Manganese Exacerbates Seasonal Health Declines in a Suicidally Breeding Mammal.

Reproductive costs must be balanced with survival to maximize lifetime reproductive rates; however, some organisms invest in a single, suicidal bout of breeding known as semelparity. The northern quoll (Dasyurus hallucatus) is an endangered marsupial in which males, but not females, are semelparous. Northern quolls living near mining sites on Groote Eylandt, Northern Territory, Australia, accumulate manganese (Mn) in their brains, testes, and hair, and elevated Mn impacts motor performance. Whether Mn is associated with other health declines is yet unknown. In the present study we show that male and female northern quolls with higher Mn accumulation had a 20% reduction in immune function and a trend toward reduced cortisol concentrations in hair. The telomere lengths of male quolls did not change pre- to postbreeding, but those with higher Mn levels had longer telomeres; in contrast, the telomeres of females shortened during the breeding season but recovered between the first year and second year of breeding. In addition, the telomeres of quolls that were recaptured declined at significantly higher rates in quolls with higher Mn between prebreeding, breeding, and/or postbreeding seasons. Future research should determine whether changes in cortisol, immune function, or telomere length affect reproductive output or survival-particularly for semelparous males. Environ Toxicol Chem 2024;43:74-86. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Pre-cleaning of hair is not beneficial in LA-ICP-MS studies of chronic metal exposure.

Chronic exposure to toxic metals is a serious global health concern. However, population-wide biomonitoring is costly and carries several sampling constraints. Though hair sampling can be a useful way to assess environmental exposure, external contamination is a long-standing concern, and a pre-cleaning step prior to metal quantification has long been recommended despite a lack of evidence for its efficacy. In this study, we quantified the spatial distribution of 16 elements in unwashed human hair samples using Laser Ablation Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS), then tested how two common pre-cleaning treatments (Triton-ethanol, Triton-nitric acid) affected metal content in external and interior layers of hair using LA-ICP-MS. We show that elements differ in their spatial distribution across hair and that pre-cleaning is not consistent in its effect on element concentrations and decreases interior concentrations of some elements. We demonstrate that differences among individuals can be quantified reliably with LA-ICP-MS analysis of interior concentrations of unwashed hair. Our study tests the widespread notion that pre-cleaning is essential in analyses of hair for environmental exposure to metals, and examines the benefits of a unified approach to analysis of metals in hair using LA-ICP-MS.

Modeling escape success in terrestrial predator-prey interactions.

Prey species often modify their foraging and reproductive behaviors to avoid encounters with predators; yet once they are detected, survival depends on out-running, out-maneuvering, or fighting off the predator. Though predation attempts involve at least two individuals-namely, a predator and its prey-studies of escape performance typically measure a single trait (e.g., sprint speed) in the prey species only. Here, we develop a theoretical model in which the likelihood of escape is determined by the prey animal's tactics (i.e., path trajectory) and its acceleration, top speed, agility, and deceleration relative to the performance capabilities of a predator. The model shows that acceleration, top speed, and agility are all important determinants of escape performance, and because speed and agility are biomechanically related to size, smaller prey with higher agility should force larger predators to run along curved paths that do not allow them to use their superior speeds. Our simulations provide clear predictions for the path and speed a prey animal should choose when escaping from predators of different sizes (thus, biomechanical constraints) and could be used to explore the dynamics between predators and prey.

Manganese contamination affects the motor performance of wild northern quolls (Dasyurus hallucatus).

Neuromotor deficits are an important sign of manganese (Mn) toxicity in humans and laboratory animals. However, the impacts of Mn exposure on the motor function of wild animals remains largely unknown. Here, we assessed the impact of chronic exposure to Mn from active mining operations on Groote Eylandt, Australia on the motor function of the semi-arboreal northern quoll (Dasyurus hallucatus), an endangered species. The three motor tests conducted-maximum sprint speed on a straight run, manoeuvrability around a corner, and motor control on a balance beam-showed that elevated Mn body burden did not diminish performance of these traits. However, quolls with higher Mn body burden approached a corner at a significantly narrower range of speeds, due to a significantly lower maximum approach speed. Slower speeds approaching a turn may reduce success at catching prey and avoiding predators. Given that maximum sprint speed on a straight run was not affected by Mn body burden, but maximum speed entering a corner was, slower speeds approaching a turn may reflect compensation for otherwise impaired performance in the turn.

