Artificial light at night alters diurnal and nocturnal behavior and physiology in green anole lizards.

Artificial light at night (ALAN) disrupts biological rhythms across widely diverse organisms. To determine how energy is allocated by animals in different light environments, we investigated the impacts of ALAN on behavior and physiology of diurnal green anole lizards (Anolis carolinensis). Two groups of 24 adult lizards (half males, half females) were maintained in a controlled lab setting for six weeks. One group was exposed to a simulated natural summer light-dark cycle; the other was exposed to ALAN that simulated urban, nocturnal light exposure. After an acclimation period, we conducted four behavioral trials. One trial examined behavioral time allocation over two 24 h periods, and three others were conducted during mid-day and mid-night: open field tests, to examine exploratory behavior; foraging trials, to examine prey consumption; and social interaction trials, to examine same-sex interactions. We then measured each lizard's snout-vent length and mass of its body, abdominal fat pads, liver, and, for males, testes. Lizards exposed to ALAN were more likely to be awake at night, using nocturnal light to explore, forage, and display to conspecifics. However, during the day, ALAN lizards were less likely to be awake, slower to move, and females displayed less frequently. ALAN lizards had heavier fat pads and testes, but ALAN did not impact body mass, liver mass, or snout-vent length. In sum, ALAN appears to cause a broad shift towards increased nocturnal activity and may alter metabolic and reproductive processes. Future work should examine the fitness consequences of these behavioral and physiological changes.

Adaptive seasonal shift towards investment in fewer, larger offspring: Evidence from field and laboratory studies.

Seasonal changes in reproduction have been described for many taxa. As reproductive seasons progress, females often shift from greater energetic investment in many small offspring towards investing less total energy into fewer, better provisioned (i.e. larger) offspring. The underlying causes of this pattern have not been assessed in many systems. Two primary hypotheses have been proposed to explain these patterns. The first is an adaptive hypothesis from life-history theory: early offspring have a survival advantage over those produced later. Accordingly, selection favours females that invest in offspring quantity early in the season and offspring quality later. The second hypothesis suggests these patterns are not intrinsic but result from passive responses to seasonal changes in the environment experienced by reproducing females (i.e. maternal environment). To disentangle the causes underlying this pattern, which has been reported in brown anole lizards (Anolis sagrei), we performed complementary field and laboratory studies. The laboratory study carefully controlled maternal environments and quantified reproductive patterns throughout the reproductive season for each female. The field study measured similar metrics from free ranging lizards across an entire reproductive season. In the laboratory, females increased relative effort per offspring as the reproductive season progressed; smaller eggs were laid earlier, larger eggs were laid later. Moreover, we observed significant among-individual variation in seasonal changes in reproduction, which is necessary for traits to evolve via natural selection. Because these patterns consistently emerge under controlled laboratory conditions, they likely represent an intrinsic and potentially adaptive adjustment of reproductive effort as predicted by life-history theory. The field study revealed similar trends, further suggesting that intrinsic patterns observed in the laboratory are strong enough to persist despite the environmental variability that characterizes natural habitats. The observed patterns are indicative of an adaptive seasonal shift in parental investment in response to a deteriorating offspring environment: allocating greater resources to late-produced offspring likely enhances maternal fitness.

Artificial light at night increases growth and reproductive output in Anolis lizards.

Since the invention of electric lighting, artificial light at night (ALAN) has become a defining, and evolutionary novel, feature of human-altered environments especially in cities. ALAN imposes negative impacts on many organisms, including disrupting endocrine function, metabolism, and reproduction. However, we do not know how generalized these impacts are across taxa that exploit urban environments. We exposed brown anole lizards, an abundant and invasive urban exploiter, to relevant levels of ALAN in the laboratory and assessed effects on growth and reproduction at the start of the breeding season. Male and female anoles exposed to ALAN increased growth and did not suffer increased levels of corticosterone. ALAN exposure induced earlier egg-laying, likely by mimicking a longer photoperiod, and increased reproductive output without reducing offspring quality. These increases in growth and reproduction should increase fitness. Anoles, and potentially other taxa, may be resistant to some negative effects of ALAN and able to take advantage of the novel niche space ALAN creates. ALAN and both its negative and positive impacts may play a crucial role in determining which species invade and exploit urban environments.

