Genz, J. , Anderson, W. G. , Stol, J. A. , Watkinson, D. A. , & Enders, E. C. (2014). Evidence of circadian rhythm, oxygen regulation capacity, metabolic repeatability and positive correlations between forced and spontaneous maximal metabolic rates in lake sturgeon Acipenser fulvescens . PLoS One, 9(4), 94693. 10.1371/journal.pone.0094693 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tomioka, K. , & Chiba, Y. (1989). Light cycle during post‐embryonic development affects adult circadian parameters of the cricket (Gryllus bimaculatus) optic lobe pacemaker. Journal of Insect Physiology, 35(4), 273–276. [Google Scholar]
  71. Treidel, L. A. , Clark, R. M. , Lopez, M. T. , & Williams, C. M. (2021). Physiological demands and nutrient intake modulate a trade‐off between dispersal and reproduction based on age and sex of field crickets. Journal of Experimental Biology, 224(7), art. no jeb237834. [DOI] [PubMed] [Google Scholar]
  72. Treidel, L. A. , Clark, R. M. , Lopez, M. T. , & Williams, C. M. (2021). Physiological demands and nutrient intake modulate a trade‐off between dispersal and reproduction based on age and sex of field crickets. Journal of Experimental Biology, 224(7)​, 10.1242/jeb.237834 [DOI] [PubMed] [Google Scholar]
  73. Van Senus, P. (1985). The effects of temperature, size, season and activity on the metabolic rate of the amphipod, Talorchestia capensis (Crustaea, Talitridae). Comparative Biochemistry and Physiology Part A: Physiology, 81(2), 263–269. 10.1016/0300-9629(85)90133-1 [DOI] [Google Scholar]
  74. Weissman, D. B. , & Gray, D. A. (2019). Crickets of the genus Gryllus in the United States (Orthoptera: Gryllidae: Gryllinae). Zootaxa, 4705(1), 1–277. 10.11646/zootaxa.4705.1.1 [DOI] [PubMed] [Google Scholar]
  75. Woodring, J. P. , & Clifford, C. W. (1986). Development and relationships of locomotor, feeding, and oxygen consumption rhythms in house crickets. Physiological Entomology, 11(1), 89–96. 10.1111/j.1365-3032.1986.tb00393.x [DOI] [Google Scholar]
  76. Xu, K. , DiAngelo, J. R. , Hughes, M. E. , Hogenesch, J. B. , & Sehgal, A. (2011). The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metabolism, 13(6), 639–654. 10.1016/j.cmet.2011.05.001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Yeung, J. , & Naef, F. (2018). Rhythms of the genome: Circadian dynamics from chromatin topology, tissue‐specific gene expression, to behavior. Trends in Genetics, 34(12), 915–926. 10.1016/j.tig.2018.09.005 [DOI] [PubMed] [Google Scholar]
  78. Zera, A. J. (2005). Intermediary metabolism and life history trade‐offs: Lipid metabolism in lines of the wing‐polymorphic cricket, Gryllus firmus, selected for flight capability vs. early age reproduction. Integrative and Comparative Biology, 45(3), 511–524. 10.1093/icb/45.3.511 [DOI] [PubMed] [Google Scholar]
  79. Zera, A. J. , & Mole, S. (1994). The physiological costs of flight capability in wing‐dimorphic crickets. Researches on Population Ecology, 36(2), 151–156. 10.1007/BF02514930 [DOI] [Google Scholar]
  80. Zera, A. J. , & Larsen, A. (2001). The metabolic basis of life history variation: Genetic and phenotypic differences in lipid reserves among life history morphs of the wing‐polymorphic cricket, Gryllus firmus . Journal of Insect Physiology, 47(10), 1147–1160. 10.1016/S0022-1910(01)00096-8 [DOI] [PubMed] [Google Scholar]
  81. Zera, A. J. , Sall, J. , & Grudzinski, K. (1997). Flight‐muscle polymorphism in the cricket Gryllus firmus: Muscle characteristics and their influence on the evolution of flightlessness. Physiological Zoology, 70(5), 519–529. 10.1086/515865 [DOI] [PubMed] [Google Scholar]
  82. Zera, A. J. , Potts, J. , & Kobus, K. (1998). The physiology of life‐history trade‐offs: Experimental analysis of a hormonally induced life‐history trade‐off in Gryllus assimilis . American Naturalist, 152(1), 7–23. 10.1086/286146 [DOI] [PubMed] [Google Scholar]
  83. Zera, A. J. , Zhao, Z. , & Kaliseck, K. (2007). Hormones in the field: Evolutionary endocrinology of juvenile hormone and ecdysteroids in field populations of the wing‐dimorphic cricket Gryllus firmus . Physiological and Biochemical Zoology, 80(6), 592–606. [DOI] [PubMed] [Google Scholar]
  84. Zera, A. J. , Vellichirammal, N. N. , & Brisson, J. A. (2018). Diurnal and developmental differences in gene expression between adult dispersing and flightless morphs of the wing polymorphic cricket, Gryllus firmus: Implications for life‐history evolution. Journal of Insect Physiology, 107, 233–243. 10.1016/j.jinsphys.2018.04.003 [DOI] [PubMed] [Google Scholar]
  85. Zhao, Z. , & Zera, A. J. (2004). The hemolymph JH titer exhibits a large‐amplitude, morph‐dependent, diurnal cycle in the wing‐polymorphic cricket, Gryllus firmus . Journal of Insect Physiology, 50(1), 93–102. 10.1016/j.jinsphys.2003.10.003 [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary information.

Click here for additional data file. (16.7KB, docx)

Data Availability Statement

All data are available upon request.

Articles from Journal of Experimental Zoology. Part A, Ecological and Integrative Physiology are provided here courtesy of Wiley

RESOURCES