Surface friction alters the agility of a small Australian marsupial.

Movement speed can underpin an animal's probability of success in ecological tasks. Prey often use agility to outmanoeuvre predators; however, faster speeds increase inertia and reduce agility. Agility is also constrained by grip, as the foot must have sufficient friction with the ground to apply the forces required for turning. Consequently, ground surface should affect optimum turning speed. We tested the speed-agility trade-off in buff-footed antechinus (Antechinus mysticus) on two different surfaces. Antechinus used slower turning speeds over smaller turning radii on both surfaces, as predicted by the speed-agility trade-off. Slipping was 64% more likely on the low-friction surface, and had a higher probability of occurring the faster the antechinus were running before the turn. However, antechinus compensated for differences in surface friction by using slower pre-turn speeds as their amount of experience on the low-friction surface increased, which consequently reduced their probability of slipping. Conversely, on the high-friction surface, antechinus used faster pre-turn speeds in later trials, which had no effect on their probability of slipping. Overall, antechinus used larger turning radii (0.733±0.062 versus 0.576±0.051 m) and slower pre-turn (1.595±0.058 versus 2.174±0.050 m s-1) and turning speeds (1.649±0.061 versus 2.01±0.054 m s-1) on the low-friction surface. Our results demonstrate the interactive effect of surface friction and the speed-agility trade-off on speed choice. To predict wild animals' movement speeds, future studies should examine the interactions between biomechanical trade-offs and terrain, and quantify the costs of motor mistakes in different ecological activities.

Manganese accumulates in the brain of northern quolls (Dasyurus hallucatus) living near an active mine.

Mining is fundamental to the Australian economy, yet little is known about how potential contaminants bioaccumulate and affect wildlife living near active mining sites. Here, we show using air sampling that fine manganese dust within the respirable size range is found at levels exceeding international recommendations even 20 km from manganese extraction, processing, and storage facilities on Groote Eylandt, Northern Territory. Endangered northern quolls (Dasyurus hallucatus) living near mining sites were found to have elevated manganese concentrations within their hair, testes, and in two brain regions-the neocortex and cerebellum, which are responsible for sensory perception and motor function, respectively. Accumulation in these organs has been associated with adverse reproductive and neurological effects in other species and could affect the long-term population viability of northern quolls.

Skill not athleticism predicts individual variation in match performance of soccer players.

Just as evolutionary biologists endeavour to link phenotypes to fitness, sport scientists try to identify traits that determine athlete success. Both disciplines would benefit from collaboration, and to illustrate this, we used an analytical approach common to evolutionary biology to isolate the phenotypes that promote success in soccer, a complex activity of humans played in nearly every modern society. Using path analysis, we quantified the relationships among morphology, balance, skill, athleticism and performance of soccer players. We focused on performance in two complex motor activities: a simple game of soccer tennis (1 on 1), and a standard soccer match (11 on 11). In both contests, players with greater skill and balance were more likely to perform better. However, maximal athletic ability was not associated with success in a game. A social network analysis revealed that skill also predicted movement. The relationships between phenotypes and success during individual and team sports have potential implications for how selection acts on these phenotypes, in humans and other species, and thus should ultimately interest evolutionary biologists. Hence, we propose a field of evolutionary sports science that lies at the nexus of evolutionary biology and sports science. This would allow biologists to take advantage of the staggering quantity of data on performance in sporting events to answer evolutionary questions that are more difficult to answer for other species. In return, sports scientists could benefit from the theoretical framework developed to study natural selection in non-human species.

Daylight saving time can decrease the frequency of wildlife-vehicle collisions.

Daylight saving time (DST) could reduce collisions with wildlife by changing the timing of commuter traffic relative to the behaviour of nocturnal animals. To test this idea, we tracked wild koalas (Phascolarctos cinereus) in southeast Queensland, where koalas have declined by 80% in the last 20 years, and compared their movements with traffic patterns along roads where they are often killed. Using a simple model, we found that DST could decrease collisions with koalas by 8% on weekdays and 11% at weekends, simply by shifting the timing of traffic relative to darkness. Wildlife conservation and road safety should become part of the debate on DST.

Multivariate analyses of individual variation in soccer skill as a tool for talent identification and development: utilising evolutionary theory in sports science.

