Energetic and physiological correlates of prey handling and ingestion in lizards and snakes

In this review, we summarize the energetic and physiological correlates of prey handling and ingestion in lizards and snakes. There were marked differences in the magnitude of aerobic metabolism during prey handling and ingestion between these two groups, although they show a similar pattern of variation as a function of relative prey mass. For lizards, the magnitude of aerobic metabolism during prey handling and ingestion also varied as a function of morphological specializations for a particular habitat, prey type, and behavior. For snakes, interspecific differences in aerobic metabolism during prey handling seem to be correlated with adaptations for prey capture (venom injection vs. constriction). During ingestion by snakes, differences in aerobic metabolism might be due to differences in cranial morphology, although allometric effects might be a potentially confounded effect. Anaerobic metabolism is used for prey handling and ingestion, but its relative contribution to total ATP production seems to be more pronounced in snakes than in lizards. The energetic costs of prey handling and ingestion are trivial for both groups and cannot be used to predict patterns of prey-size selection. For lizards, it seems that morphological and ecological factors set the constraints on prey handling and ingestion. For snakes, besides these two factors, the capacity of the cardio-respiratory system may also be an important factor constraining the capacity for prey handling and ingestion.     

Historical contingency and behavioural divergence in territorial Anolis lizards

The extent that evolution - including adaptation - is historically contingent (dependent on past events) has often been hotly debated, but is still poorly understood. In particular, there are little data on the degree that behaviour, an aspect of the phenotype that is strongly linked to contemporary environments (social or physical), retains the imprint of evolutionary history. In this study, I examined whether differences in the design of the territorial displays among species of Caribbean Anolis lizards reflect island-specific selection regimes, or historically contingent predispositions associated with different clade histories. Adult males advertise territory ownership using a series of headbobs and dewlap extensions, bouts of which vary in duration among species. When display durations were mapped onto the Anolis phylogeny, prominent differences between species belonging to the Western and Eastern Caribbean radiations were apparent. Statistical analyses confirmed that species differences in the duration of headbob displays, and to some extent the duration of dewlap extensions, were historically contingent. The unique evolutionary histories of each clade have seemingly had a profound effect on the subsequent direction of display evolution among descendent taxa. These results combined with those from previous studies on these lizards show that past history can have an important impact on the type of behaviour exhibited by species today, to the point that adaptive evolution can proceed quite differently in lineages originating from different evolutionary starting points.     

Activity metabolism of lizards after thermal acclimation

1. 1. I tested the hypothesis that thermal acclimation necessarily exerts the same effect on resting metabolism and on aerobic and anaerobic activity metabolism in Anolis carolinensis and Sceloporus jarrovi, diurnally active iguanid lizards that exhibit reduced winter activity but not prolonged dormancy and that are often active on warm winter days.

2. 2. Cold acclimation reduced the total metabolic scope for activity in these lizards by 33–40%. The benefits of winter activity must outweigh the increased risk of predation that presumably accompanies this reduction in capacity for intense, short term muscular exercise.

3. 3. Acclimation did not influence resting metabolism, aerobic activity metabolism, and anaerobic activity metabolism in parallel ways.

Dawn and dusk "chorus" in visually communicating Jamaican anole lizards

A key hypothesis explaining the existence of dawn and dusk choruses in acoustically communicating animals centers on the need to advertise continued territorial occupancy after and before a period of nocturnal inactivity. If this hypothesis is correct, it follows that similar dawn and dusk choruses should occur in territorial animals exploiting other signal modalities. Adult male Anolis lizards defend territories by using elaborate head-bobbing displays and extensions of a throat fan or dewlap. Males are inactive at night and return to their territories at dawn, remaining there until dusk. I quantified the production of visual displays as a function of time of day for four species on the island of Jamaica: Anolis lineatopus, Anolis sagrei, Anolis grahami, and Anolis opalinus. All exhibited dawn and/or dusk peaks in display behavior. These patterns have remarkable parallels with the dawn and dusk choruses reported for many acoustically communicating animals.     