Obtaining plasma to measure baseline corticosterone concentrations in reptiles: How quick is quick enough?

There is growing interest in the use of glucocorticoid (GC) hormones to understand how wild animals respond to environmental challenges. Blood is the best medium for obtaining information about recent GC levels; however, obtaining blood requires restraint and can therefore be stressful and affect GC levels. There is a delay in GCs entering blood, and it is assumed that blood obtained within 3 min of first disturbing an animal reflects a baseline level of GCs, based largely on studies of birds and mammals. Here we present data on the timing of changes in the principle reptile GC, corticosterone (CORT), in four reptile species for which blood was taken within a range of times 11 min or less after first disturbance. Changes in CORT were observed in cottonmouths (Agkistrodon piscivorus; 4 min after first disturbance), rattlesnakes (Crotalus oreganus; 2 min 30 s), and rock iguanas (Cyclura cychlura; 2 min 44 s), but fence lizards (Sceloporus undulatus) did not exhibit a change within their 10-min sampling period. In both snake species, samples taken up to 3-7 min after CORT began to increase still had lower CORT concentrations than after exposure to a standard restraint stressor. The "3-min rule" appears broadly applicable as a guide for avoiding increases in plasma CORT due to handling and sampling in reptiles, but the time period in which to obtain true baseline CORT may need to be shorter in some species (rattlesnakes, rock iguanas), and may be unnecessarily limiting for others (cottonmouths, fence lizards).

Presence of an invasive species reverses latitudinal clines of multiple traits in a native species.

Understanding the processes driving formation and maintenance of latitudinal clines has become increasingly important in light of accelerating global change. Many studies have focused on the role of abiotic factors, especially temperature, in generating clines, but biotic factors, including the introduction of non-native species, may also drive clinal variation. We assessed the impact of invasion by predatory fire ants on latitudinal clines in multiple fitness-relevant traits-morphology, physiological stress responsiveness, and antipredator behavior-in a native fence lizard. In areas invaded by fire ants, a latitudinal cline in morphology is opposite both the cline found in museum specimens from historical populations across the species' full latitudinal range and that found in current populations uninvaded by fire ants. Similarly, clines in stress-relevant hormone response to a stressor and in antipredator behavior differ significantly between the portions of the fence lizard range invaded and uninvaded by fire ants. Changes in these traits within fire ant-invaded areas are adaptive and together support increased and more effective antipredator behavior that allows escape from attacks by this invasive predator. However, these changes may mismatch lizards to the environments under which they historically evolved. This research shows that novel biotic pressures can alter latitudinal clines in multiple traits within a single species on ecological timescales. As global change intensifies, a greater understanding of novel abiotic and biotic pressures and how affected organisms adapt to them across space and time will be central to predicting and managing our changing environment.

What Is Stress? A Systems Perspective.

The term "stress" is used to describe important phenomena at multiple levels of biological organization, but finding a general and rigorous definition of the concept has proven challenging. Current models in the behavioral literature emphasize the cognitive aspects of stress, which is said to occur when threats to the organism are perceived as uncontrollable and/or unpredictable. Here we adopt the perspective of systems biology and take a step toward a general definition of stress by unpacking the concept in light of control theory. Our goal is to clarify the concept so as to facilitate integrative research and formal analysis. We argue that stress occurs when a biological control system detects a failure to control a fitness-critical variable, which may be either internal or external to the organism. Biological control systems typically include both feedback (reactive, compensatory) and feedforward (predictive, anticipatory) components; their interplay accounts for the complex phenomenology of stress in living organisms. The simple and abstract definition we propose applies to animals, plants, and single cells, highlighting connections across levels of organization. In the final section of the paper we explore some extensions of our approach and suggest directions for future research. Specifically, we discuss the classic concepts of conditioning and hormesis and review relevant work on cellular stress responses; show how control theory suggests the existence of fundamental trade-offs in the design of stress responses; and point to potential insights into the effects of novel environmental conditions, including those resulting from anthropogenic change.