The development of a comprehensive protocol for quantifying soccer-specific skill could markedly improve both talent identification and development. Surprisingly, most protocols for talent identification in soccer still focus on the more generic athletic attributes of team sports, such as speed, strength, agility and endurance, rather than on a player's technical skills. We used a multivariate methodology borrowed from evolutionary analyses of adaptation to develop our quantitative assessment of individual soccer-specific skill. We tested the performance of 40 individual academy-level players in eight different soccer-specific tasks across an age range of 13-18 years old. We first quantified the repeatability of each skill performance then explored the effects of age on soccer-specific skill, correlations between each of the pairs of skill tasks independent of age, and finally developed an individual metric of overall skill performance that could be easily used by coaches. All of our measured traits were highly repeatable when assessed over a short period and we found that an individual's overall skill - as well as their performance in their best task - was strongly positively correlated with age. Most importantly, our study established a simple but comprehensive methodology for assessing skill performance in soccer players, thus allowing coaches to rapidly assess the relative abilities of their players, identify promising youths and work on eliminating skill deficits in players.

How Fast Should an Animal Run When Escaping? An Optimality Model Based on the Trade-Off Between Speed and Accuracy.

How fast should animals move when trying to survive? Although many studies have examined how fast animals can move, the fastest speed is not always best. For example, an individual escaping from a predator must run fast enough to escape, but not so fast that it slips and falls. To explore this idea, we developed a simple mathematical model that predicts the optimal speed for an individual running from a predator along a straight beam. A beam was used as a proxy for straight-line running with severe consequences for missteps. We assumed that success, defined as reaching the end of the beam, had two broad requirements: (1) running fast enough to escape a predator, and (2) minimizing the probability of making a mistake that would compromise speed. Our model can be tailored to different systems by revising the predator's maximal speed, the prey's stride length and motor coordination, and the dimensions of the beam. Our model predicts that animals should run slower when the beam is narrower or when coordination is worse.

Does individual quality mask the detection of performance trade-offs? A test using analyses of human physical performance.

Why are performance trade-offs so rarely detected in animals when their underlying physiological basis seems so intuitive? One possibility is that individual variation in health, fitness, nutrition, development or genetics, or 'individual quality', makes some individuals better or worse performers across all motor tasks. If this is the case, then correcting for individual quality should reveal functional trade-offs that might otherwise be overlooked. We tested this idea by exploring trade-offs in maximum physical performance and motor skill function in semi-professional soccer players. We assessed individual performance across five maximum 'athletic' tasks providing independent measures of power, stamina and speed, as well as five soccer-specific 'motor skill' tasks providing independent measures of foot control. We expected to find functional trade-offs between pairs of traits (e.g. endurance versus power/speed tasks or specialist-generalist performance) - but only after correcting for individual quality. Analyses of standardised raw data found positive associations among several pairs of traits, but no evidence of performance trade-offs. Indeed, peak performance across a single athletic task (degree of specialisation) was positively associated with performance averaged across all other athletic tasks (generalist). However, after accounting for an individual's overall quality, several functional trade-offs became evident. Within our quality-corrected data, 1500 m-speed (endurance) was negatively associated with squat time (power), jump distance (power) and agility speed - reflecting the expected speed-endurance trade-off; and degree of specialisation was negatively associated with average performance across tasks. Taken together, our data support the idea that individual variation in general quality can mask the detection of performance trade-offs at the whole-animal level. These results highlight the possibility that studies may spuriously conclude certain functional trade-offs are unimportant or non-existent when analyses that account for variation in general quality may reveal their cryptic presence.

Dehydration hardly slows hopping toads (Rhinella granulosa) from xeric and mesic environments.

The locomotor capacity of amphibians depends strongly on temperature and hydration. Understanding the potential interactions between these variables remains an important challenge because temperature and water availability covary strongly in natural environments. We explored the effects of temperature and hydration on the hopping speeds of Rhinella granulosa, a small toad from the semiarid Caatinga and the Atlantic Rain Forest in Brazil. We asked whether thermal and hydric states interact to determine performance and whether toads from the Caatinga differ from their conspecifics from the Atlantic Forest. Both dehydration and cooling impaired hopping speed, but effects were independent of one another. In comparison to performances of other anurans, the performance of R. granulosa was far less sensitive to dehydration. Consequently, dehydrated members of this species may be able to sustain performance through high body temperatures, which agrees with the exceptional heat tolerance of this species. Surprisingly, toads from both the Caatinga and the Atlantic Forest were relatively insensitive to dehydration. This observation suggests that migration or gene flow between toads from the forest and those from a drier region occurred or that toads from a dry region colonized the forest secondarily.