Mite load predicts the quality of sexual color and locomotor performance in a sexually dichromatic lizard

Since Darwin, the maintenance of bright sexual colors has recurrently been linked to mate preference. However, the mechanisms underpinning such preferences for bright colors would not be resolved for another century. Likely, the idea of selection for colors that could decrease the chances of survival (e.g., flashy colors that can inadvertently attract predators) was perceived as counterintuitive. It is now widely accepted that these extreme colors often communicate to mates the ability to survive despite a “handicap” and act as honest signals of individual quality when they are correlated with the quality of other traits that are directly linked to individual fitness. Sexual colors in males are frequently perceived as indicators of infection resistance, in particular. Still, there remains considerable discord among studies attempting to parse the relationships between the variables associating sexual color and infection resistance, such as habitat type and body size. This discord may arise from complex interactions between these variables. Here, we ask if sexual color in male Florida scrub lizards (Sceloporus woodi) is an honest signal of resistance to chigger mite infection. To this end, we use linear modeling to explore relationships between mite load, different components of sexual color, ecological performance, body size, and habitat type. Our data show that that the brightness of sexual color in scrub lizards is negatively associated with the interaction between mite load and body size, and scrub lizards suffer decreased endurance capacity with increases in mite load. Our data also indicate that mite load, performance, and sexual color in male scrub lizards can vary between habitat types. Collectively, these results suggest that sexual color in scrub lizards is an honest indicator of individual quality and further underscore the importance of considering multiple factors when testing hypotheses related to the maintenance of sexual color.     

Seasonal variations in activity,aerobic energetic capacities,and plasma thyroid hormones (T3 and T4) in an iguanid lizard

Summary Dipsosaurus dorsalis were collected at approximately monthly intervals over 2 years for measurements of plasma concentrations of thyroxine (T4) and triiodothyronine (T3) in field-active lizards. Additionally, lizards were collected at four times of the year for an assessment of seasonal variations in standard (SMR) and maximal ( max) rates of O₂ consumption, tissue oxidative capacity, and locomotor endurance capacity. All measured variables were lowest in animals retrieved from hibernation. During the active season, plasma T4 was highest in the spring and late summer and was significantly lower in early and middle summer. Plasma T3 underwent similar seasonal variations, but the late summer resurgence was less pronounced than for T4. There was a significant correlation between plasma T4 and T3 on an individual basis during the active season. Standard metabolic rate was highest in newly emerged animals and decreased progressively during the active season. There was no association between plasma thyroid hormones and standard metabolism in field-active lizards, contrary to expectations based on previous experimental studies. Maximal , hepatic and mixed hind-limb muscle mass-specific citrate synthase activity, and endurance underwent patterns of seasonal variation similar to the pattern of variation in thyroid hormones. These data suggest that thyroid hormones may be involved in the regulation of aerobic energetic capacities in field-active lizards, consistent with previous experimental reports. High endurance capacity may have been important in selection for metabolic responses to thyroid hormones.Abbreviations CSA citrate synthase activity - SMR standard metabolic rate - T3 triiodothyronine - T4 thyroxine     

Anaerobic metabolism during activity in lizards

Summary A new technique developed for the determination of total lactate production in small animals was used to evaluate the role of anaerobiosis during activity at different temperatures in lizards. Measurements on six species of small lizards indicate little interspecific variation or thermal effect in resting lactate levels (0.35 mg lactate/g body weight) or maximal lactate levels achieved at exhaustion (1.4 mg lactate/g). Normally activeAnolis in captivity had a lactate content of 0.5 mg lactate/g. Rates of lactate formation were most rapid during the first 30 sec of activity and had a low thermal dependence (Q₁₀=1.1–1.3 above 20 °C). The lactate formed during activity persists for long periods; e.g., for 30 to 60 min between 20 and 37 °C inAnolis carolinensis (Fig. 1). Recovery rate generally increases with temperature. Muscle lactate concentrations peak at the end of activity, but liver and blood lactate are not maximal until 10 and 30 min, respectively, after activity (Fig. 2). The decrease in the blood lactate is shown to be a poor estimator of total recovery. An estimated 80–90% of the total energy utilized during initial vigorous activity comes from anaerobic sources. Because of its low thermal dependence, anaerobiosis permits high levels of activity in lizards at all body temperatures without requiring high levels of aerobic resting metabolism.Support for this research was provided by a Miller Post-doctoral Research Felowship to AFB and NSF Grant GB 22642 to PL.     