Are Invasive Species Stressful? The Glucocorticoid Profile of Native Lizards Exposed to Invasive Fire Ants Depends on the Context.

Invasive species represent a substantial threat to native species worldwide. Research on the impacts of invasive species on wild living vertebrates has focused primarily on population-level effects. The sublethal, individual-level effects of invaders may be equally important but are poorly understood. We investigated the effects of invasive fire ants (Solenopsis invicta) on the physiological stress response of a native lizard (Sceloporus undulatus) within two experimental contexts: directly exposing lizards to a fire ant attack and housing lizards with fire ants in seminatural field enclosures. Lizards directly exposed to brief attack by fire ants had elevated concentrations of the stress hormone corticosterone (CORT), suggesting that these encounters can be physiologically stressful. However, lizards exposed for longer periods to fire ants in field enclosures had lower concentrations of CORT. This may indicate that the combined effects of confinement and fire ant exposure have pushed lizards into allostatic overload. However, lizards from fire ant enclosures appeared to have intact negative feedback controls of the stress response, evidenced by functioning adrenocorticotropic hormone responsiveness and lack of suppression of innate immunity (plasma bactericidal capacity). We review previous studies examining the stress response of wild vertebrates to various anthropogenic stressors and discuss how these-in combination with our results-underscore the importance of considering context (the length, frequency, magnitude, and types of threat) when assessing these impacts.

Irresistible ants: exposure to novel toxic prey increases consumption over multiple temporal scales.

As species become increasingly exposed to novel challenges, it is critical to understand how evolutionary (i.e., generational) and plastic (i.e., within lifetime) responses work together to determine a species' fate or predict its distribution. The introduction of non-native species imposes novel pressures on the native species that they encounter. Understanding how native species exposed to toxic or distasteful invaders change their feeding behavior can provide insight into their ability to cope with these novel threats as well as broader questions about the evolution of this behavior. We demonstrated that native eastern fence lizards do not avoid consuming invasive fire ants following repeated exposure to this toxic prey. Rather fence lizards increased their consumption of these ants following exposure on three different temporal scales. Lizards ate more fire ants when they were exposed to this toxic prey over successive days. Lizards consumed more fire ants if they had been exposed to fire ants as juveniles 6 months earlier. Finally, lizards from populations exposed to fire ants over multiple generations consumed more fire ants than those from fire ant-free areas. These results suggest that the potentially lethal consumption of fire ants may carry benefits resulting in selection for this behavior, and learning that persists long after initial exposure. Future research on the response of native predators to venomous prey over multiple temporal scales will be valuable in determining the long-term effects of invasion by these novel threats.

Epigenetic response to environmental change: DNA methylation varies with invasion status.

Epigenetic mechanisms may be important for a native species' response to rapid environmental change. Red Imported Fire Ants (Solenopsis invicta Santschi, 1916) were recently introduced to areas occupied by the Eastern Fence Lizard (Sceloporus undulatus Bosc & Daudin, 1801). Behavioral, morphological and physiological phenotypes of the Eastern Fence Lizard have changed following invasion, creating a natural biological system to investigate environmentally induced epigenetic changes. We tested for variation in DNA methylation patterns in Eastern Fence Lizard populations associated with different histories of invasion by Red Imported Fire Ants. At methylation sensitive amplified fragment length polymorphism loci, we detected a higher diversity of methylation in Eastern Fence Lizard populations from Fire Ant uninvaded versus invaded sites, and uninvaded sites had higher methylation. Our results suggest that invasive species may alter methylation frequencies and the pattern of methylation among native individuals. While our data indicate a high level of intrinsic variability in DNA methylation, DNA methylation at some genomic loci may underlie observed phenotypic changes in Eastern Fence Lizard populations in response to invasion of Red Imported Fire Ants. This process may be important in facilitating adaptation of native species to novel pressures imposed by a rapidly changing environment.