Predicting the physiological performance of ectotherms in fluctuating thermal environments.

Physiological ecologists have long sought to understand the plasticity of organisms in environments that vary widely among years, seasons and even hours. This is now even more important because human-induced climate change is predicted to affect both the mean and variability of the thermal environment. Although environmental change occurs ubiquitously, relatively few researchers have studied the effects of fluctuating environments on the performance of developing organisms. Even fewer have tried to validate a framework for predicting performance in fluctuating environments. Here, we determined whether reaction norms based on performance at constant temperatures (18, 22, 26, 30 and 34°C) could be used to predict embryonic and larval performance of anurans at fluctuating temperatures (18-28°C and 18-34°C). Based on existing theory, we generated hypotheses about the effects of stress and acclimation on the predictability of performance in variable environments. Our empirical models poorly predicted the performance of striped marsh frogs (Limnodynastes peronii) at fluctuating temperatures, suggesting that extrapolation from studies conducted under artificial thermal conditions would lead to erroneous conclusions. During the majority of ontogenetic stages, growth and development in variable environments proceeded more rapidly than expected, suggesting that acute exposures to extreme temperatures enable greater performance than do chronic exposures. Consistent with theory, we predicted performance more accurately for the less variable thermal environment. Our results underscore the need to measure physiological performance under naturalistic thermal conditions when testing hypotheses about thermal plasticity or when parameterizing models of life-history evolution.

Fall field crickets did not acclimate to simulated seasonal changes in temperature.

In nature, many organisms alter their developmental trajectory in response to environmental variation. However, studies of thermal acclimation have historically involved stable, unrealistic thermal treatments. In our study, we incorporated ecologically relevant treatments to examine the effects of environmental stochasticity on the thermal acclimation of the fall field cricket (Gryllus pennsylvanicus). We raised crickets for 5 weeks at either a constant temperature (25°C) or at one of three thermal regimes mimicking a seasonal decline in temperature (from 25 to 12°C). The latter three treatments differed in their level of thermal stochasticity: crickets experienced either no diel cycle, a predictable diel cycle, or an unpredictable diel cycle. Following these treatments, we measured several traits considered relevant to survival or reproduction, including growth rate, jumping velocity, feeding rate, metabolic rate, and cold tolerance. Contrary to our predictions, the acclimatory responses of crickets were unrelated to the magnitude or type of thermal variation. Furthermore, acclimation of performance was not ubiquitous among traits. We recommend additional studies of acclimation in fluctuating environments to assess the generality of these findings.

Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate metabolic performance to thermal variability.

Human-induced climate change is predicted to affect not only the mean temperature of the environment but also the variability and frequency of extreme climatic events. Variability in an organism's developmental environment has the potential to markedly affect an individual's growth trajectory and physiological function, leading to impacts on individual fitness and population dynamics. Thus, it is important to consider the consequences of thermal variability on developing organisms and understand their capacity to respond to such increased variation. We investigated the capacity of larval striped marsh frogs (Limnodynastes peronii) to initiate a response to increases in the thermal variability of their developmental environment by reducing the sensitivity of their physiological rate functions to changes in temperature. In variable environments, we expected the thermal sensitivity of rate functions to decrease and their performance breadth to widen so as to buffer the effect of thermal variability. We raised larvae in stable (24°C), narrowly variable (22-26°C; mean 24°C) and widely variable (14-34°C; mean 24°C) thermal environments and measured the thermal sensitivity of their locomotor performance, heart rate, oxygen consumption and activities of two metabolic enzymes, lactate dehydrogenase and cytochrome c oxidase. We found that the temperature-dependent relationships of these physiological functions did not differ between tadpoles raised in stable or variable thermal conditions. Furthermore, the Q(10) values of each response variable were virtually unaffected by treatment when measured over the entire thermal range. Our results reveal that larval amphibians exhibit little plasticity in metabolic traits to thermal variability. This lack of plasticity may have important implications for the growth and population dynamics of organisms in environments that are beginning to experience increased thermal variability.