Intermittent locomotion increases endurance in a gecko

Nocturnal geckos can actively forage at low temperatures. A low minimum cost of locomotion allows greater sustainable speeds by partially offsetting the decrease in maximal oxygen consumption (VO2max) associated with low nocturnal temperatures. The nocturnality hypothesis (Autumn et al. 1997) proposes that the reduced cost of continuous locomotion is a shared, derived characteristic that increases the capacity to sustain locomotion at low temperatures. Yet many lizards move intermittently at speeds exceeding those that elicit VO2max. We exercised the frog-eyed gecko, Teratoscincus przewalskii, continuously and intermittently on a treadmill. At an exercise speed of 0.90 km h-1 (270% maximum aerobic speed), lizards alternating a 15-s exercise period with a 30-s pause period exhibited a 1.7-fold increase in distance capacity (total distance traveled before fatigue) compared with lizards exercised continuously at the same average speed (0.30 km h-1). The average aerobic cost of intermittent exercise was not significantly different from VO2max. Locomoting intermittently could augment the increase in endurance resulting from the low minimum cost of continuous locomotion in nocturnal geckos. Intermittent behavior could increase the endurance of lizard movement in general.     

Timing of prenuptial molt as a sexually selected indicator of male quality in superb fairy-wrens (Malurus cyaneus)

Seasonally dichromatic male superb fairy-wrens (Malurus cyaneus)solicit extra-group fertilizations through displays of theirbrightly colored nuptial plumage during visits to females inneighboring territories. This ornamental plumage is lost atthe end of the breeding season, and reacquired before the nextbreeding season after a highly variable period spent in a cryptic,female-like, "eclipse" plumage. Individuals start visiting femalesas soon as they return to nuptial plumage, often several monthsbefore the start of breeding.We examine variation in the timingof acquisition of nuptial plumage in relation to environmentalconditions and the age, social status, and condition of males.We show that males undergo the prenuptial molt earlier as theyage and when in superior condition, and that molt is delayedin years of more adverse winter weather conditions. We proposethat the purpose of male displays may be to advertise theirquality, and that females use this variation in the timing ofacquisition of nuptial plumage to assess the relative qualityof prospective extra-group mates. Molting earlier is apparentlycostlier, so this handicap would appear to be a reliable reflectionof male quality.     

Variation in metabolic rate between populations of a geographically widespread lizard

In geographically widespread ectotherms, variation in life history phenotypes may be caused by differences in maintenance metabolism of individuals. I estimated daily and annual maintenance metabolism of eastern fence lizards, Sceloporus undulatus, from two populations with markedly different life histories; lizards in South Carolina grow faster, mature earlier, and have greater annual reproductive output than lizards in New Jersey. I measured diel cycles of resting metabolic rate (RMR) at four temperatures (20 degrees, 30 degrees, 33 degrees, and 36 degrees C) during spring, summer, and fall. In all seasons, RMR increased significantly from 20 degrees to 33 degrees C but did not differ significantly between 33 degrees and 36 degrees C. Adults from New Jersey had a higher RMR than adults from South Carolina in summer and fall but not in spring. Juveniles from South Carolina had a higher RMR than juveniles from New Jersey in summer but not in spring or fall. Annual maintenance metabolism of New Jersey lizards (53.7 kJ) was greater than that of South Carolina lizards (45.8 kJ), despite the shorter duration of activity in New Jersey. I conclude that the difference in maintenance metabolism between populations contributes to the greater production by S. undulatus in South Carolina.     

The influence of muscle metabolic characteristics on physical performance

This study describes the influence of muscle fiber type composition, enzyme activities and capillary supply on muscle strength, local muscle endurance or aerobic power and capacity. Muscle biopsies were obtained from m. vastus lateralis in thirteen physically active men. Histochemical staining procedures were applied to assess the percentage of fast twitch (FT) fibers, muscle fiber area, and capillary density. Also, the activity of citrate synthase (CS), creatine kinase (CK), hexokinase (HK), lactate dehydrogenase (LDH), and phosphofructokinase (PFK) were analysed using fluorometrical assays. Peak torque at 'low' and 'high' angular velocities was measured during leg extension. Similarly, muscle fatigue (e.g. peak torque decline) and recovery from a short-term exercise task were measured during maximal, voluntary consecutive leg extensions. Aerobic power (VO2max) and aerobic capacity (e.g. onset of blood lactate concentration; OBLA), as defined by a blood lactate concentration of 4 mol X 1(-1) were measured during cycling. Peak torque at a high angular velocity was positively correlated with % FT area (p less than 0.001). Fatigue and recovery were correlated with LDH X CS-1 (p less than 0.001). WOBLA was best correlated with PFK and PFK X CS-1 (p less than 0.001). Hence, muscle strength was partly determined by fiber type composition whereas local muscle endurance, recovery and aerobic capacity reflect mainly capillary supply and the activity of key enzymes involved in aerobic and anaerobic metabolism.     