Females prefer athletes, males fear the disadvantaged: different signals used in female choice and male competition have varied consequences.

The most commonly assumed cost for exaggerated male ornamentation is increased predation pressure owing to decreased locomotor performance or increased conspicuousness to predators. Despite its intuitive basis, the locomotor costs of male ornamentation are not well established. We tested the hypothesis that multiple male signals that are used independently during female choice and male competition could lead to varied locomotor costs. Multiple signals with varied costs could provide a more detailed indicator of overall male quality, as only the highest-quality individuals could support all costs. To test this idea, we investigated the burst locomotor consequences of multiple ornaments for males of the pacific blue-eye (Pseudomugil signifer). We evaluated five competing models relating body size, ornament size and performance traits to field measures of dominance and attractiveness. Non-propulsive male fin ornaments used during male competition were different from those used in female choice. First dorsal fin length was the most important predictor of male attractiveness, while dominance was only associated with anal fin length. Furthermore, first dorsal fin length was positively correlated with swim speed, while anal fin length was negatively associated with speed. Our study shows that multiple male signals that are used independently during male competition and female choice also differ in their associated costs. This provides a mechanism for understanding why locomotor costs for exaggerated male ornamentation are not often empirically demonstrated.

Urban physiology: city ants possess high heat tolerance.

Urbanization has caused regional increases in temperature that exceed those measured on a global scale, leading to urban heat islands as much as 12 degrees C hotter than their surroundings. Optimality models predict ectotherms in urban areas should tolerate heat better and cold worse than ectotherms in rural areas. We tested these predications by measuring heat and cold tolerances of leaf-cutter ants from South America's largest city (São Paulo, Brazil). Specifically, we compared thermal tolerances of ants from inside and outside of the city. Knock-down resistance and chill-coma recovery were used as indicators of heat and cold tolerances, respectively. Ants from within the city took 20% longer to lose mobility at 42 degrees C than ants from outside the city. Interestingly, greater heat tolerance came at no obvious expense of cold tolerance; hence, our observations only partially support current theory. Our results indicate that thermal tolerances of some organisms can respond to rapid changes in climate. Predictive models should account for acclimatory and evolutionary responses during climate change.

Short- and long-term consequences of thermal variation in the larval environment of anurans.

1. To survive adverse or unpredictable conditions in the ontogenetic environment, many organisms retain a level of phenotypic plasticity that allows them to meet the challenges of rapidly changing conditions. Larval anurans are widely known for their ability to modify behaviour, morphology and physiological processes during development, making them an ideal model system for studies of environmental effects on phenotypic traits. Although temperature is one of the most important factors influencing the growth, development and metamorphic condition of larval anurans, many studies have failed to include ecologically relevant thermal fluctuations among their treatments. 2. We compared the growth and age at metamorphosis of striped marsh frogs Limnodynastes peronii raised in a diurnally fluctuating thermal regime and a stable regime of the same mean temperature. We then assessed the long-term effects of the larval environment on the morphology and performance of post-metamorphic frogs. 3. Larval L. peronii from the fluctuating treatment were significantly longer throughout development and metamorphosed about 5 days earlier. Frogs from the fluctuating group metamorphosed at a smaller mass and in poorer condition compared with the stable group, and had proportionally shorter legs. 4. Frogs from the fluctuating group showed greater jumping performance at metamorphosis and less degradation in performance during a 10-week dormancy. Treatment differences in performance could not be explained by whole-animal morphological variation, suggesting improved contractile properties of the muscles in the fluctuating group.

Interannual differences in the relative timing of southward migration of male and female western sandpipers (Calidris mauri).

In the shorebird subfamily Calidridinae, one of the parents shortens parental care and initiates southward migration before the other. We estimated the difference in passage date between male and female western sandpipers (Calidris mauri) at their first major stopover on the southward migration from breeding areas in Alaska, in 18 years between 1978 and 2000. Overall, adult females preceded adult males by 1.22 days. A novel finding was that among juveniles, which migrate approximately a month later than adults, females preceded males by similar magnitude (1.14 days). There was wide variation among years, however, and males actually preceded females in years with late hatch. We relate these findings to hypotheses for female-first southward migration in sandpipers.