Behavioural mating displays depend on mitochondrial function: a potential mechanism for linking behaviour to individual condition

Males of many animal species court females using complex behavioural displays that are challenging to produce, and some of these displays have been shown to be associated with aspects of male quality. However, the mechanisms by which behavioural displays are linked to individual condition remain uncertain. Herein, we illustrate fundamental mechanistic connections between mitochondrial function and neurogenesis, energy production, and a variety of pathways that underlie the ability of an individual to perform complex behaviours. We consider the biomedical evidence for how mitochondrial activity shapes neurogenesis during development and neural function in adulthood, and how both genetics and environmental conditions can cause variation in mitochondrial function in wild animals. An individual's mitochondrial phenotype determines not just metabolism and available energy, but also appears to serve as an important driver of capacity to perform cognitively complex and other challenging display behaviours. We apply this concept to the example of birdsong, a well‐studied display behaviour with known links to neural pathways, and we describe how mitochondrial involvement in a variety of important internal processes creates links between display quality and key traits like immunocompetence. By synthesizing the intimate involvement of mitochondria in neural processes with the physiological bases of display behaviour, we aim to provide new mechanistic explanations for information that females may gain by assessing complex male displays.     

Metabolic implications of a 'run now,pay later' strategy in lizards: an analysis of post-exercise oxygen consumption

Lizards and many other animals often engage in locomotor behaviors that are of such short duration that physiological steady-state conditions are not attained. It is sometimes difficult to estimate the energetic costs of this type of locomotor activity. This difficulty is addressed by considering as reflective of the metabolic cost of activity (C(act)) not only the oxygen consumed during the activity itself, but also the excess post-exercise oxygen consumption (EPOC) and any excess metabolites persisting at the end of EPOC. Data from both lizards and mammals demonstrate that EPOC is the major energetic cost when activity is short and intense. This paper evaluates the major metabolic components of EPOC in lizards. We then examine how behavioral variables associated with locomotion (duration, intensity, frequency) can influence EPOC and C(act). Short and intense activity is much more expensive by this measure than is steady-state locomotion. Evidence is provided that intermittent activity of short duration can be more economical relative to single bouts of the same activity. Metabolic savings appear greatest when the pause period between behaviors is short. In contrast, endurance is enhanced by short activity periods and longer pause periods, suggesting a tradeoff between endurance and EPOC-related metabolic costs.     

Nestling testosterone is associated with begging behaviour and fledging success in the pied flycatcher, Ficedula hypoleuca

Animal signals are hypothesized to be costly in order to honestly reflect individual quality. Offspring solicitation signals given by nestling birds are thought to have evolved to advertise either need or individual quality. We tested the potential role of testosterone (T) in controlling the intensity of these signals by measuring begging behaviour as: (i) duration of the begging display and (ii) maximum height of the begging stretch, and by sampling endogenous T levels in nestling blood. We tested nestling pied flycatchers (Ficedula hypoleuca) using well-established experimental paradigm involving transient food deprivation to encourage begging behaviour and then blood-sampled nestlings at the end of these tests for T levels. Our results show that individual nestlings with the most intense begging displays had the highest circulating levels of T immediately after testing. In addition, we found substantial differences between broods in terms of circulating T. Finally, we found evidence that broods with higher levels of T showed increased fledging success, indicating a benefit for increased T production in nestlings. The potential trade-offs involved in T-mediated begging behaviour are discussed.     

Postnatal changes of some enzymatic activities of energy supplying metabolism in the cortex, inner and outer medulla of the rat kidney

1. In rat kidney cortex, outer and inner medulla the development of activities of seven enzymes was investigated during postnatal ontogeny (10, 20, 30, 60 and 90 days of age). The enzymes were selected in such a manner, as to characterize most of the main metabolic pathways of energy supplying metabolism: hexokinase (glucose phosphorylation, HK), glycerol-3-phosphate dehydrogenase (glycerolphosphate metabolism or shunt, GPDH), triose phosphate dehydrogenase (glycolytic carbohydrate breakdown, TPDH), lactate dehydrogenase (lactate metabolism, LDH), citrate synthase (tricarboxylic acid cycle, aerobic metabolism, CS), malate NAD dehydrogenase (tricarboxylic acid cycle, intra-extra mitochondrial hydrogen transport, MDH) and 3-hydroxyacyl-CoA-dehydrogenase (fatty acid catabolism, HOADH). 2. The renal cortex already differs metabolically from the medullar structures on the 10th day of life. It displays a high activity of aerobic breakdown of both fatty acids and carbohydrates. Its metabolic capacity further increases up to the 30th day of life. 3. The outer medullar structure is not grossly different from the inner medulla on the 10th day of life. Further it differentiates into a highly aerobic tissue mainly able to utilize carbohydrates. It can, however, to some extent, also utilize fatty acids aerobically and produce lactate from carbohydrates anaerobically. 4. The inner medullar structure is best equipped to utilize carbohydrates by anaerobic glycolysis, forming lactate. This feature is already pronounced on the 10th day of life, its capacity increases to some extent during postnatal development, being highest between the 10th and the 60th day of life.     

Improved exercise performance and increased aerobic capacity after endurance training of patients with stable polymyositis and dermatomyositis

Introduction

This randomized, controlled study on patients with polymyositis or dermatomyositis was based on three hypotheses: patients display impaired endurance due to reduced aerobic capacity and muscle weakness, endurance training improves their exercise performance by increasing the aerobic capacity, and endurance training has general beneficial effects on their health status.

Methods

In the first part of this study, we compared 23 patients with polymyositis or dermatomyositis with 12 age- and gender-matched healthy controls. A subgroup of patients were randomized to perform a 12-week endurance training program (exercise group, n = 9) or to a non-exercising control group (n = 6). We measured maximal oxygen uptake (VO₂ max) and the associated power output during a progressive cycling test. Endurance was assessed as the cycling time to exhaustion at 65% of VO₂ max. Lactate levels in the vastus lateralis muscle were measured with microdialysis. Mitochondrial function was assessed by measuring citrate synthase (CS) and β-hydroxyacyl-CoA dehydrogenase (β-HAD) activities in muscle biopsies. Clinical improvement was assessed according to the International Myositis Assessment and Clinical Studies Group (IMACS) improvement criteria. All assessors were blinded to the type of intervention (that is, training or control).

Results

Exercise performance and aerobic capacity were lower in patients than in healthy controls, whereas lactate levels at exhaustion were similar. Patients in the exercise group increased their cycling time, aerobic capacity and CS and β-HAD activities, whereas lactate levels at exhaustion decreased. Six of nine patients in the exercise group met the IMACS improvement criteria. Patients in the control group did not show any consistent changes during the 12-week study.

Conclusions

Polymyositis and dermatomyositis patients have impaired endurance, which could be improved by 12 weeks of endurance training. The clinical improvement corresponds to increases in aerobic capacity and muscle mitochondrial enzyme activities. The results emphasize the importance of endurance exercise in addition to immunosuppressive treatment of patients with polymyositis or dermatomyositis.

Trial registration

ClinicalTrials.gov: {"type":"clinical-trial","attrs":{"text":"NCT01184625","term_id":"NCT01184625"}}NCT01184625     

Displays of the Honeyeater Manorina melanocephala

Investigated displays of Noisy Miners, Manorina melanocephala, in Australia. This unusual bird lives in colonies and many ♂♂ care for the offspring of each ♀ flight displays, 11 non-flight displays, and several components of facial displays (including a variable eye patch) are described. The eye patch provides a large yellow and black augmented eye, important in intimidation. No stereotyped sequence of courtship behaviour precedes copulation. Displays are used to advertise nest locations. A greeting display, the corrohoree, is extremely common. The possibility of the evolution of submissive display from threat is discussed. Special vocalisations of ♂♂ and ♀♀ are use in a duet. The maintenance of bonds among many individuals in a colony may be more important than strong pair bonds. Group cohesion is probably maintained by flight display, nest display, mobbing, and other communal activities. High interspecific aggression results in few resident species in colonies. This level of interspecific aggression might be maintained by incorporating much intraspecific mimetic display and ritualised submissive behaviour.     

Individual and sibling-group variation in metabolism of lizards: The aerobic capacity model for the origin of endothermy

• 1.1. We measured standard, resting and exercise metabolism of 28 Chaicides ocellatus (Scincidae). Individual lizards consistently showed statistically significant differences in mass-independent rates of standard and exercise metabolism during three replicates of the experiments at weekly intervals.
• 2.2. Metabolic differences were also detected among groups of siblings.
• 3.3. Mass-independent resting metabolic rates were closely correlated with standard rates, but there was no correlation of metabolic rates during forced activity with either standard or resting rates.
• 4.4. These data suggest a heritable component of metabolism for lizards, but they do not support the “aerobic capacity model” of the origin of endothermy, which proposes that initial selection for high resting metabolic rates operated via selection for high rates of aerobic metabolism during exercise.